Extensively managed grasslands, particularly in mountain regions,
are considered to be one of the most diverse agroecosystems worldwide. Their
decline due to land use abandonment affects the diversity of both plants and
associated pollinators. Extensive grasslands constitute an important habitat
type and food resource for hoverflies (syrphids); however, not much is known
about the effects of abandonment on this important pollinator group. In the
present study, we investigated how abandonment affects species richness and the
composition of syrphids in mountainous meadows. We recorded the richness of
vascular plants, vegetation cover, flower cover and the surrounding
landscape to examine whether and how syrphids are affected by plant and
landscape parameters. We investigated the species richness, abundance and
species composition of syrphids by sweep netting and by using observation
plots in 18 semidry meadows across two Austrian regions and one Swiss region. For
each region, we selected three meadows abandoned for more than 20 years and three
annually mown non-fertilized meadows. Abandonment or mowing had no
significant effect on the total number of syrphid species or individuals or on the number of aphidophagous and non-aphidophagous species and individuals.
However, the total number of species and the number of non-aphidophagous species
significantly increased with the increasing number of plant species. The
surrounding landscape and other plant parameters showed no association with
the assessed syrphid parameters. Although syrphids were unaffected by
abandonment, higher syrphid species numbers in response to a higher plant
richness in annual mown meadows suggest that the management of mountain meadows is beneficial in preserving syrphid richness.
Introduction
Seminatural grasslands are considered one of the most valuable
agroecosystems throughout Central European landscapes and are characterized
by a high biodiversity (Chytrý et al., 2015; Habel et al., 2013; Maurer
et al., 2006). In particular, extensive management by mowing or grazing is
an important management scheme to maintain these habitats of high nature
conservation value (Hansson and Fogelfors, 2000; Moog et al., 2002). Most of
these grassland habitats have a long history and were maintained by local
farmers for hay making and animal husbandry over hundreds of years (Chemini
and Rizzoli, 2003; Poschlod and WallisDeVries, 2002). Since their
conservation relies strongly on human land use activities, they are
considered seminatural habitats (Heijcman et al., 2013). Due to a
high economical pressure in recent decades, traditional management has
become more and more unviable (Hinojosa et al., 2016; McGinlay et al.,
2017). Thus, to increase the yield, new agricultural and cultivation
techniques were developed which have led to an intensification of grasslands in
favorable regions on the one hand and afforestation or abandonment in
marginal regions on the other hand (Graf et al., 2014; Tasser et al., 2007).
Besides economical reasons, ecological factors like slope inclination and
accessibility are important drivers for farmers' decisions to
cease management especially in mountainous landscapes (Tasser et al., 2007;
Rey Benayas et al., 2007; Strijker, 2005). Abandonment has led to an ongoing
decline of traditionally managed seminatural meadows, confining them to
small patches within the landscape (Graf et al., 2014). Successional
processes alter habitat conditions and have been leading to an increase in
dominant grass species and the establishment of trees and shrubs on formerly
managed meadows (Cremene et al., 2005; Diemer et al., 2001; Galvánek and
Lepš, 2008; Tasser and Tappeiner, 2002). Consequently, plant species
which demand regular management decline during this succession process
(Hülber et al., 2017; Pykälä et al., 2005). Thus, an important
research question is how insect populations might respond to changing
vegetation characteristics after abandonment.
Generally, the extent of how abandonment affects insects depends very much
on the considered insect groups (Bonari et al., 2017; Burel, 1991; Walcher
et al., 2017) and can even differ between species within the same taxon
(Jovičić et al., 2017). While some insect taxa benefit from the
altered structural and environmental conditions in abandoned meadows, e.g.,
ants (Azcárate and Peco, 2011; Wiezik et al., 2013) and grasshoppers
(Baur et al., 2006; Schirmel et al., 2011), recent studies showed
detrimental effects of abandonment on pollinators such as butterflies
(Öckinger et al., 2006) and bumblebees (Walcher et al., 2017).
Until now, the response of hoverflies (syrphids) to the abandonment of
extensively managed meadows in mountainous regions has been little studied.
Along with wild bees, syrphids are important pollinators of both wildflowers
and crops (Jauker and Wolters, 2008). They may also play a role as
pollinators in habitats which are unsuitable, for example, for wild and honey bees
(Jauker et al., 2009; Rader et al., 2016). Besides providing important
pollination services, hoverfly species whose larvae are aphidophagous
contribute strongly to the efficient control of aphid populations (Leroy et
al., 2014). Furthermore, hoverflies represent important bioindicators, which
makes them an important insect group to study the effects of land use
changes (Burgio and Sommagio, 2007).
In a study investigating hoverfly communities in regularly mown and
abandoned mountainous grasslands, extensively managed meadows contained
a higher number of hoverfly individuals compared to abandoned meadows
(Hussain et al., 2017). Furthermore, the study found a positive relationship between
flower cover and plant richness with hoverfly abundance. However, it is
unclear whether these relationships vary among different regions. Thus, it
is important to collect and merge data from several mountainous regions to
obtain more generally valid results. Therefore, in the present study, we
analyzed the data of three regions including those reported by Hussain et
al. (2017). Analogous to their study, we tested the effects of abandonment,
vegetation parameters and further surrounding landscape parameters on
species richness and the abundance of syrphids in three regions across the Alps.
