Landscape Heterogeneity and Farming Practice Alter the Species

Basic and Applied Ecology 14 (2013) 540–546

Landscape heterogeneity and farming practice alter the species

composition and taxonomic breadth of pollinator communities

a,b,∗ b b a,b

Georg K.S. Andersson , Klaus Birkhofer , Maj Rundlöf , Henrik G. Smith

Centre for Environmental and Climate Research, Lund University, Ecology Building, SE-223 62 Lund, Sweden

Department of Biology, Lund University, Ecology Building, SE-223 62 Lund, Sweden

Received 24 July 2012; accepted 4 August 2013

Available online 8 September 2013

Abstract

Effects of landscape heterogeneity and farming practice on species composition are less well known than those on species

richness, in spite of the fact that community composition can be at least as important for ecosystem services, such as pollination.

Here, we assessed the effect of organic farming and landscape heterogeneity on pollinator communities, focusing on multivariate

patterns in species composition and the taxonomic breadth of communities. By relating our results to patterns observed for species

richness we show that: (1) species richness generally declines with decreasing landscape heterogeneity, but taxonomic breadth

only declines with landscape heterogeneity on conventionally managed farms. We further highlight the importance to provide

results of species composition analyses as (2) primarily hoverﬂy species beneﬁted from organic farming, but three bee species

from different families were favoured by conventionally managed farms and (3) two hoverﬂy species with aphidophagous

larvae showed contrasting responses to landscape heterogeneity. These results advance the understanding of how landscape

heterogeneity and farming practices alter insect communities and further suggest that diversity patterns need to be analysed

beyond species richness to fully uncover consequences of agricultural intensiﬁcation.

Zusammenfassung

Der Einﬂuss der Heterogenität von Landschaften und der Bewirtschaftungsform auf die Artenzusammensetzung von

Gemeinschaften ist allgemein weniger gut verstanden als deren Auswirkung auf die Artenzahl. Die Zusammensetzung von

Bestäubergemeinschaften ist jedoch eine wichtige Eigenschaft welche ökosystemare Dienstleistungen wie z.B. die Bestäubung

von Pﬂanzen durch Insekten beeinﬂussen kann. In dieser Studie wurde der Effekt der ökologischen und konventionellen

Bewirtschaftung und unterschiedlicher Landschaftskomplexität auf die Artenzahl, Artenzusammensetzung und taxonomische

Breite von Bestäubergemeinschaften untersucht. Aus dem Vergleich dieser Ergebnisse ergaben sich folgende Schlussfolgerun-

gen: (1) die Artenzahl nimmt generell mit abnehmender Heterogenität der Landschaften ab, die taxonomische Breite einer

Gemeinschaft nimmt jedoch nur unter konventioneller Bewirtschaftung ab. Es zeigten sich deutliche Unterschiede zwischen den

analysierten Gruppen, da (2) hauptsächlich Schwebﬂiegenarten von der ökologischen Bewirtschaftung proﬁtierten, wohinge-

gen drei Bienenarten von konventioneller Bewirtschaftung proﬁtierten. Zwei Schwebﬂiegenarten mit aphidophagen Larven

∗

Corresponding author at: Centre for Environmental and Climate Research, Lund University, Ecology Building, SE-223 62 Lund, Sweden.

Tel.: +46 46 2229293.

E-mail address: [email protected] (G.K.S. Andersson).

G.K.S. Andersson et al. / Basic and Applied Ecology 14 (2013) 540–546 541

zeigten gegensätzliche Antworten auf eine zunehmende Heterogenität der Landschaft. Diese Ergebnisse tragen zu einem

verbesserten Verständnis darüber bei, wie die Heterogenität von Landschaften und die Bewirtschaftungsform auf die Arten-

zusammensetzung von Insektengemeinschaften wirken. Des Weiteren wird gezeigt, dass Biodiversitätsstudien neben der

Artenzahl auch die Artenzusammensetzung berücksichtigen sollten, da nur auf diese Weise die Auswirkungen der land-

wirtschaftlichen Intensivierung in vollem Umfang deutlich werden.

