Insect–flower interactions: network structure in organic versus conventional vineyards

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Animal Conservation. Print ISSN 1367-9430
Insect–flower interactions: network structure in organic
versus conventional vineyards
T. Kehinde* & M. J. Samways
Department of Conservation Ecology and Entomology, Stellenbosch University, Stellenbosch, South Africa
Keywords
food web; network indices; management;
Mediterranean; mutualistic network;
insect–flower interactions; organic; vineyard.
Correspondence
Temitope Kehinde, Department of
Conservation Ecology and Entomology,
Stellenbosch University, Private Bag X1,
7602 Matieland, South Africa.
Tel: +27 82 579 9978; Fax: +27 21 808 4807
Email: topekehinde@gmail.com
*Current address: Department of Zoology
Obafemi Awolowo University, Ile-Ife,
Nigeria.
Editor: Darren Evans
Associate Editor: Darren Evans
Received 25 November 2012; accepted 24
February 2014
Abstract
Ecosystems are made up of various mutualistic and antagonistic plant and animal
interactions. These interactions are subject to various global change phenomena
such as land use change and habitat modification. While the effect of environmentally friendly farming practices on the taxonomic diversity of plants and animal
species has been reported, it is uncertain whether these schemes provide benefit for
species interaction networks. We compared insect–flower interaction networks by
analyzing important web structure indices from organic and conventional vineyards and natural vegetation sites in five different localities in the Cape Floristic
Region biodiversity hotspot. Average number of insect–flower interactions was
higher in organic vineyards compared with conventional vineyards and natural
sites. Abundance of flowering plants contributed significantly to explain the
observed difference in number of interactions in the model. Other network indices
were similar between the different land use types. Our results support the importance of less intensive farming for promoting biodiversity. Approaches such as
organic farming are especially beneficial for important interaction networks that
drive the process of maintaining biodiversity. The potential of well-managed
vineyard ecosystems for promoting conservation of ecologically important insect–
flower interactions is demonstrated.
doi:10.1111/acv.12118
The use of interaction networks and food webs has been
identified as crucial to the science and practice of conservation (Vázquez et al., 2009; Burkle & Alarcón, 2011). This is
especially so with beneficial interactions such as plant–
pollinator networks, which have played a major role in
maintaining the Earth’s biodiversity and crop production
(Klein et al., 2007; Garibaldi et al., 2013). It has been shown
that land use change, habitat modification and other potential drivers of global change may alter network properties
even without biodiversity loss (Tylianakis, Tscharntke &
Lewis, 2007; Laliberté & Tylianakis, 2010). This may affect
ecosystem services such as pest control and pollination,
which are critical for maintaining functioning ecosystems in
biotic communities. For a better understanding of the
underlying processes, Macfadyen et al. (2009) suggested
that attention should be given to investigating how these
species interactions are structured within communities and
how community interactions shape functionality.
Focus on species and their interactions are required to
gain a holistic perspective on biodiversity conservation
(Tylianakis et al., 2010). This ensures that biodiversity estimates are based not only on the occurrence of species but also
on their co-occurring interaction partners (Tylianakis et al.,
2010). The identity and frequency of interactions that form
the building block of an interaction network are vital for
characterizing the structure of ecological networks (Laliberté
& Tylianakis, 2010). However, these networks may vary in
dimension and topology across agricultural landscapes with
different management regimes (Tylianakis et al., 2010).
Wildlife-friendly agricultural management, such as
organic farming, has been shown to support species diversity at both habitat and landscape scales (Clough et al.,
2007; Holzschuh et al., 2007; Holzschuh, Steffan-Dewenter
& Tscharntke, 2008). This is achieved through low-intensity
practices that aim for minimal disturbance, thereby providing feeding and nesting resources for farmland organisms.