In addition to the former study, here we further distinguished between
species whose larvae have an aphidophagous of non-aphidophagous feeding mode.
In the present study, we expected a clear response of hoverflies to
abandonment due to altered vegetation characteristics, like decreasing plant
and flower resources, which in turn are important determinants of hoverfly
richness and abundance (Haenke et al., 2009). The surrounding landscape was
included in the present study because it was reported to affect the number of
hoverflies in grassland ecosystems (e.g., Gittings et al., 2006; Power et al.,
2016).
We expected (i) different numbers of hoverfly species and individuals and a
different hoverfly species composition between management types. Furthermore, we
investigated (ii) whether and how hoverflies are affected by plant richness,
flower cover, the cover of the vegetation and the surrounding landscape.
Additionally, we investigated (iii) the effects of abandonment and plant
and landscape parameters on both aphidophagous and non-aphidophagous
hoverflies.
Investigations were carried out in June and August 2015. Altogether, 18
mountainous meadows in the Austrian and Swiss Alps were investigated. Two
regions were located in Austria (central Ennstal and Großes Walsertal)
and one region in Switzerland (Val Müstair) (Fig. 1). Investigations
in the central Ennstal region were carried out in the municipalities of Sankt Gallen, Stainach and Pürgg, in Großes Walsertal in the municipality of
Sonntag/Buchboden, and in the Val Müstair region in the municipalities of
Valchava, St. Maria and Tschierv. The central Ennstal region is located in
the Austrian federal state of Styria ranging from the Gesäuse national park in the east to Grimming mountain in the west. The meadows were situated at
altitudes between 690 and 770 m above sea level (a.s.l.). Großes Walsertal is
a biosphere reserve located in the Austrian federal state of Vorarlberg.
Meadows were situated at altitudes between 1170 and 1280 m a.s.l. Val
Müstair in the canton of Graubünden is situated in the Eastern Alps of
Switzerland near the border with South Tyrol (Italy). Meadows in this
region were situated at altitudes between 1740 and 1800 m a.s.l. Detailed
information on the investigated meadows is shown in Table S1 in the Supplement. Within each region, six south-facing meadows were selected (n=18). Three
of the six meadows were annually mown and non-fertilized. The farmers
usually mow the meadows from the end of July to the beginning of August depending on
the annual weather conditions. Due to restricted accessibility with
mowing machines, the meadows are mown manually with sickle bar mowers. Three
of the six meadows had been abandoned for at least 20 years (Val Müstair
20 years, central Ennstal 20–40 years and Großes Walsertal 35–60 years since
abandonment). Before the cessation of management, the abandoned meadows were
annually mown and were never used as pastures. The annually mown meadows had
an average area of 3049 m2, and the abandoned meadows had an average
area of 1366 m2. The sizes of the abandoned and annually mown meadows
were not significantly different within each region (t test: central
Ennstal, p=0.295; Großes Walsertal, p=0.131; Müstair,
p=0.323).
Hoverfly sampling
We surveyed the number of hoverfly species and individuals once in mid-June and
once in mid-August 2015 and finished one round of investigations within 2 d per month in each region. We started sampling at 10:00 and stopped at
17:00 (all times are in Central European time). In this time period, we found that optimal sampling conditions were a
minimum temperature of 20 ∘C, dry vegetation and sunshine.
In order to increase sampling efficacy, we assessed the number of hoverfly
species and individuals by sweep net sampling and an observation plot method
(Hussain et al., 2018). Especially the observation plot method has been
shown to increase the number of collected species and individuals (Hussain et
al., 2018). Syrphid data from the central Ennstal region (Eisenwurzen) for
June and August 2015 were provided by Hussain et al. (2017) who used the
same sampling methods. Sweep net sampling was performed along three
15 m long and 2 m wide transects which were selected in the center of each
meadow. Thus, we covered a sampling area of 90 m2. The distances
between the transects were 10 m. We used a sweep net consisting of a white
cloth (40 cm opening diameter, 70 cm length). We conducted 30 sweeps per
transect summing up to 90 sweeps per meadow. The contents of the sweep net
were emptied after 30 sweeps and collected insects were killed with ethyl
acetate and stored in previously prepared and labeled plastic vials.
The sorting of hoverflies was carried out in the laboratory. Hoverflies were
stored in glass vials filled with 70 % ethanol.