Keywords: Pollinators; Landscape context; Landscape ecology; Agricultural intensiﬁcation; Agri-environment schemes

Introduction Any effect of organic farming on diversity and community

composition of pollinators may depend on spatial context

Agricultural intensiﬁcation is a major driver of biodiversity (Jauker, Diekötter, Schwarzbach, & Wolters 2009; Murray

loss in farmland (Krebs, Wilson, Bradbury, & Siriwardena et al. 2012) and temporal duration of the farming practice.

1999; Geiger et al. 2010; Kleijn, Rundlöf, Scheper, Smith, First, the effect of farming practice on species richness and

& Tscharntke 2011), and agri-environment schemes (AES) abundances depends on the heterogeneity of the surround-

have been developed to mitigate this negative effect (Kleijn ing landscape (Carvell et al. 2011; Roschewitz, Gabriel,

& Sutherland 2003; Whittingham 2007). One of the more Tscharntke, & Thies 2005; Rundlöf & Smith 2006; Rundlöf,

prominent AES in Europe is organic farming which has Nilsson, & Smith 2008). Second, there may be a time lag

been shown to provide higher biodiversity in various groups in the response of communities to agricultural homogeni-

(Bengtsson, Ahnström, & Weibull 2005; Diekötter, Wamser, sation (Andersson, Rundlöf, & Smith 2010; Bissonette &

Wolters, & Birkhofer 2010; Power & Stout 2011; Power, Storch 2007). Such a time lag has been shown for the effect

Kelly, & Stout 2012; Rundlöf & Smith 2006; Rundlöf, of an AES, organic farming, on abundances of butterﬂies

Edlund, & Smith 2010). Taxa that beneﬁt from organic (Jonason et al. 2011). Both a better understanding of inter-

farming, such as pollinators, provide a range of impor- actions between landscape heterogeneity and the effects of

tant services to human societies (Isbell et al. 2011; Mace, farming practice and transition age on taxonomic breadth may

Norris, & Fitter 2012) and such services are often posi- improve our ability to predict consequences of agricultural

tively related to species richness (Klein, Steffan-Dewenter, intensiﬁcation for pollinator communities.

& Tscharntke 2003; Kremen, Williams, & Thorp 2002; Our main questions were how organic farming, time since

Winqvist, Ahnström, & Bengtsson 2012). The key role of conversion to organic farming and landscape heterogeneity

insect pollinators of different crops makes understanding modiﬁed community composition and taxonomic breadth of

their response to management and landscape particularly pollinators. We addressed these questions by analysing dif-

important (Eilers, Kremen, Smith Greenleaf, Garber, & Klein ferences in species composition and taxonomic breadth of

2011; Greenleaf & Kremen 2006; Klein et al. 2007; Kremen pollinator communities between (i) organic and conventional

et al. 2002; Viana et al. 2012; Winfree, Williams, Gaines, ﬁelds, (ii) old and new organic ﬁelds and (iii) in landscapes

Ascher, & Kremen 2007). However, species number may along a heterogeneity gradient. Finally (iv), we relate our

not be the only characteristic that modiﬁes the provision results to patterns observed for species richness to highlight

of ecosystem services, which as in the case of pollination the importance of accounting for the taxonomic relatedness

can also depend on the identity of species (Albano, Salvado, between species and for the species composition of commu-

Duarte, Mexia, & Borges 2009; Chagnon, Gingras, & De nities while studying effects of landscape heterogeneity.