On the contrary, intensive agriculture has accelerated the
rate of habitat and biota loss in many communities
(Tscharntke et al., 2005). Yet little is known about the effect
of low-intensity management on the topology of interaction
networks (but see Macfadyen et al., 2009; Power & Stout,
2011). Network indices characterize the structure and
Animal Conservation •• (2014) ••–•• © 2014 The Zoological Society of London
1
Introduction
Promoting conservation of ecologically important insect–flower interactions
T. Kehinde and M. J. Samways
that (1) organic vineyards have networks with higher insect
and flowering plant richness compared with conventional
vineyards; (2) organic vineyards maintain a higher number
of interactions compared with conventional vineyards; (3)
insect–flower networks of organic vineyards are more
complex in configuration compared with networks in conventional vineyards.
configuration of interaction networks and are useful in
determining the pattern of interaction networks under different farm management practices (Macfadyen et al., 2009;
Power & Stout, 2011). Indices such as interaction strength
asymmetry (ISA) which quantifies the imbalance in the
interaction strength of species pairs (Dormann et al., 2009)
and nestedness which describes the distribution of interaction between specialist and generalist species in a network
(Ings et al., 2009) are important descriptors of network
structure. Furthermore, they help us to understand the
response of habitat network topology to habitat disturbance
and agricultural management (Piazzon, Larrinaga &
Santamaria, 2011). For mutualistic networks such as insect–
flower interactions, generality, vulnerability and quantitative connectance are network indices which describe the
average number of plants a pollinator species visits, the
average number of pollinators a plant species receives, and
the proportion of the possible interaction that is realized,
respectively. These indices determine the configuration of
complexity in networks (Okuyama & Holland, 2008;
Dormann et al., 2009) and can help our understanding of
the response of farmland organisms and their interaction
networks to agricultural management practices (Power &
Stout, 2011).
How farmland organisms and their interactions respond
to different management practices is yet to be investigated
for economically important perennial crops such as
winegrape (Vitis vinifera). Winegrape cultivation is a major
agricultural activity in the Cape Floristic Region (CFR)
(Rogers, 2006), a major biodiversity hotspot, and has contributed to the agriculturally driven loss of the highly
endemic flora and fauna of this region (Fairbanks, Hughes
& Turpie, 2004). Similarly, other Mediterranean-type ecosystems are also well suited for winegrape cultivation, as
well as important for irreplaceable biodiversity and species
endemism (Myers et al., 2000; Fairbanks et al., 2004; Viers
et al., 2013). As winegrape cultivation and biodiversity conservation in these areas can be considered as in conflict,
there is need to mitigate the impact of production threats to
ensure that biodiversity is conserved without significantly
impacting agricultural production (Biodiversity and Wine
Initiative, 2011). Furthermore, Bruggisser, Schmidt-Entling
& Bacher (2010) called for the protection of vineyard habitats, as these can support biodiversity when ecological and
viticultural practices are harmonized (Viers et al., 2013).
Fundamental to the conservation action in association with
vineyards is the way in which they are managed. Therefore,
expanding knowledge on the effect of different management
practices for biodiversity, as well as grape production, is
urgently needed (Viers et al., 2013). This is important in the
endemic species-rich CFR and other Mediterranean-type
ecosystems across the globe, which are areas of high priority
for winegrape cultivation and where pollinators are of
immense ecological and evolutionary importance (Johnson,
2010). In response, we investigate here the effect of three
land use types: conventional vineyards, organic vineyards
and natural vegetation (as control/reference sites) on the size
and structure of insect–flower networks. We hypothesize
The study area was in the Stellenbosch wine region of South
Africa (centred at 33°S, 18°E) in the CFR, an area of
87 892 km2, notable for high endemism among its flora and
fauna (Rouget et al., 2003). For a Mediterranean-type ecosystem, the CFR has an exceptional floral richness,
with ≤ 100 unique species of vascular plants within an area of
1000 km2. This compares favourably with many tropical
rainforests and is unparalleled in most other Mediterraneantype ecosystems (Goldblatt & Manning, 2002).
