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Weed-Insect Pollinator Networks As Bio-Indicators of Ecological Sustainability in Agriculture

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Weed-Insect Pollinator Networks As Bio-Indicators of Ecological Sustainability in Agriculture Agron. Sustain. Dev. DOI 10.1007/s13593-015-0342-x REVIEW ARTICLE Weed-insect pollinator networks as bio-indicators of ecological sustainability in agriculture. A review Orianne Rollin1,2 & Giovanni Benelli3 & Stefano Benvenuti 4 & Axel Decourtye1,2,5 & Steve D. Wratten6 & Angelo Canale3 & Nicolas Desneux7 Accepted: 12 November 2015 # The Author(s) 2016. This article is published with open access at Springerlink.com Abstract The intensification of agricultural practices contrib- arable lands; (2) weed-insect pollinator interactions are mod- utes to the decline of many taxa such as insects and wild ulated by the flowers’ features and their quality which are plants. Weeds are serious competitors for crop production attracting insects; (3) most weeds are associated with general- and are thus controlled. Nonetheless, weeds enhance floral ist insect pollinators; and (4) even if weed-pollinator networks diversity in agricultural landscapes. Weeds provide food for are largely mutualistic, some antagonist networks can be ob- insects in exchange for pollination. The stability of mutualistic served when deception occurs. We propose three weed-insect interactions in pollination networks depends on conservation pollinator networks as potential bio-indicators to evaluate the of insect pollinator and weed communities. Some agricultural ecological sustainability of arable land management strategies practices can destabilize interactions and thus modify the sta- in temperate areas: (1) Geometridae and Bombyliidae species bility of pollination networks. Therefore, more knowledge on visiting Caryophyllaceae, (2) Papilionidae foraging on weed-insect networks is needed. Here, we review the interac- Apiaceae, and (3) Syrphidae visiting Asteraceae. tions involved in insect visits to weed flowers in temperate arable lands. Our main findings are that (1) weed pollination Keywords Arthropods . Biodiversity . Pollination . Weed by insects has a key role in maintaining weed communities in management . Wildflowers * Giovanni Benelli Contents [email protected]; [email protected] 1. Introduction * Nicolas Desneux 2. Pollination strategies of weeds in temperate arable [email protected] lands: the key role of insects 3. Insect-pollinated plants: “attract and reward” 1 French National Institute for Beekeeping and Pollination mechanisms (ITSAP-Institut de l’abeille), Avignon, France 4. Do generalist insect pollinators serve weeds better? Not 2 UMT PrADE, Avignon, France always 3 Department of Agriculture, Food and Environment, Insect Behaviour 5. Diversity and stability of weed-insect pollinator net- Group, University of Pisa, via del Borghetto 80, 56124 Pisa, Italy works: a bio-indicator of the arable land health? 4 Department of Agriculture, Food and Environment, Agronomy and 6. Agricultural practices affecting the stability of weed- Agro-ecosystem Management Section, University of Pisa, via del insect pollinator networks Borghetto 80, 56124 Pisa, Italy 6.1. The spatiotemporal dynamic in agricultural land- 5 ACTA, 228 route de l’aérodrome, Site Agroparc, scapes: the importance of a heterogeneous mosaic 84914 Avignon, France 6.2. The key role of the untilled areas for weed-insect 6 Bio-Protection Research Centre, Lincoln University, PO Box 84, pollinator networks Lincoln 7647, New Zealand 6.3. Reduce external inputs to increase biodiversity 7 INRA, UMR 1355 ISA Institut Sophia Agrobiotech, 400 route des 6.4. No tillage: an efficient practice to associate with Chappes, BP 167, F-06903 Sophia Antipolis, France other environmental strategies O. Rollin et al. 7. Conclusions species in arable lands. This is due both to agronomic reasons Acknowledgements (e.g., herbicide resistance) (Preston and Powles 2002)andto References environmental concerns (e.g., pollen transfer between geneti- cally modified crops and hybridizable weeds) (Conner et al. 2003). In addition, several concerns have been raised regard- 1 Introduction ing the decreased plant and pollinator biodiversity in different ecosystems, focusing on the possible relation between the Agricultural ecosystems are the dominant landscapes rarefaction of some plants and their dependence on particular throughout Western Europe and worldwide (Robinson insect pollinators (Benvenuti 2004;Gibsonetal.2006; and Sutherland 2002; Scheper et al. 2013). Due to the Nicholls and Altieri 2012; Grass et al. 2013). The decline in continuous increase of the world human population, wild bee diversity has been strongly correlated with the de- “cropland”, “arable land”, “farmland” or “agricultural cline in wildflowers (Biesmeijer et al. 2006; Bretagnolle and land” have considerably increased (Matson et al. 1997; Gaba 2015 for a recent review). Tscharntke et al. 2005), by conversion of natural and On this basis, the aims of this review are to (i) examine the semi-natural areas. These changes have accelerated es- key role of insects in the pollination strategies of weeds in pecially in the post-war period characterized by in- temperate arable lands, (ii) highlight the mechanisms involved creased external inputs such as fertilizers and pesticides in insect visits to weed flowers in arable lands, (iii) provide a (Tscharntke et al. 2005). This agricultural intensification focus on the ecological importance of generalized interactions had led to a decline of landscape diversity and a loss of in insect pollinator-weed dynamics, (iv) highlight the diversity biodiversity observed in many taxa, especially for in- of weed-insect pollinator interactions and their potential as sects and plants (Sotherton 1998; Chamberlain et al. bio-indicators to evaluate the health of temperate arable lands, 2000;Bentonetal.2002; Kleijn and Sutherland 2003; and (v) analyze sustainable farming practices designed to part- Thomas et al. 2004;Tscharntkeetal.2005; Flynn et al. ly maintain weed-insect pollinator interactions. 2009; Brückmann et al. 2010). Weeds are particularly affected due to their contentious relationship with crop production. Indeed, they are historically considered as a serious competitor for crop plants and therefore for crop 2 Pollination strategies of weeds in temperate arable production (Oerke 2006; Meiss et al. 2008; Fried et al. lands: the key role of insects 2008). However, weeds are a significant part of the floral diversity in agricultural landscapes. They play ma- Not all flowering plants have the same pollination require- jor functional roles for agricultural ecosystems and their ments. Plants can use different mechanisms to realize self- biodiversity and thus have several consequences on eco- pollination, which is pollination of a flower by pollen from system services, especially pollination (Biesmeijer et al. the same flower or flower on the same plant (Pesson and 2006; Bretagnolle and Gaba 2015). Increasing weed Louveaux 1984). In agreement with the time limitation hy- abundance can (i) maintain pollinator populations, (ii) pothesis, self-pollination is crucial for rapid seed formation ensure pollination services, (iii) increase honey yields (Aarssen 2000). Due to this rapid seed set, arable land and therefore be a benefit for beekeepers, and (iv) im- weeds can persist despite the vast range of agronomic dis- prove the sociocultural value of landscape by ensuring turbances (Sutherland 2004). For instance, Amaranthus the persistence and survival of wild flora (Bretagnolle retroflexus L. (Amaranthaceae) is characterized by unattrac- and Gaba 2015). For instance, some studies have tive flowers, almost total self-pollination (Brenner et al. showed the importance of weeds as food resource for 2000), and produces mature seeds just a few weeks after insect pollinators, especially bees (Rollin et al. 2013; emergence (Costea et al. 2004). This reproductive strategy Requier et al. 2014). is an advantage if pollinators are in decline or absent Weed-insect pollinator interactions are also very important (Barbier 1986). For instance, if cross-pollination by insects to maintain weeds in agricultural landscapes. Even if weeds does not occur, dandelion (Taraxacum ssp.) and plants of are predominantly self-pollinating (Sutherland 2004), wind- the thistle family (Carthamus ssp.) ensure their reproduc- and insect-pollinated species are also typical of agricultural tion by a mechanical self-pollination within the flower, ecosystems (Petanidou and Lamborn 2005). The persistence through contact between the ripe stigma and pollen grains dynamics of most weed species in arable land are largely of anthers (Barbier 1986). Other weeds with flowers that driven by insect pollination; the frequency of flower visits are easily recognizable by insects are mainly self-pollinated, by insects is a good parameter for classifying a weed’spolli- for example Convolvulus arvensis L. (Convolvulaceae) nation strategy (Hoffmann 2005; Lunau 2006). There is a (Westwood et al. 1997), Stellaria media (L.) Vill. growing interest in the gene flow mechanisms among weed (Caryophyllaceae) (Verkleij et al. 1980), Portulaca oleracea Weed-insect pollinator networks as bio-indicators L. (Portulacaceae) (Zimmerman 1977), and Anagallis Pollen self-incompatibility is one of the various strategies arvensis L. (Primulaceae) (Gibbs and Talavera 2001). adopted by plant species to prevent the pollination of different However, to prevent self-pollination and inbreeding, many flowers growing on the same plant, especially in the case of species use cross-pollination which promotes genetic diversity individuals with numerous blooms (Di Pasquale and Jacobi and permits the
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