Oliveira 1993). This compositional component of communi-

ties may also be affected by agricultural intensiﬁcation and

farming practices. Methods

Communities with identical species numbers can for exam-

ple consist of closely or distantly related species which means Study sites and design

that they differ in average taxonomic breadth between species

pairs (Clarke & Warwick 1998). If a community consists of The study sites were selected in Scania, southern Swe-

more distantly related species one would assume that it rep- den, along a gradient of landscape heterogeneity measured

resents a larger range of functional groups. Theoretical and as the proportion of tilled crop and ley of all farmland in a 1-

empirical studies suggest that such differences in functional km radius around all sampling points (see Persson, Olsson,

group diversity can affect pollination services (Blüthgen Rundlöf, & Smith 2010). This was based on land-use data

& Klein 2011; Hoehn, Tscharntke, Tylianakis, & Steffan- obtained from the Integrated Administrative and Control Sys-

Dewenter 2008). Therefore, if taxonomic breadth indeed tem (IACS) database, which provides the areas of arable land

correlates with functional diversity then it would be an impor- and other habitats, such as semi-natural grassland or mar-

tant additional response metric to agricultural intensiﬁcation gins. The homogenous landscapes do not generally consist

(Purvis & Hector 2000). of more agricultural land. We selected ten conventional and

542 G.K.S. Andersson et al. / Basic and Applied Ecology 14 (2013) 540–546

using information from a Linnaean classiﬁcation tree that is

based on the relationship between all species taken from the

Fauna Europaea database (Warwick & Clarke 1995; for tree

see Appendix A). As we are not aware of any phylogenetic

tree or any traits that cover all 180 species included our data

we could not estimate phylogenetic or functional diversity.

Linnaean classiﬁcation trees for our pollinator communities

at each site were formed based on order (2), family (13),

genus (67) and species (176) identity. Given these four levels

of hierarchy, two pairs of species from different orders (as

the highest hierarchical level) were deﬁned as most distantly

related and the step length to connect these species through

the tree was always set to 100. In contrast species from the

same genus were as closely related as possible and always

had a minimum pair-wise step length of 25. We calculated the

average taxonomic breadth, of a pollinator community ( )

at a particular site, by summing up step lengths in the clas-

siﬁcation tree between all pair-wise combinations of species

and by then dividing this value by the number of pairs. High

values suggest that a community consists of several dis-

Fig. 1. Map of the farms in Scania. Yellow circles are conventional

farms, light green young and dark green old organic farms. Numbers tantly related species and is taxonomically broad, whereas

represent the landscape heterogeneity index category where 1 is the a low value suggests that a community rather consists

most heterogeneous and 5 the most homogeneous landscapes. (For of closely related species. To account for a possible bias of

interpretation of the references to colour in this ﬁgure legend, the the number of observed individuals on values in each

reader is referred to the web version of the article.)

community, we correlated landscape heterogeneity and taxo-

nomic breadth while accounting for the number of observed

individuals by partial correlation analyses.

twenty organic farms along this gradient of landscape het-

To analyse the effect of landscape heterogeneity and

erogeneity. To investigate time-lags, we chose organic farms

farming practice on species richness, taxonomic breadth and

varying in time since transition from conventional to organic

community composition we used permutational analyses

farming and classiﬁed ten as new (2–4 years) and ten as old

of variance (Anderson 2001a). Distance matrices for the

(11–24 years) organic farms. Farms were at least 2 km apart,

two univariate analyses of species richness and taxonomic

so landscape heterogeneity was estimated from independent

breadth were based on Euclidean distances. Species com-

landscapes (Fig. 1).

position was analysed based on Bray–Curtis distances for

At each farm we chose one ﬁeld border of a cereal ﬁeld,

log(x + 1) transformed abundances of all 176 species to

deﬁned as non-cropped area along the ﬁeld, and established a

avoid that joint absences of a species at two sites contributes

200 m long transect. Each transect was equipped with two pan

to similarity between sites (Legendre & Legendre 1998).

traps 50 m from the transect ends and therefore separated by

Abundances were log-transformed to down-weight the

100 m from each other. The pan trap consisted of three cups

importance of abundant versus rare species. In a ﬁrst set of

coloured with white, blue and yellow UV-reﬂecting spray

models we tested for effects of farming system (organic vs.