Five pairs of organic and conventional vineyard sites were
selected in five different localities within the study area. Close
to each vineyard pair, a natural vegetation site was also
selected. Natural sites and vineyards were selected such that
they were close enough for environmental conditions to be
similar (e.g. soil type, altitude, precipitation) but were separated enough for the pollinator community to be sampled
independently. All sets of three sites were within 4 km to each
other in each locality (Fig. 1). All organic vineyards were
managed as such for at least 4 years prior to the study and
were officially sanctioned by certification bodies such as the
Bio-Dynamic and Organic Certification Authority, the
Quality Certification Services, and the Société Generale de
Surveillance. Organic vineyards received no agrochemical
treatments except fungicides. In contrast, conventional vineyards were treated with agrochemicals at the rates recommended by Integrated Production of Wine (see Integrated
Production of Wine agrochemical list and coding at http://
www.ipw.co.za). Between-row spaces in vineyards had
various species of annual and perennial cover crops, as well
as some weeds. Plant species between winegrape rows
included members of families Asteraceae, Fabaceae and
Lamiaceae. All vineyards, irrespective of the management
approach, had a similar vineyard layout: range of winegrape
height 1.5–2.0 m, range of between-row spaces 2–3 m, range
of within-row spaces 1.2–1.4 m and size from 4–10 ha.
The vegetation of the natural areas was mostly fynbos
and renosterveld, which is an endemic sclerophylous
vegetation type with fire-driven ecology (Conservation
International, 2013). The natural areas are conservation
areas in the various vineyard localities (Biodiversity and
Wine Initiative, 2011) and share with the vineyards some
plant species, including Felicia filifolia (Vent.) Burtt Davy,
Helichrysum grandiflorum (L.) D. Don, Helichrysum indicum
(L.) and Senecio pterophorus DC. These sites range in size
from 20 to ≥ 100 ha and were included in the study as
2
Animal Conservation •• (2014) ••–•• © 2014 The Zoological Society of London
Materials and methods
Research area
T. Kehinde and M. J. Samways
Promoting conservation of ecologically important insect–flower interactions
Flower-visiting insect samples were collected to confirm
identification to species level in the laboratory. Samples
were identified to morphospecies, genus and family level
where species identification was not possible especially for
groups that are difficult to identify and which are made up
of cryptic species (e.g. Braconidae, Tachinidae, Syrphidae).
Transect sampling was done fortnightly, with a total of six
visits to each site within the sampling period. Species estimation showed 72% of the asymptotic richness of flowervisiting insects were detected while 51% of interactions were
detected (Chao 1 estimator) (Colwell & Coddington, 1994;
Chacoff et al., 2012) (Supporting Information Fig. S5).
Vegetation sampling was done along the same transects
where insect–flower interactions were recorded. Species
richness of flowering plants and abundance of floral units
were recorded in six 1-m2 quadrats at 10-m intervals along
each 50-m transect. Flower unit was defined in terms of bee
movement such that a medium-sized bee has to fly between
separate flower units/heads (Dicks, Corbet & Pywell, 2002).
Data analyses
Sampling took place in spring, between October and December 2010, the time of peak flowering at the study sites. A
100 × 50-m plot was demarcated at the centre of each site,
and three 50-m transects were placed randomly within the
plots. Transect walks were done on days with no rain,
minimal wind (Beaufort scale 0–1) and minimal cloud (< 5%)
cover at all sites. Records of insect–flower interactions were
taken within a 2-m swathe along each transect. An interaction occurs when a flower visitor touches the reproductive
part of a flowering plant. A network link is a pairwise connection between two nodes (i.e. flowering plant species and a
flower visitor species) of a network (Hagen et al., 2012).
An insect–flower interaction matrix was set up for each site.
Web structure for each site was plotted and illustrated as a
bipartite visitation graph (Dormann et al., 2009). Qualitative
and quantitative web structure indices were computed for
each site with ‘networklevel’ function in the bipartite package
in r (version 3.0.1, R Development Core Team, 2013).
These indices were then compared among the three land
use types: organic vineyards, conventional vineyards and
natural habitats [referred to here as ‘land use(s)]. Qualitative
indices determined were as follows: species richness of
flower-visiting insects and flowering plants, and number of
insect–flower interactions.
