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Wild Pollinator Activities Negatively Related to Honey Bee Colony

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Wild Pollinator Activities Negatively Related to Honey Bee Colony bioRxiv preprint doi: https://doi.org/10.1101/667725; this version posted June 11, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 Wild pollinator activities negatively related to honey bee 2 colony densities in urban context 3 4 Lise Ropars1,2*¶, Isabelle Dajoz2&, Colin Fontaine3&, Audrey Muratet4&, Benoît Geslin1¶ 5 6 (1) IMBE, Aix Marseille Univ, Avignon Université, CNRS, IRD, Marseille, France 7 (2) Institut d’Ecologie et des Sciences de l’Environnement de Paris (iEES Paris UMR 7618) 8 Equipe Ecologie et Evolution des réseaux d’interactions, Université Paris Diderot, CNRS-SU. 9 (3) Centre d’Ecologie et des Sciences de la Conservation (CESCO UMR 7204), CNRS- 10 Muséum National d’Histoire Naturelle-SU. 11 (4) Agence régionale de la biodiversité en Île-de-France (ARB îdF). 12 * Corresponding author - e-mail: [email protected] 13 ¶ These authors contributed equally to this work. 14 & These authors also contributed equally to this work. 15 16 Abstract 17 As pollinator decline is increasingly reported in natural and agricultural environments, cities 18 are perceived as shelters for pollinators because of low pesticide exposure and high floral 19 diversity throughout the year. This has led to the development of environmental policies 20 supporting pollinators in urban areas. However, policies are often restricted to the promotion 21 of honey bee colony installations, which resulted in a strong increase in apiary numbers in 22 cities. Recently, competition for floral resources between wild pollinators and honey bees has 23 been highlighted in semi-natural contexts, but whether urban beekeeping could impact wild 24 pollinators remains unknown. Here, we show that in the city of Paris (France), wild pollinator 25 visitation rates is negatively correlated to honey bee colony densities present in the bioRxiv preprint doi: https://doi.org/10.1101/667725; this version posted June 11, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 26 surrounding (500m – slope = -0.614; p = 0.001 – and 1000m – slope = -0.489; p = 0.005). 27 More particularly, large solitary bees and beetles were significantly affected at 500m 28 (respectively slope = -0.425, p = 0.007 and slope = - 0.671, p = 0.002) and bumblebees were 29 significantly affected at 1000m (slope = - 0.451, p = 0.012). Further, lower interaction 30 evenness in plant-pollinator networks was observed with honey bee colony densities within 31 1000 meter buffers (slope = -0.487, p = 0.008). Finally, honey bees tended to focus their 32 foraging activity on managed rather than spontaneous plant species (student t-test, p = 0.001) 33 whereas wild pollinators equally visited managed and spontaneous species. We advocate 34 responsible practices mitigating the introduction of high density of hives in urban 35 environments. Future studies are needed to deepen our knowledge about the potential 36 negative interactions between wild and domesticated pollinators. 37 38 Introduction 39 The recent decline of pollinating insect populations is driven by a conjunction of factors, 40 including habitat fragmentation, use of pesticides, multiplication of pathogens, global 41 warming and the decline of the wild flora [1]. Agricultural landscapes have changed, 42 harbouring fewer floral resources and habitats to support diverse pollinating communities 43 [2,3]. Consequently, many agricultural landscapes are becoming less conducive for 44 pollinators and for beekeeping activities [4]. At the same time, areas that were previously 45 rarely exploited by beekeepers are now under strong pressure to receive apiaries; this is the 46 case in natural habitats and cities [5,6]. Indeed, cities harbour diverse plant species flourishing 47 all year long due to management practices [7] and heat island effect, thus providing resources 48 throughout the year for pollinators [8]. The low pesticide policies applied in many 49 conurbations also may create favourable conditions for the maintenance of diverse pollinator 50 communities [9]. In parallel, inhabitants have associated A. mellifera to the quality of their bioRxiv preprint doi: https://doi.org/10.1101/667725; this version posted June 11, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 51 environment, and honey bees have become a symbol of biodiversity for media and general 52 public [10]. Many citizens have thus installed colonies as their own contribution to mitigate 53 the pollinator decline [11,12] and urban introductions of honey bee colonies have been 54 promoted by public authorities and decision makers. In many cities, this has translated into 55 very recent and rapid increases in the number of honey bee colonies (10 colonies per km2 in 56 London – United Kingdom [13], 15 colonies per km2 in Brussels – Belgium [14]). 