colour and all traps were half-ﬁlled with 50% propylene gly-

conventional) as ﬁxed factor and landscape heterogeneity

col. We emptied the pan traps once a week for eight weeks

as co-variable on these distance matrices. In a second set of

in July and August 2008. In additional surveys, at the same

models we tested for effects of transition age (young vs. old)

time as pan traps were emptied, we walked along transects

as ﬁxed factor and landscape heterogeneity as co-variable on

with insect nets catching hoverﬂies and wild bees every 5 m

these distance matrices. In case of a signiﬁcant main effect,

within 1 m of the transect. We performed transect surveys

◦ discriminating species between levels of this factor were

only in calm wind, temperatures above 16 C and no rain,

identiﬁed by similarity percentage analyses (Clarke 1993).

resulting in ﬁve transect surveys at each site.

Species were discussed if their individual contribution to

the observed dissimilarity was >2%, as a cut-off value that

Statistical analysis provided the 13 most discriminating species between organ-

ically and conventionally managed systems. All p-values are

We calculated the species richness and taxonomic breadth based on 9999 permutations of residuals under a reduced

of pollinator communities at all 30 sampling sites. Whereas model (Anderson 2001b). Ordination of species composition

the species number reﬂects the diversity of the community is based on principle coordinate analysis (PCO; Gower 1966)

irrespective of the taxonomic relationship between species, and vectors are shown for pollinator species that closely

taxonomic breadth accounts for taxonomic relatedness by relate to the axes with a multiple correlation coefﬁcient higher

G.K.S. Andersson et al. / Basic and Applied Ecology 14 (2013) 540–546 543

Table 1. Average abundance of the most discriminating species

(contribution > 2% per species) between organically (Org.) and con-

ventionally (Conv.) managed farms.

Species Org. Conv.

Syrphus torvus 12.6 34.5

Eupeodes corollae 33.7 16.8

Sphaerophoria taeniata 3.1 8.6

Apis mellifera 6.4 12.3

Psithyrus rupestris 5.8 1.7

Platycheirus clypeatus 25.0 44.9

Bombus lapidarius 22.0 20.5

Syrphus vitripennis 17.3 15.9

Syritta pipiens 8.9 11.6

Platycheirus peltatus 1.9 4.7

Platycheirus albimanus 3.2 4.0

Syrphus ribesii 5.9 5.1

Halictus tumulorum 3.5 2.8

Mean within group similarity 57.6 57.0

Mean between group dissimilarity 43.5

Based on Bray–Curtis similarity from log(x + 1) transformed abun-

dances.

Fig. 2. Relationship between landscape heterogeneity and (A) managed farms (33 vs. 39; pseudo-F1,26 = 4.85; p = 0.039).

average taxonomic breadth in organically ( , dashed line) and con- The interaction between landscape homogeneity and farming

᭹

ventionally ( , solid line) managed farms and (B) species richness practice was not signiﬁcant (pseudo-F1,26 = 0.38; p = 0.54).

of pollinator communities at all 30, both organic and conventional,

The species richness of pollinator communities did not differ

study sites.

between age classes of organic farms (pseudo-F1,16 = 0.28;

p = 0.61) and age class did not show a signiﬁcant interaction

with landscape homogeneity (pseudo-F1,16 = 0.04; p = 0.85).

than 0.3 (chosen to limit the number of displayed species). Farming practice (pseudo-F1,26 = 1.77; p = 0.017) and