In addition to the sweep net method, we applied an observation plot method
in which we observed four 2 m2 plots each for 15 min within every
meadow. The plots were distanced 3, 9 and 27 m from the first plot. The
starting plot was selected approximately in the center of each meadow to
avoid spillover effects from adjacent habitats. For the collection of single
species, we used an insect net (20 cm opening diameter, 20 cm length)
mounted on a handle 30 cm long. Syrphids entering an observation plot
were caught and stored in plastic vials. In the laboratory, hoverfly
individuals were preserved in glass vials in 70 % ethanol. For analysis,
we pooled the individuals caught by sweep netting and those caught during
the 15 min observations. Identification was performed using a binocular
microscope and identification literature by Stubbs and Falk (1983)
and van Veen (2010). For further analysis, we distinguished between
hoverflies whose larvae are aphidophagous or non-aphidophagous. We did not
consider hoverflies with saprophagous and phytophagous larvae separately due
to the low number of species. Larvae of these species are all considered
non-aphidophagous. The subdivision into feeding groups is an important aspect
because the aphidophagous feeding group most likely contributes to an
essential aphid control in nearby arable land. Thus, it is important to test
whether the observed meadows can enhance aphidophagous syrphid populations.
Vegetation and landscape parameters
The assessment of plant parameters was carried out in June and August 2015
within 2 d in each month. We recorded plant parameters within four
plots sized 1 m2. As with the plots for syrphid sampling, these plots
were situated in the center of the meadows. Within the plots, we identified
all plants to the species level and assessed vegetation cover and flower cover.
Besides living biomass, vegetation cover included necromass on the ground.
For further analysis, we determined the amount of plant species with flowers
having a flat corolla (hereafter designated as open nectar flowers, e.g.,
Ranunculaceae, Asteraceae and Apiaceae) because this flower type is an
important food source for hoverflies. Additionally, we measured the
surrounding landscape structure from orthophotos in ArcGIS (ArcGIS basemap).
Therefore, we measured the percentage of open land (containing, for example, meadows
and pastures in the surrounding) and forest (containing, for example, closed forest
and hedges) within a 500 m circle drawn around the center of each meadow. We
derived the vegetation and landscape data from the central Ennstal region
(Eisenwurzen) for June and August 2015 from Hussain et al. (2017).
Correlation between plant and landscape parameters. Significant
and marginally significant r and p values are pointed out in bold.
Plant species Vegetation cover Flower cover Open flowers Forest cover rp valuerp valuerp valuerp valuerp valueVegetation cover-0.220.375Flower cover0.660.003-0.51<0.001Open flowers0.77<0.0010.160.5130.420.084Forest cover-0.100.680-0.540.0200.400.103-0.260.298Open landscape-0.0380.8820.400.097-0.450.060-0.95<0.0010.0440.862Statistical analysis
We used generalized linear models (GLMs) for count data and Poisson error
distributions to analyze the effects of management and plant and landscape
parameters on hoverfly species and individuals and aphidophagous species and
individuals. We included the variable region as a fixed factor in the GLMs.
Before testing plant and landscape parameters in a GLM, we ran correlation
tests between them. Therefore, we first computed the corr.test function (R package
psych; Revelle, 2019) to receive p values and correlation coefficients (r). We
found certain correlations between plant and landscape parameters (Table 1).
Furthermore, to assess for multicollinearity between predictor variables
(management type and vegetation and landscape parameters), we computed the
variance inflation factors (VIFs) using the R package car (Fox et al., 2020). Any
variables with a VIF greater than 5 were removed from the models. Based on
these results, we computed our GLMs. We found that the predictor
variables of plant richness, flower cover, vegetation cover and open nectar
flowers could have been included in one model (all predictor variables with
a VIF less than 3) to evaluate their effects on hoverflies. To investigate the
effects of open landscape and forest, we analyzed both factors in a separate
model (VIF less than 5). Similarly, according to the VIF output, we also tested the
variable management type separately. We accounted for over- and
underdispersion of the data by computing the dispersion.test function in R (Kleiber and
Zeileis, 2018). In cases of over- or underdispersion, we corrected the
GLMs by using quasi-Poisson error distributions.
To avoid spatial autocorrelation, we performed the Moran's
test by applying the Moran.I function (Paradis et al., 2017) for each region
individually. Our analysis revealed no spatial autocorrelation between meadows
within each region (central Ennstal, p=0.678; Großes Walsertal,
p=0.339; Val Müstair, p=0.563).
We performed a principal coordinate analysis based on a Bray–Curtis
similarity matrix, to evaluate differences in hoverfly species composition
between meadow types. As with the GLM, we included the variable region as a
fixed factor. Possible significant differences in hoverfly species
composition between meadow types were tested with a permutational ANOVA (analysis of variance; PERMANOVA). We calculated p values using 9999 permutations of residuals under a reduced model.
We used version 6.1.13 of the software PRIMER including PERMANOVA+
(PRIMER-e Ltd., Plymouth, UK) to conduct the principal coordinate analysis
and PERMANOVA. We performed all other statistical analyses in R version 3.5.2 (R Core Team, 2018).
Generalized linear models (GLMs) showing the effects of plant and
landscape parameters on hoverfly species and individuals and on
aphidophagous and non-aphidophagous species and individuals. Significant
p values are shown in bold, and “df” signifies degrees of freedom.
Regression showing (a) the significant relationship between the number
of hoverfly species and the number of plant species and (b) the significant
relationship between the number of non-aphidophagous species and the number of plant
species in managed and abandoned meadows with a 95 % confidence interval.