Quantitative indices weight interactions by their frequency, which reduces their sensitivity to sampling
intensity and network size (Dormann et al., 2009). The following quantitative indices were computed: quantitative
connectance, generality, vulnerability, weighted nestedness,
ISA and specialization asymmetry. These indices are known
to characterize network structure and stability and have
been used to determine the response of insect–flower interactions network to organic versus conventional management in dairy grasslands (Dormann et al., 2009; Power &
Stout, 2011). The effect of land use on each of the network
indices was tested with generalized linear mixed effects
models (Poisson error distribution) with land use as a fixed
factor. Flower abundance was included in the number of
insect–flower interactions and specialization asymmetry
models to test the effect of this variable on the indices
(Power & Stout, 2011). A Bonferroni corrected α of 0.0056
was used to account for multiply analyses done on the same
dataset (Tylianakis et al., 2007). To account for spatial
autocorrelation and the nested sampling design, a nested
random factor was fitted to the model where sites were
nested within land use, and land use was nested within
locality. Tukey’s least significant difference was done to
determine the pairwise comparison of sites for the response
Animal Conservation •• (2014) ••–•• © 2014 The Zoological Society of London
3
Figure 1 Study sites in the Western Cape region of South Africa:
JO = Joostengerg Organic vineyard, JC = Joostengerg Conventional
vineyard, JN = Joostenberg Natural vegetation, LN = Laibach
Organic vineyard, LC = Laibach Conventional vineyard, LN = Laibach
Natural vegetation, FO = Firgroove Organic vineyard, FC = Firgroove
Conventional vineyard, FN = Firgroove Natural vegetation,
UO = Uitzicht Organic vineyard, UC = Uitzicht Conventional vineyard,
UN = Uitzicht Natural vegetation, SO = Spier Organic vineyard,
SC = Spier Conventional vineyard, SN = Spier Natural vegetation.
reference or control sites to ascertain whether they provide
ecological benefit by enhancing insect–flower interactions
compared with vineyards, the dominant agricultural footprint in this region.
Sampling of insect–flower interactions
Promoting conservation of ecologically important insect–flower interactions
T. Kehinde and M. J. Samways
Figure 2 Insect–flower interaction networks of (a) conventional vineyard, (b) organic vineyard and (c) natural site from one of the five localities
sampled. The top levels are the insect species which visit plant species at the bottom level. The arrows between the two levels represent the
interactions between the two levels. The width of the upper and lower rectangles indicates the abundance of insects and plants involved in
visitations, respectively.
The 15 food webs at the study sites were associated with a
total of 90 species of flower-visiting insects (Supporting
Information Appendix S1), 41 species of flowering plants
(Supporting Information Appendix S2), 1911 insect–flower
interactions and 245 links. Bipartite network plots for a
conventional vineyard (Fig. 2a), organic vineyard (Fig. 2b)
and natural vegetation (Fig. 2c) for one of the localities in
this study. Network plots of other study sites are given in
Supporting Information Figs S1–S4 in the supplementary
material.
4
Animal Conservation •• (2014) ••–•• © 2014 The Zoological Society of London
variables that were significantly different. All data analyses
were done in r (version 3.0.1, R Development Core Team,
2013, lme4 package).
Results
T. Kehinde and M. J. Samways
Promoting conservation of ecologically important insect–flower interactions
Figure 2 Continued.
Table 1 Mean (± SE) of network indices of organic and conventional vineyards and natural vegetation obtained from generalized linear mixed
effects models
Flower visitor richness
Flowering plant richness
Number of insect–flower interactionsa
Connectance
ISA
Nestedness
Vulnerability
Generality
Specialization
Organic
Conventional
Natural
d.f.
t
P-value
15.0 ± 2.25
5.0 ± 1.22
155.8 ± 125.19b
0.29 ± 0.05
0.29 ± 0.27
15.37 ± 4.29
3.45 ± 1.66
1.780 ± 0.54
0.44 ± 0.23
15.0 ± 3.54
5.6 ± 1.34
99.8 ± 84.97b
0.28 ± 0.04
0.20 ± 0.20
17.16 ± 9.03
4.34 ± 1.63
2.16 ± 0.70
0.31 ± 0.13
19.4 ± 3.44
10.0 ± 3.44
88.6 ± 66.82b
0.15 ± 0.03
0.21 ± 0.22
6.38 ± 8.02
3.92 ± 1.29
2.06 ± 0.90
0.20 ± 0.07
8
8
9
8
8
8
9
8
8
1.67
2.46
4.18
–0.46
0.27
–2.47
–0.45
–0.41
–0.34
NS
NS
< 0.001
NS
NS
NS
NS
NS
NS
Significant at Bonferroni-corrected α of 0.0056.