All analyses were performed in the PRIMER 6 software. landscape homogeneity (pseudo-F1,26 = 4.58; p = 0.001) but

not age class of organic farms (pseudo-F1,16 = 0.88; p = 0.65)

affected the species composition of pollinator communities,

Results with no signiﬁcant interaction between farming practice and

landscape homogeneity (pseudo-F1,26 = 0.78; p = 0.79) or

We collected on average 51 individuals per trap per day age class and landscape homogeneity (pseudo-F1,16 = 0.95;

resulting in 176 species of pollinating insects, with 88 Diptera p = 0.55). In total, 31% of the dissimilarity between pol-

species in 3 families and 88 Hymenoptera species in 10 linator communities at organic and conventional farms

families (Appendix B). The taxonomic breadth of pollina- was explained by the abundances of 13 pollinator species

tor communities decreased with landscape homogeneity, but (Table 1). Nine species were more abundant in organically

the effect depended on farming system (pseudo-F1,26 = 5.99; managed farms, 8 Diptera, and 1 Hymenoptera. Four species

p = 0.023; Fig. 2A). In conventionally managed farms, were more abundant on conventional farms, 1 Diptera and

taxonomic breadth strongly declined with landscape homo- 3 Hymenoptera. Landscape homogeneity also affected com-

geneity (N = 10; Rpartial = 0.79; p = 0.011), whereas in organic position. For example according to axis one of the PCO, a

farms there was no such decline (N = 20; Rpartial = 0.06; high proportion of arable land increased the abundance of

p = 0.80). The taxonomic breadth of pollinator communi- Eupeodes corollae (r = 0.33), but decreased the abundance

−

ties did not differ between age classes of organic farms of Syrphus torvus (r = 0.37; Fig. 3).

(pseudo-F1,16 = 0.59; p = 0.45) and age class did not show a

signiﬁcant interaction with landscape homogeneity (pseudo-

F1,16 = 1.77; p = 0.21). Discussion

The species richness of pollinators decreased with land-

scape homogeneity (N = 30; pseudo-F1,26 = 10.48; p = 0.003; The species richness of pollinator communities declined

R = −0.47; Fig. 2B) and conventional farming practice, which with landscape homogeneity independent of farming

had on average of six fewer species less than organically practice, whereas the taxonomic breadth of communities

544 G.K.S. Andersson et al. / Basic and Applied Ecology 14 (2013) 540–546

farming primarily favoured syrphid species (Table 1) and

as hoverﬂies act as both pollinators and natural enemies

of pests (Bartsch, Binkiewitz, Klintbjer, Rådén, & Nasibov

2009) this AES may promote multiple services. In contrast,

conventional farming increased abundances of three bee

species from different families. These species were a

mining bee, Halictus tumulorum, a bumblebee, Bombus

lapidarius; and a cuckoo bee, Bombus rupestris. As B.

rupestris is the cuckoo bee of B. lapidarius (Benton 2006)

our results suggest an indirect effect of farming practice on

this nest parasite–host interaction. This suggests that the

nest parasite directly beneﬁts from higher abundances of its

host under conventional farming. Farming practices have

been shown to affect ratios between parasitoids and aphid

hosts (Caballero-López et al. 2012; Pareja, Brown, & Powell

2008), but our study suggests that farming practices can also

alter nest parasite–host interactions between pollinators.

In addition to farming practice, landscape heterogeneity

modiﬁed the species composition of pollinator commu-

Fig. 3. Ordination of species composition of pollinator communities. Abundances of two hoverﬂy species, both with

nities at all 30 study sites based on principle coordinate analysis

aphidophagous larvae, were related to landscape heterogene-

(PCO). The size of bubbles scales according to the landscape het-

ity in opposite directions. Eupeodes corollae primarily prey

erogeneity at each site (0.14–1.00). Vectors are superimposed for

on aphid species that feed on crops like beets, which existed

species with a multiple correlation coefﬁcient >0.3 with PCO axis

only in landscapes with a high degree of homogeneity in our

1 (the circle indicates the vector length for the multiple correlation

study. This may explain the negative relationship between

coefﬁcient = 1.0).