Results
We collected 175 syrphid individuals belonging to 30 species (Table S2). A total of 25 species with 84 individuals were detected in managed meadows
and 18 species with 91 individuals in abandoned meadows. We distinguished
between 15 aphidophagous and 12 non-aphidophagous species. Six species
contributed to more than 75 % of the total individuals. These were
Melanostoma mellinum (26.3 %), Sphaerophoria scripta (14.3 %), Lapposyrphus lapponicus (12 %), Melanostoma scalare (11.43 %), Episyrphus balteatus (7.43 %) and Syritta pipiens (4 %).
Five species (Orthonevra geniculata, Parasyrphus annulatus, Platycheirus albimanus, Rhingia borealis and Sphegina sibirica) were only found in abandoned meadows; all other
species were found in both meadow types. Three species which could only be
identified to the genus level were not assigned to a feeding type. The total number
of hoverfly species and individuals did not significantly differ between
management types (GLM: p=0.158 and p=0.823, respectively), and this was
also true for the number of aphidophagous and non-aphidophagous species and
individuals (GLM: p=0.430 and p=0.130, respectively). The total number of
species significantly increased with the increasing number of plant species
(Fig. 2a; Table 2). Similarly, the number of non-aphidophagous species
increased with the increasing number of plant species (Fig. 2b; Table 2). All
other recorded plant and landscape parameters did not significantly affect the
number of species and individuals of syrphids, and they also had no influence on
the number of aphidophagous and non-aphidophagous species and individuals
(Table 2). Regarding species composition, there was no difference between
both meadow types (PERMANOVA: p=0.549), which is also graphically
represented in the principal coordinate analysis (PCO) (Fig. 3). Regarding plant parameters, the number of
vascular plant species was significantly higher in mown meadows (ANOVA:
F=16.31 and p<0.001). Flower cover and vegetation cover were higher
in mown compared to abandoned meadows (ANOVA: F=34.3 and p<0.001; F=6.52 and p=0.020, respectively). A species list of identified plant
species in the three study regions is attached in the Supplement
(Table S3).
Principal coordinate analysis (PCO) showing hoverfly species
composition in managed (▴) and abandoned (○) meadows.
Discussion
With 46 individuals, Melanostoma mellinum was by far the most abundant hoverfly species in the
present study. Furthermore, a higher abundance was made up of the eurytopic
species Sphaerophoria scripta, Lapposyrphus lapponicus and Melanostoma scalare. These species are highly migratory, which can lead to a higher
abundance in favorable years (Röder, 1990; Speight, 2014).
Regarding the total number of species and individuals, we found no differences
between both meadow types. Considering the habitat requirements, most of the
observed hoverfly species were eurytopic habitat generalists which use a
variety of different habitats (Röder, 1990; Speight, 2014), and it can
be assumed that both meadow types fulfilled hoverfly needs by providing
similar resources and facilitating suitable microhabitats for their
development. The most important factors which a habitat should provide for
hoverflies are the availability of suitable floral resources (Hennig and
Ghazoul, 2012; Moquet et al., 2018) and the presence of diverse larval
habitats (Jauker et al., 2009; Weiner et al., 2014). Similar to the total
number of species and abundance, the number of hoverfly species and individuals
belonging to the aphidophagous and non-aphidophagous feeding guilds did not
differ between meadow types. Especially the abundance of aphidophagous
hoverflies is mainly determined by the presence of suitable aphid hosts
(Almohamad et al., 2009). There is a very important contribution by Kök
et al. (2020) which focused on the tritrophic relationships between plants,
aphids and hoverflies. They found that plant species host different aphid
species which in turn are a suitable prey for the larvae of aphidophagous
hoverfly species like Sphaerophoria scripta and Episyrphus balteatus. This suggests that the choice of the habitats is
mainly driven by these relationships.
Consistent with the lack of differences of species richness and abundance,
we found a similar species composition in both meadow types. Only five
species were confined to abandoned meadows and all other species were found
in both meadow types. In contrast to, for example, bumblebees who have to provide
pollen for their offspring, adult hoverflies are highly mobile, free in
their dispersal (Meyer et al., 2009; Sutherland et al., 2001) and able to
track suitable flower resources among a wide range of habitats (Jauker et
al., 2009; Meyer et al., 2017).
The diversity of vascular plants turned out to be an important factor for
hoverflies. Both the number of total hoverfly species and the number of
non-aphidophagous species increased with an increasing plant richness. This
indicates that a high variety of plant resources is most beneficial in
maintaining hoverfly diversity in these grasslands (e.g., Meyer et al., 2009).
The status of a high plant richness can only be preserved through regular
extensive management. Grassland abandonment results in a decrease in plant
richness (Pykälä et al., 2005) and consequently would have negative
effects on hoverfly richness.
