Weed-insect pollinator networks as bio-indicators of ecological sustainability in agriculture. A review Orianne Rollin, Giovanni Benelli, Stefano Benvenuti, Axel Decourtye, Steve D. Wratten, Angelo Canale, Nicolas Desneux To cite this version: Orianne Rollin, Giovanni Benelli, Stefano Benvenuti, Axel Decourtye, Steve D. Wratten, et al.. Weed- insect pollinator networks as bio-indicators of ecological sustainability in agriculture. A review. Agronomy for Sustainable Development, Springer Verlag/EDP Sciences/INRA, 2016, 36 (1), pp.8. 10.1007/s13593-015-0342-x. hal-01532374 HAL Id: hal-01532374 https://hal.archives-ouvertes.fr/hal-01532374 Submitted on 2 Jun 2017 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License Agron. Sustain. Dev. (2016) 36: 8 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 /Published online: 11 January 2016 # INRA and Springer-Verlag France 2016. This article is published with open access at Springerlink.com Abstract The intensification of agricultural practices contrib- by insects has a key role in maintaining weed communities in utes to the decline of many taxa such as insects and wild arable lands; (2) weed-insect pollinator interactions are mod- plants. Weeds are serious competitors for crop production ulated by the flowers’ features and their quality which are and are thus controlled. Nonetheless, weeds enhance floral attracting insects; (3) most weeds are associated with general- diversity in agricultural landscapes. Weeds provide food for ist insect pollinators; and (4) even if weed-pollinator networks insects in exchange for pollination. The stability of mutualistic are largely mutualistic, some antagonist networks can be ob- interactions in pollination networks depends on conservation served when deception occurs. We propose three weed-insect of insect pollinator and weed communities. Some agricultural pollinator networks as potential bio-indicators to evaluate the practices can destabilize interactions and thus modify the sta- ecological sustainability of arable land management strategies bility of pollination networks. Therefore, more knowledge on in temperate areas: (1) Geometridae and Bombyliidae species weed-insect networks is needed. Here, we review the interac- visiting Caryophyllaceae, (2) Papilionidae foraging on tions involved in insect visits to weed flowers in temperate Apiaceae, and (3) Syrphidae visiting Asteraceae. arable lands. Our main findings are that (1) weed pollination Keywords Arthropods . Biodiversity . Pollination . Weed management . Wildflowers * Giovanni Benelli [email protected]; [email protected] Contents * Nicolas Desneux 1. Introduction [email protected] 2. Pollination strategies of weeds in temperate arable lands: the key role of insects 1 French National Institute for Beekeeping and Pollination 3. Insect-pollinated plants: “attract and reward” 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 networks: a Group, University of Pisa, via del Borghetto 80, 56124 Pisa, Italy bio-indicator of the arable land health? 4 Department of Agriculture, Food and Environment, Agronomy and 6. Agricultural practices affecting the stability of weed-insect Agro-ecosystem Management Section, University of Pisa, via del 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 pol- 6 Bio-Protection Research Centre, Lincoln University, PO Box 84, linator 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 other Chappes, BP 167, F-06903 Sophia Antipolis, France environmental strategies 8 Page 2 of 22 Agron. Sustain. Dev. (2016) 36: 8 7. Conclusions 2003). In addition, several concerns have been raised regard- Acknowledgements ing the decreased plant and pollinator biodiversity in different References ecosystems, focusing on the possible relation between the rarefaction of some plants and their dependence on particular insect pollinators (Benvenuti 2004;Gibsonetal.2006; 1 Introduction Nicholls and Altieri 2012; Grass et al. 2013). The decline in wild bee diversity has been strongly correlated with the de- Agricultural ecosystems are the dominant landscapes through- cline in wildflowers (Biesmeijer et al. 2006; Bretagnolle and out Western Europe and worldwide (Robinson and Sutherland Gaba 2015 for a recent review). 2002; Scheper et al. 2013). Due to the continuous increase of On this basis, the aims of this review are to (i) examine the the world human population, “cropland”, “arable land”, key role of insects in the pollination strategies of weeds in “farmland” or “agricultural land” have considerably increased temperate arable lands, (ii) highlight the mechanisms involved (Matson et al. 1997; Tscharntke et al. 2005), by conversion of in insect visits to weed flowers in arable lands, (iii) provide a natural and semi-natural areas. These changes have accelerat- focus on the ecological importance of generalized interactions ed especially in the post-war period characterized by increased in insect pollinator-weed dynamics, (iv) highlight the diversity external inputs such as fertilizers and pesticides (Tscharntke of weed-insect pollinator interactions and their potential as et al. 2005). This agricultural intensification had led to a de- bio-indicators to evaluate the health of temperate arable lands, cline of landscape diversity and a loss of biodiversity observed and (v) analyze sustainable farming practices designed to part- in many taxa, especially for insects and plants (Sotherton ly maintain weed-insect pollinator interactions. 1998; Chamberlain et al. 2000; Benton et al. 2002; Kleijn and Sutherland 2003; Thomas et al. 2004; Tscharntke et al. 2005; Flynn et al. 2009; Brückmann et al. 2010). Weeds are 2 Pollination strategies of weeds in temperate arable particularly affected due to their contentious relationship with lands: the key role of insects crop production. Indeed, they are historically considered as a serious competitor for crop plants and therefore for crop pro- Not all flowering plants have the same pollination require- duction (Oerke 2006; Meiss et al. 2008; Fried et al. 2008). ments. Plants can use different mechanisms to realize self- However, weeds are a significant part of the floral diversity pollination, which is pollination of a flower by pollen from in agricultural landscapes. They play major functional roles the same flower or flower on the same plant (Pesson and for agricultural ecosystems and their biodiversity and thus Louveaux 1984). In agreement with the time limitation hy- have several consequences on ecosystem services, especially pothesis, self-pollination is crucial for rapid seed formation pollination (Biesmeijer et al. 2006; Bretagnolle and Gaba (Aarssen 2000). Due to this rapid seed set, arable land weeds 2015). Increasing weed abundance can (i) maintain pollinator can persist despite the vast range of agronomic disturbances populations, (ii) ensure pollination services, (iii) increase hon- (Sutherland 2004). For instance, Amaranthus retroflexus L. ey yields and therefore be a benefit for beekeepers, and (iv) (Amaranthaceae) is characterized by unattractive flowers, al- improve the sociocultural value of landscape by ensuring the most total self-pollination (Brenner et al. 2000), and produces persistence and survival of wild flora (Bretagnolle and Gaba mature seeds just a few weeks after emergence (Costea et al. 2015). For instance, some studies have showed the importance 2004). This reproductive strategy is an advantage if pollina- of weeds as food resource for insect pollinators, especially tors are in decline or absent (Barbier 1986). For instance, if bees (Rollin et al. 2013; Requier et al. 2014). cross-pollination by insects does not occur, dandelion Weed-insect pollinator interactions are also very important (Taraxacum ssp.) and plants of the thistle family (Carthamus to maintain weeds in agricultural landscapes. Even if weeds ssp.) ensure their reproduction by a mechanical self- are predominantly self-pollinating (Sutherland 2004), wind- pollination within the flower, through contact between the ripe and insect-pollinated species are also typical of agricultural stigma and pollen grains of anthers (Barbier