landscape heterogeneity and abundances of E. corollae. The

second species, Syrphus torvus, preys on aphid species that

live on trees, especially conifers. Woodland edges, hedgerows

only declined in conventional ﬁelds. This pattern suggests and orchards are common habitats for the adults. These habi-

that with increasing landscape homogeneity, pollinator tat types are common in heterogeneous landscapes indicating

communities in organically managed ﬁelds primarily lost why the abundance of this species was positively related to

species that were closely related to other remaining species. landscape heterogeneity. Both species are mobile, E. corol-

In contrast, pollinator communities in conventional ﬁelds lae even migrates to overwinter in central Europe (Bartsch

primarily lost species that had no close relatives. Landscape et al. 2009) and it therefore seems that the abundance of these

homogeneity therefore affected pollinator communities more species is rather determined by their habitat needs than by

negatively in conventional ﬁelds, as increasing homogeneity limited mobility.

not only reduced the species richness, but also lead to In conclusion we showed that even though conventional

taxonomically more narrow communities. The presence of ﬁelds had the taxonomically broadest communities, effects

a range of distantly related pollinator species, which may of decreasing landscape heterogeneity were most detrimental

be functionally more dissimilar (Carmona et al. 2012), in this farming context. Our results highlight the importance

can be important for the provision of pollination services to consider interactions between AES and landscape het-

(Cadotte, Cardinale, & Oakley 2008; Chagnon et al. 1993). erogeneity for pollinator communities and strengthen the

Our results may explain previous observations, suggesting argument that future studies should go beyond analysing

that pollination potential in organic ﬁelds was higher species richness to uncover potential effects on community-

compared to conventional ﬁelds in homogeneous landscapes wide patterns. In the future, it would be interesting to analyse

(Andersson, Rundlöf, & Smith 2012). We argue that the if the observed changes in taxonomic breadth and species

measure of taxonomic breadth is an important additional composition alter the trait composition to further understand

diversity metric, as we would have missed such relationship how landscape heterogeneity and farming practices affect

by only focusing on species richness. As it would be very the provision of ecosystem functions. We show that organic

difﬁcult to provide a complete matrix of functional traits for farming maintains the taxonomic breadth of pollinator com-

all 180 species in our data, we further argue that utilisation of munities at intermediate levels independent of landscape

taxonomic information is an important next step in analysing heterogeneity, and it affects community composition with

community responses to anthropogenic disturbance. consequences for inter-speciﬁc interactions. These results

We also studied the community responses in detail contribute to an improved understanding of why the provi-

by analysing the response of all pollinator species to sion of pollination services may vary in a context dependent

landscape heterogeneity and farming practice. Organic manner in different landscapes.

G.K.S. Andersson et al. / Basic and Applied Ecology 14 (2013) 540–546 545

Acknowledgments productivity. Proceedings of the National Academy of Science,

105, 17012–17017.

Carmona, C. P., Azcárate, F. M., de Bello, F., Ollero, H. S.,

We thank the farmers for letting us work on their land and

Leps,ˇ J., & Peco, B. (2012). Taxonomical and functional diver-

for ﬁeld assistants for valuable support in data collection. We

sity turnover in Mediterranean grasslands: Interactions between

are very thankful to Erik Sjödin who identiﬁed the species.

grazing, habitat type and rainfall. Journal of Applied Ecology,

Thanks also to Johan Ekroos and three anonymous refer-

49, 1084–1093.

ees for comments on a previous version of the manuscript.

Carvell, C., Osborne, J. L., Bourke, A. F. G., Freeman, S. N., Pywell,

This study was ﬁnanced by The Swedish Research Council

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for Environment, Agricultural Sciences and Spatial Planning targeted conservation measure depend on landscape context and

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(Hymenoptera). Journal of Economic Entomology, 86, 416–420.

Appendix A. Supplementary data

Clarke, K. R. (1993). Non-parametric multivariate analyses of

changes in community structure. Australian Journal of Ecology,

Supplementary material related to this article can be found,

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