Surprisingly, we found no relationship between hoverflies and flower cover,
contradicting the results of other studies (Meyer et al., 2009; Frank, 1999;
Fründ et al., 2010; Power et al., 2016). However, our results are in line
with those of Hussain et al. (2017) who reported that flower cover had no
effect on syrphid richness and abundance. They mainly attributed this result
to the presence of more flowers which have a deep, non-accessible corolla
(e.g., Salvia pratensis and Rhinanthus minor), which is presumably also a good explanation for the findings in our
study. For example, only a few syrphid species from the genus Rhingia developed
specialized mouth parts to access the hidden nectar (Speight, 2014).
However, with the exception of Rhingia borealis, these species were absent in our meadows.
Another explanation for the missing relationship between flowers and
hoverflies could be that hoverflies also feed on the honeydew from aphids that
can be unrelated to the abundance of suitable flowers (van Rijn et al.,
2013).
Conclusion
Although there was no overall effect of abandonment on syrphid richness,
abundance and composition in the present study, plant richness turned out to
be an important determinant for syrphid diversity in the investigated
meadows, confirming also the results of other studies (e.g., Meyer et al.,
2009; Hussain et al., 2017). In turn, this high plant richness can only be
maintained by a regular extensive management. However, abandoned
meadows also have the potential to contribute to a high hoverfly diversity in
mountainous grasslands since some species were only found in abandoned
meadows. Our results suggest that the maintenance of a heterogenous
landscape containing both regularly mown and abandoned meadows is most
beneficial for the conservation of hoverfly diversity in mountainous
grasslands.
Data availability
The data used in this study are provided in the
Supplement.
The supplement related to this article is available online at: https://doi.org/10.5194/we-20-143-2020-supplement.
Author contributions
RW conducted field work, analyzed the data and wrote
the paper. RIH and DB sampled and identified collected syrphids. RIH
contributed hoverfly data from central Ennstal, and JK and AB recorded plant
parameters. AA, JGZ and TF were the project leaders who designed and
developed the “Healthy Alps” project. All authors reviewed the paper.
Competing interests
The authors declare that they have no conflict of interest.
Acknowledgements
We want to thank all the farmers and land owners for their
cooperation and for providing their meadows for our investigations.
Review statement
This paper was edited by Matthias Foellmer and reviewed by three anonymous referees.
Financial support
This research has been supported by the Austrian Academy of Sciences (project: Healthy Alps).
References
Almohamad, R., Verheggen, F. J., and Haubruge, E.: Searching and oviposition
behavior of aphidophagous hoverflies (Diptera: Syrphidae): a review,
Biotechnol. Agron. Soc. Environ., 13, 467–481, 2009.Azcárate, F. M. and Peco, B.: Abandonment of grazing in a mediterranean
grassland area: consequences for ant assemblages, Insect Conserv. Diver., 5,
279–288, 10.1111/j.1752-4598.2011.00165.x, 2011.Basemap.at: Verwaltungsgrundkarte von Österreich, available at: https://www.basemap.at, last access: April 2020.Baur, B., Cremene, C., Groza, G., Rakosy, L., Schileyko, A. A., Baur, A.,
Stoll, P., and Erhardt, A.: Effects of abandonment of subalpine hay meadows
on plant and invertebrate diversity in Transylvania, Romania, Biol. Conserv.,
132, 261–273, 10.1016/j.biocon.2006.04.018, 2006.Bonari, G., Fajmon, K., Malenovský, I., Zelený, D., Holuša, J.,
Jongepierová, I., Kočárek, P., Ondřej, K.,
Uřičář, J., and Chytrý, M.: Management of semi-natural
grasslands benefiting both plant and insect diversity: The importance of
heterogeneity and tradition, Agric. Ecosyst. Environ., 246, 243–252,
10.1016/j.agee.2017.06.010, 2017.
Burel, F.: Ecological consequences of land abandonment on carabid beetles
distribution in two contrasted grassland areas, Options
Méditerranéennes, 15, 111–119, 1991.Burgio, G. and Sommagio, D.: Syrphids as landscape bioindicators in Italian
agroecosystems, Agr. Ecosyst. Environ., 120, 416–422,
10.1016/j.agee.2006.10.021, 2007.
Chemini, C. and Rizzoli, A.: Land use change and biodiversity conservation
in the Alps, J. Mt. Ecol., 7, 1–7, 2003.