57 However, cities are not depauperate in wild pollinating insects and there is increasing 58 evidence that they host diverse assemblages of wild bees [15,16]. This has led to rising 59 concern about numerous introductions of honey bees in cities, that may negatively impact the 60 wild pollinating fauna through competition for floral resources [11]. In other habitats, such as 61 semi-natural (calcareous meadows [17] or scrubland [18,19]) or agricultural landscapes, 62 several authors have detected exploitative competition between domesticated and wild 63 pollinators through the monopolization of floral resources by honey bees [20,21]. However, it 64 is largely unknown to what extent honey bee introductions in cities could impact wild 65 pollinator communities and their foraging activity on urban plant communities. Moreover, the 66 effect of increasing honey bee densities has rarely been assessed using network approaches 67 [11]. Massively introduced honey bees might impair the pollination function at community 68 level by, for example, focusing their visits on managed (ornamental) plant species rather than 69 spontaneous ones [11]. Here, we explore those issues in the city of Paris (France), which has 70 recently experienced a strong growth of its honey bee populations within a few years. In 71 2013, Paris hosted 300 honey bee colonies, and in 2015 this figure had more than doubled, 72 reaching 687 colonies, corresponding to 6.5 colonies.km-2 (data of the veterinary services of 73 Paris; Fig 1), and has continued to increase since. In this context, our first objective was to 74 analyze the effect of increasing honey bee colony density on the visitation rates of wild 75 pollinators at the community and morphological group levels. Secondly, we explored how the bioRxiv preprint doi: https://doi.org/10.1101/667725; this version posted June 11, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 76 evenness of plant-pollinator networks was affected by increasing honey bee colony densities. 77 Finally, we investigated the floral preferences of wild and domesticated pollinators for 78 managed or spontaneous plant species. 79 80 Fig 1. Localisation of honey bee colonies and study sites in the city of Paris. Vegetation 81 height and land use map were obtained from APUR database 82 (http://opendata.apur.org/datasets/). 83 84 Methods 85 Study sites and plant-pollinator survey. 86 The city of Paris (48°51′12″ N, 2°20′55″ E, Île-de-France, France) is a densely populated 87 urban area (2 220 445 inhabitants in 2014, 105km2). In this city, for three consecutive years, 88 we monitored plant-pollinator interactions in five (in 2014) to seven (in 2015 and 2016) green 89 spaces. We chose these green spaces by their contrasted densities of honey bee colonies in 90 their surroundings (Figs 1 and 2) and for their relative accessibility (access granted by the 91 Bibliothèque nationale de France, campus of Paris Diderot University, Pierre et Marie Curie 92 University, Descartes University, and 3 gardens monitored by the Paris Direction des Espaces 93 Verts et de l’Environnement). Sites were distant from 410 to 6 264 meters (see S2 Table). 94 From May to July 2014 and from April to July 2015 and 2016, we carried respectively 8, 11 95 and 13 observation rounds per green space, spaced out at least by a week. For each round, we 96 focused our observations on three one-meter squared patches chosen to be well-flourished. 97 For each flower visit, we identified the visited plant to the lowest possible taxonomical level 98 according to the taxonomic repository of France [22] and classified it as managed or 99 spontaneous (see S1 Table). Mean richness of visited plant species within patches could vary 100 from 2.5 to 6.5 species depending on the flowering phenology of the plants present in the site. bioRxiv preprint doi: https://doi.org/10.1101/667725; this version posted June 11, 2019. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 101 Further, we classified the insect visitors into one of eight morphological groups: small and 102 large solitary bees, honey bees – A. mellifera, bumblebees, beetles, butterflies, hoverflies and 103 other flies [23]. Observation rounds were performed during warm sunny days with no wind 104 (<15°C) and were carried out between 9 a.m. and 7 p.m. 105 106 Fig 2. Study sites within Paris (France) and related plant-pollinator networks. Bipartite 107 networks are retrieved from the compilation of all observed interactions between pollinators 108 (top bar) and plants (bottom bar). Numbers under networks indicate observations year. Each 109 pollinator block represents a morphological group and each plant block represents a species.
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