Significantly different based on Turkey’s least significant difference test.
d.f., degrees of freedom; ISA, interaction strength asymmetry; NS, not significant; SE, standard error.
a
b
Species richness of flower-visiting insects and flowering
plants was not significantly different between organic and
conventional vineyards (P > 0.05, Table 1). Our models also
showed significantly higher number of insect–flower interactions in organic compared with conventional vineyards
and natural sites (Table 1). Abundance of flowering
plants contributed significantly to explain the observed difference in number of interactions in the model (P < 0.001,
z = 7.31, degrees of freedom = 9). None of the quantitative
indices was significantly different between organic and
Animal Conservation •• (2014) ••–•• © 2014 The Zoological Society of London
5
Promoting conservation of ecologically important insect–flower interactions
T. Kehinde and M. J. Samways
We found no difference in species richness of insects and
flowering plants in organic farming compared with conventional farming systems. This contrasts with other studies on
organic farming, which have shown organic farming to be
beneficial for insect diversity (Isaia, Bona & Badino, 2006;
Gaigher & Samways, 2010), yet agrees with others that
found no benefits (Brittain et al., 2010b; Bruggisser et al.,
2010). Availability of floral resources plays a vital role in
determining the diversity of flower visitors in natural and
agricultural landscapes (Ebeling et al., 2008; Carvalheiro
et al., 2010). Management practices with similar floral richness as found in the organic and conventional vineyards
here are likely to have comparable pollinator richness
(Brittain et al., 2010b). Both organic and conventional vineyards in the CFR support floral-rich vegetation between the
vineyard rows, which may be beneficial for flower visitors.
Our results show that the number of insect–flower interactions in organic vineyards was higher than in conventional vineyards. This could be attributed to habitat free of
synthetic pesticides provided by organic vineyards in this
study, bearing in mind that pesticide use is one of the key
drivers of pollinator decline in agricultural landscapes
(Brittain et al., 2010a; Potts et al., 2010). However, networks of both management systems were similar in terms of
other structure and complexity-related indices. Number of
interaction in mutualistic networks has been identified as
one of the structural indices that determine the complexity
of mutualistic networks (Okuyama & Holland, 2008).
Network indices such as specialization asymmetry, ISA,
weighted nestedness, richness of plants and pollinators, and
frequency of interaction are all important structural indices
of mutualistic networks. However, the effects of these
indices on network structure and complexity are sometimes
related as they are often influenced by similar biological
processes (Vázquez et al., 2007; Okuyama & Holland,
2008). This implies that networks of organic vineyards are
not necessarily more complex in structure than those of
conventional vineyards as only one of the structural indices
was higher for organic vineyards. It has been shown that
inferences from analyses of structural properties of
mutualistic networks are not in isolation of one another
(Santamaría & Rodríguez-Gironés, 2006).
Flower-facilitated response of flower-visiting insects,
which have been reported in agricultural landscapes
(Holzschuh et al., 2007; Carvalheiro et al., 2011), was supported here. This is shown by the significant effect of flower
abundance in the number of insect–flower interactions’
model. This underscores the importance of floral-rich
habitat in promoting conservation of flower visitors and
their ecologically important interactions (Holzschuh et al.,
2007; Carvalheiro et al., 2011).