Chytrý, M., Dražil, T., Hájek, M., Kalníková, V.,
Preislerová, Z., Šibík, J., Ujházy, K., Axmanová, I.,
Bernátová, D., Blanár, D., Dančák, M., Dřevojan, P.,
Fajmon, K., Galvánek, D., Hájková, P., Herben, T., Hrivnák,
R., Janeček, Š., Janišová, M., Jiráská, Š.,
Kliment, J., Kochjarová, J., Lepš, J., Leskovjanská, A.,
Merunková, K., Mládek, J., Slezák, M., Šeffer, J.,
Šefferová, V., Škodová, I., Uhlířová, J.,
Ujházyová, M., and Vymazalová, M.: The most species-rich plant
communities in the Czech Republic and Slovakia (with new world records),
Preslia, 87, 217–278, 2015.Cremene, C., Groza, G., Rakosy, L., Schileyko, A. A., Baur, A., Erhardt, A.,
and Baur, B.: Alterations of steppe-like grasslands in Eastern Europe: a
threat to regional biodiversity hotspots, Conserv. Biol., 19, 1606–1618,
10.1111/j.1523-1739.2005.00084.x, 2005.Diemer, M., Oetiker, K., and Billeter, R.: Abandonment alters community
composition and canopy structure of Swiss calcareous fens, Appl. Veg. Sci.,
4, 237–246, 10.1111/j.1654-109X.2001.tb00492.x, 2001.Fox, J., Weisberg, S., Adler, D., Bates, D., Baud-Bovy, G., Ellison, S.,
Firth, D., Friendly, M., Gorjanc, G., Graves, S., Heiberger, R., Krivitsky,
P., Laboissiere, R., Maechler, M., Monette, G., Murdoch, D., Nilsson, H.,
Ogle, D., Ripley, B., Venables, W., Walker, S., Winsemius, D., and Zeileis, A.:
car: Companion to applied regression, R-package 3.0-8, 2020.Frank, T.: Density of adult hoverflies (Diptera, Syrphidae) in sown weed
strips and adjacent fields, J. Appl. Ent., 123, 351–355,
10.1046/j.1439-0418.1999.00383.x, 1999.Fründ, J., Linsenmair, K. E., and Blüthgen, N.: Pollinator diversity
and specialization in relation to flower diversity, Oikos, 119, 1581–1590,
10.1111/j.1600-0706.2010.18450.x, 2010.Galvánek, D. and Lepš, J.: Changes of species richness pattern in
mountain grasslands: abandonment versus restoration, Biodivers. Conserv., 17,
3241–3253, 10.1007/s10531-008-9424-2, 2008.Gittings, T., O'Halloran, J., Kelly, T., and Giller, P. S.: The
contribution of open spaces to the maintenance of hoverfly (Diptera,
Syrphidae) biodiversity in Irish plantation forests, Forest Ecol. Manag.,
237, 290–300, 10.1016/j.foreco.2006.09.052, 2006.Graf, R., Müller, M., Korner, P., Jenny, M., and Jenni, L.: 20 % loss
of unimproved farmland in 22 years in the Engadin, Swiss Alps, Agric.
Ecosyst. Environ., 185, 48–58, 10.1016/j.agee.2013.12.009, 2014.Habel, J. C., Dengler, J., Janišová, M., Török, P.,
Wellstein, C., and Wiezik, M.: European grassland ecosystems: threatened
hotspots of biodiversity, Biodivers. Conserv., 22, 2131–2138,
10.1007/s10531-013-0537-x, 2013.Haenke, S., Scheid, B., Schaefer, M., Tscharntke, T., and Thies, C.: Increasing syrphid fly diversity and density in sown flower strips within simple vs. complex landscapes, J. Appl. Ecol., 46, 1106–1114, 10.1111/j.1365-2664.2009.01685.x, 2009.Hansson, M. and Fogelfors, H.: Management of a semi-natural grassland;
results from a 15-year-old experiment in southern Sweden, J. Veg. Sci., 11,
31–38, 10.2307/3236772, 2000.Heijcman, M., Hejcmanová, V., Pavlů, V., and Beneš, J.: Origin
and history of grasslands in Central Europe – a review, Grass Forage Sci.,
68, 345–363, 10.1111/gfs.12066, 2013.Hennig, E. I. and Ghazoul, J.: Pollinating animals in the urban
environment, Urban Ecosyst., 15, 149–166, 10.1007/s11252-011-0202-7,
2012.Hinojosa, L., Napoléone, C., Moulery, M., and Lambin, E. F.: The
“mountain effect” in the abandonment of grasslands: Insights from the
French Southern Alps, Agric. Ecosyst. Environ., 221, 115–124,
10.1016/j.agee.2016.01.032, 2016.Hülber, K., Moser, D., Sauberer, N., Maas, B., Staudinger, M., Grass,
V., Wrbka, T., and Willner, W.: Plant species richness decreased in
semi-natural grasslands in the Biosphere Reserve Wienerwald, Austria, over
the past two decades, despite agri-environmental measures, Agr. Ecosyst.
Environ., 243, 10–18, 10.1016/j.agee.2017.04.002, 2017.Hussain, R. I., Walcher, R., Brandl, D., Jernej, I., Arnberger, A., Zaller,
J. G., and Frank, T.: Influence of abandonment on syrphid assemblages in
mountainous meadows, J. Appl. Entomol., 142, 450–456,
10.1111/jen.12482, 2017.Hussain, R. I., Walcher, R., Brandl, D., Arnberger, A., Zaller, J. G., and
Frank, T.: Efficiency of two methods of sampling used to assess the
abundance and species diversity of adult Syrphidae (Diptera) in mountainous
in the Austrian and Swiss Alps, Eur. J. Entomol., 115, 150–156, 10.14411/eje.2018.014, 2018.Jauker, F. and Wolters, V.: Hoverflies are efficient pollinators of oilseed
rape, Oecologia, 156, 819–823, 10.1007/s00442-008-1034-x, 2008.Jauker, F., Diekötter, T., Schwarzbach, F., and Wolters, V.: Pollinator
dispersal in an agricultural matrix: opposing responses of wild bees and
hoverflies to landscape structure and distance from main habitat, Landscape
Ecol., 24, 547–555, 10.1007/s10980-009-9331-2, 2009.Jovičić, S., Burgio, G., Diti, I., Krašić, D., Markov, Z.,
Radenković, S., and Vujić, A.: Influence of landscape structure and
land use on Merodon and Cheilosia (Diptera: Syrphidae): contrasting
responses of two genera, J. Insect. Conserv., 21, 53–64,
10.1007/s10841-016-9951-1, 2017.
Kleiber, C. and Zeileis, A.: AER: Applied Econometrics with R, R package
version 1.2-6, 2018.Kök, S., Tomanović, Z., Nedeljković, Z., Şenal, D., and Kasap,
İ.: Biodiversity of the natural enemies of aphids
(Hemiptera: Aphididae) in Northwest Turkey, Phytoparasitica, 48, 51–61,
10.1007/s12600-019-00781-8, 2020.Leroy, P. D., Almohamad, R., Attia, S., Capella, Q., Verheggen, F. J.,
Haubruge, E., and Francis, F.: Aphid honeydew: An arrestant and a contact
kairomone for Episyrphus balteatus (Diptera: Syrphidae) larvae and adults, Eur. J. Entomol., 111,
237–242, 2014.Maurer, K., Weyand, A., Fischer, M., and Stöcklin, J.: Old cultural
traditions, in addition to land use and topography, are shaping plant
diversity of grasslands in the Alps, Biol. Conserv., 130, 438–446,
10.1016/j.biocon.2006.01.005, 2006.McGinlay, J., Gowing, D. J. G., and Budds, J.: The threat of abandonment in
socio-ecological landscapes: Farmers' motivations and
perspectives on high nature value grassland conservation, Environ. Sci.
Policy, 69, 39–49, 10.1016/j.envsci.2016.12.007, 2017.Meyer, B., Jauker, F., and Steffan-Dewenter, I.: Contrasting
resource-dependent responses of hoverfly richness and density to landscape
structure, Basic Appl. Ecol., 10, 178–186,
10.1016/j.baae.2008.01.001, 2009.Meyer, S., Unternährer, D., Arlettaz, R., Humbert, J.-Y., and Menz, M. H.
M.: Promoting diverse communities of wild bees and hoverflies requires a
landscape approach to managing meadows, Agr. Ecosyst. Environ., 239, 376–384,
10.1016/j.agee.2017.01.037, 2017.Moog, D., Poschlod, P., Kahmen, S., and Schreiber, K. F.: Comparison of
species composition between different grassland management treatments after
25 years, Appl. Veg. Sci., 5, 99–106,
10.1111/j.1654-109X.2002.tb00539.x, 2002.Moquet, L., Laurent, E., Bacchetta, R., and Jacquemart, A-L.: Conservation
of hoverflies (Diptera, Syrphidae) requires complementary resources at the
landscape and local scales, Insect Conserv. Diver., 11, 72–87,
10.1111/icad.12245, 2018.Öckinger, E., Eriksson, A. K., and Smith, H. G.: Effects of grassland
abandonment, restoration and management on butterflies and vascular plants,
Biol. Conserv., 133, 291–300, 10.1016/j.biocon.2006.06.009, 2006.
Paradis, E., Blomberg, S., Bolker, B., Brown, J., Claude, J., Sien Cuong,
H., Desper, R., Didier, G., Durand, B., Dutheil, J., Ewing, R. J., Gascuel,
O., Guillerme, T., Heibl, C., Ives, A., Jones, B., Krah, F., Lawson, D.,
Lefort, V., Legendre, P., Lemon, J., Marcon, E., McCloskey, R., Nylander,
J., Opgen-Rhein, J., Popescu, A-A., Royer-Carenzi, M., Schliep, K.,
Strimmer, K., and de Vienne, D.: ape: Analysis of phylogenetics and
evolution, R Package version 5.0, 2017.Poschlod, P. and WallisDeVries, M. F.: The historical and socioeconomic
perspective of calcareous grasslands – lessons from the distant and recent
past, Biol. Conserv., 104, 361–376, 10.1016/S0006-3207(01)00201-4,
2002.Power, F. E., Jackson, Z., and Stout J. C.: Organic farming and landscape
factors affect abundance and richness of hoverflies (Diptera, Syrphidae) in
grasslands, Insect Conserv. Diver., 9, 244–253, 10.1111/icad.12163,
2016.Pykälä, J., Luoto, M., Heikkinen, R. K., and Kontula, T.: Plant
species richness and persistence of rare plants in abandoned semi-natural
grasslands in northern Europe, Basic Appl. Ecol., 6, 25–33,
10.1016/j.baae.2004.10.002, 2005.Rader, R., Bartomeus, I., Garibaldi, L. A., Garratt, M. P. D., Howlett, B.