Although the networks here were similar in terms of
connectance, generality, vulnerability, ISA and specialization asymmetry, in contrast, networks of natural sites had
lower number of insect–flower interactions compared with
organic vineyards. While it may be uncertain that networks
in natural sites are less complex than in organic vineyards,
based on an index that was lower in the natural sites, our
results nevertheless draw attention to the size of insect–
flower interactions in the natural sites (Memmott, Waser &
Price, 2004; Burgos et al., 2007; Okuyama & Holland,
2008). From a practical conservation point of view, the
quality and quantity of natural habitats are crucial for
conservation of pollinator communities and their interacting partners (Potts et al., 2003, 2005). When the quality of
these patches is low, they may not fully deliver conservation
benefits for insect–flower interactions and other components of biodiversity (Kleijn & Van Langevelde, 2006).
However, vineyards have the potential of increasing uniformity of previously heterogeneous floral communities in
natural and semi-natural habitats, which provides support
for biodiversity and guarantees protection against local
extinction (Gabriel, Thies & Tscharntke, 2005; Kehinde &
Samways, 2014). Furthermore, the biodiversity benefits of
floral-rich and pesticide-free vineyard habitats can only be
assured provided further expansion of such habitats is
curtailed.
Perennial systems, such as vineyards, may hold some
value for conservation, especially in the case of organic
vineyards, which can have a significantly higher number of
insect–flower interactions compared with the other land
uses. Mediterranean-type ecosystems across the globe are
areas of high priority for winegrape cultivation and high
biota endemism. Yet our results show that it is possible to
have winegrape cultivation that is not entirely adverse for
the maintenance of indigenous biodiversity in a biodiversity hotspot. This also supports other findings where vineyard habitats and appropriate biodiversity-friendly
management can benefit the local biota (Gliessman, 2001;
Isaia et al., 2006; Bruggisser et al., 2010; Kehinde &
Samways, 2012). This is especially important for endemic
taxa in the CFR, such as the flower-visiting insects (bees,
hoplini beetles, hoverflies, etc.) studied here, which are of
immense ecological and evolutionary importance (Johnson,
2010).
Although the Biodiversity and Wine Initiative (2011) has
succeeded in conserving an appreciable portion of natural
vegetation in the CFR, the emerging holistic approach to
conservation should involve conservation in both natural
and managed systems (Thompson, 1994; Ings et al., 2009;
Tylianakis et al., 2010). Vineyard ecosystems should be well
managed to support non-crop vegetation as well as receive
minimal disturbance from pesticide use. Natural vegetation
patches should be carefully evaluated periodically to ensure
availability of the quality and quantity of habitat needed for
the delivery of conservation benefits required from such
conservation areas.
Halting biodiversity loss involves conservation efforts
targeted at organisms and their interacting partners in both
6
Animal Conservation •• (2014) ••–•• © 2014 The Zoological Society of London
conventional vineyards in our models (Table 1). Quantitative connectance, generality, vulnerability, ISA, weighted
nestedness and specialization asymmetry were not significantly different between the three land uses (Table 1).
Discussion
T. Kehinde and M. J. Samways
Promoting conservation of ecologically important insect–flower interactions
natural and agricultural landscapes (Ings et al., 2009). This
implies that there is a need to gain knowledge of how organisms and their interaction networks respond to various
threats such as climate change, biological invasions and
intensive agriculture, especially for farmland organisms as
shown in this study. Furthermore, this knowledge, when
obtained on various spatial and temporal scales (e.g.
Vrdoljak & Samways, 2014), will promote our understanding of how sustainable conservation policy and practices can
be adopted in the face of various dynamic global change
phenomena (Burkle & Alarcón, 2011).
Acknowledgements
We thank the landowners for making their vineyards available. We also thank C. Eardley, J. Colville, H. Geertsema
and S. Kritzinger-Klopper for help with insect and plant
identification. We also thank F. Fornoff and anonymous
reviewers for their insightful comments on the paper.
Funding was provided by Spier wine farms. T. K. also
received funding from DAAD and AG Leventis Foundation. M. J. S. acknowledges financial support from National
Research Foundation, South Africa.
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Supporting information
Additional Supporting Information may be found in the
online version of this article at the publisher’s web-site:
Figures S1–S4. Insect–flower interaction networks from
study sites.
Figure S5. Species accumulation curve of flower-visiting
insects (a) and links (b) in the study sites.
Appendix S1 Insect species sampled during the study.
Appendix S2 Plant species sampled during the study.
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