G., Winfree, R., Cunningham, S. A., Mayfield, M. M., Arthur, A. D.,
Andersson, G. K. S., Bommarco, R., Brittain, C., Carvalheiro, L. G.,
Chacoff, N. P., Entling, M. H., Foully, B., Freitas, B. M., Gemmill-Herren,
B., Ghazoul, J., Griffin, S. R., Gross, C. L., Herbertsson, L., Herzog, F.,
Hipólito, J., Jaggar, S., Jauker, F., Klein, A.-M., Kleijn, D., Krishnan,
S., Lemos, C. Q., Lindström, S. A. M., Mandelik, Y., Monteiro, V. M.,
Nelson, W., Nilsson, L., Pattemore, D. E., Pereira, N. de O., Pisanty, G.,
Potts, S. G., Reemer, M., Rundlöf, M., Sheffield, C. S., Scheper, J.,
Schüepp, C., Smith, H. G., Stanley, D. A., Stout, J. C.,
Szentgyörgyi, H., Taki, H., Vergara, C. H., Viana, B. F., and
Woyciechowski, M.: Non-bee insects are important contributors to global crop
pollination, P. Natl. Acad. Sci. USA, 113, 146–151,
10.1073/pnas.1517092112, 2016.R Core Team: R: A language and environment for statistical computing (Ver.
3.5.2), available at: https://www.R-project.org/, last access: May 2018.Revelle, W.: psych: Procedures for psychological, psychometric and
personality research, R package version 1.8.12, 2019.Rey Benayas, J. M., Martins, A., Nicolau, J. M., and Schulz, J.: Abandonment
of agricultural land: an overview of drivers and consequences, CAB Reviews,
2, 1–14, 10.1079/PAVSNNR20072057, 2007.
Röder, G.: Biologie der Schwebfliegen Deutschlands (Diptera: Syrphidae),
Erna Bauer-Verlag, Keltern-Weiler, Germany, 1990.Schirmel, J., Mantilla-Contreras, J., Blindow, I., and Fartmann, T.: Impacts
of succession and grass encroachment on heathland Orthoptera, J. Insect.
Conserv., 15, 633–642, 10.1007/s10841-010-9362-7, 2011.
Speight, M. C. D.: Species accounts of European Syrphidae (Diptera), 2014,
Syrph the Net, the database of European Syrphidae, Dublin, Ireland, 2014.Strijker, D.: Marginal lands in Europe – causes of decline, Basic Appl.
Ecol., 6, 99–106, 10.1016/j.baae.2005.01.001, 2005.
Stubbs, A. and Falk, A. E.: British hoverflies: An illustrated
identification guide, British Entomological and Natural History Society,
London, 1983.Sutherland, J. P., Sullivan, M. S., and Poppy, G. M.: Distribution and
abundance of aphidophagous hoverflies (Diptera: Syrphidae) in wildflower
patches and field margin habitats, Agric. For. Entomol., 3, 57–64,
10.1046/j.1461-9563.2001.00090.x, 2001.Tasser, E. and Tappeiner, U.: Impact of land use changes on mountain
vegetation, Appl. Veg. Sci., 5, 173–184,
10.1111/j.1654-109X.2002.tb00547.x, 2002.Tasser, E., Walde, J., Tappeiner, U., Teutsch, A., and Noggler, W.: Land-use
changes and natural reforestation in the Eastern Central Alps, Agric.
Ecosyst. Environ., 118, 115–129, 10.1016/j.agee.2006.05.004, 2007.van Rijn, P. C. J., Kooijman, J., and Wäckers, F. L.: The contribution of
floral resources and honeydew to the performance of predatory hoverflies
(Diptera: Syrphidae), Biol. Control, 67, 32–38,
10.1016/j.biocontrol.2013.06.014, 2013.
van Veen, M. P. V.: Hoverflies of Northwest Europe: Identification keys to
the Syrphidae, KNNV Publishing, Utrecht, 2010.Walcher, R., Karrer, J., Sachslehner, L., Bohner, A., Pachinger, B., Brandl,
D., Zaller, J. G., Arnberger, A., and Frank, T.: Diversity of bumblebees,
heteropteran bugs and grasshoppers maintained by both: abandonment and
extensive management of mountain meadows in three regions across the
Austrian and Swiss Alps, Landscape Ecol., 32, 1937–1951,
10.1007/s10980-017-0556-1, 2017.
Weiner, C. N., Werner, M., Linsenmair, K. E., and Blüthgen, N.: Land-use
impacts on plant-pollinator networks: interaction strength and
specialization predict pollinator declines, Ecology, 95, 466–474,
10.1890/13-0436.1, 2014.Wiezik, M., Svitok, M., Wieziková, A., and Dovčiak, M.: Shrub
encroachment alters composition and diversity of ant communities in
abandoned grasslands of western Carpathians, Biodivers. Conserv., 22,
2305–2320, 10.1007/s10531-013-0446-z, 2013.