The Bee Fauna of Large Parks in Downtown Paris, France

Home , Andrena semilaevis, Anthidium punctatum, Chelostoma campanularum, Chelostoma rapunculi, Halictus maculatus, Halictus sexcinctus

Annales de la Société entomologique de France (N.S.) International Journal of Entomology

ISSN: 0037-9271 (Print) 2168-6351 (Online) Journal homepage: http://www.tandfonline.com/loi/tase20

The bee fauna of large parks in downtown Paris, France

Benoît Geslin, Violette Le Féon, Michael Kuhlmann, Bernard E. Vaissière & Isabelle Dajoz

To cite this article: Benoît Geslin, Violette Le Féon, Michael Kuhlmann, Bernard E. Vaissière & Isabelle Dajoz (2016): The bee fauna of large parks in downtown Paris, France, Annales de la Société entomologique de France (N.S.)

To link to this article: http://dx.doi.org/10.1080/00379271.2016.1146632

Published online: 11 Apr 2016.

Submit your article to this journal

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tase20

Download by: [Aix-Marseille Université], [Benoit Geslin] Date: 11 April 2016, At: 08:29 Annales de la Société entomologique de France (N.S.), 2016 http://dx.doi.org/10.1080/00379271.2016.1146632

The bee fauna of large parks in downtown Paris, France Benoît Geslina,b*, Violette Le Féonc, Michael Kuhlmannd, Bernard E. Vaissièrec & Isabelle Dajozb aInstitut Méditerranéen de Biodiversité et d’Ecologie Marine et Continentale (IMBE) Aix Marseille Université, CNRS, IRD, Avignon Université, av. Escadrille N. Niemen, F-13397, Marseille cedex 20, France; bInstitut d’écologie et des sciences de l’environnement de Paris (iEES-Paris), CNRS UMR 7618, Université Paris-Diderot-7, UPMC, IRD, INRA, UPEC, UMR 7618, iEES-Paris, F-75005, Paris, France; cINRA, UR 406 Abeilles et Environnement, Laboratoire Pollinisation & Écologie des Abeilles, Site Agroparc, F-84914, Avignon, France; dNatural History Museum, Deptartment of Life Sciences, Cromwell Road, London, SW7 5BD, UK (Accepté le 22 janvier 2016)

Summary. In recent years, a growing number of studies have focused on the potential interest of urban green areas for supporting biodiversity. Private gardens, urban parks or green roofs may support relatively high densities of diverse wild bees. Knowledge is lacking regarding bee assemblages in Paris, the French capital, and one of the most densely populated part of France. In this context, we here provide a ﬁrst assessment of the taxonomic and functional composition of bee assemblages in three urban parks in downtown Paris. Bees were sampled with a set of three coloured pan traps per park. Fifteen 24-hour sessions were performed from April to July 2011. We captured 425 specimens from 44 species representing ﬁve families and 11 genera. The assemblage was dominated by Halictidae (15 species representing 70.1% of total abundance), especially the eusocial species Lasioglossum morio that made 25.2% of total abundance. From a functional point of view, there were only two species of parasitic bees that made 1.2% of total abundance. Most non-parasitic species were polylectic and below-ground nesting. This study highlights the importance of preserving and managing urban parks and other green areas to promote the conservation of wild bees and ultimately the functionality of pollination service in urban ecosystems.

Résumé. La faune d'abeilles sauvages des grands parcs du centre de Paris, France. Au cours de ces dernières années, un nombre croissant d’études se sont penchées sur l’intérêt potentiel des espaces verts dans les villes pour la préservation de la biodiversité. Il a été mis en évidence que les jardins privés, les parcs urbains ou les toits végétalisés peuvent héberger des densités relativement importantes de certaines espèces d’abeilles sauvages, avec des assemblages diversiﬁés. Nous n’avons àl’heure actuelle pas de connaissances sur les assemblages d’abeilles au sein de Paris, capitale française et une des zones la plus densément peuplée de France. Dans ce contexte, nous proposons ici une première évaluation de la composition taxonomique et fonctionnelle des assemblages d’abeilles dans trois parcs urbains du centre de la ville. Les abeilles ont été échantillonnées à l’aide de trois coupelles colorées par parc. Quinze sessions de capture de 24 heures ont été réalisées entre avril et juillet 2011. Nous avons capturé 425 spécimens appartenant à 44 espèces représentant cinq familles et 11 genres. L’assemblage était dominé par les Halictidae (15 espèces représentant 70,1% de l’abondance totale), tout particulièrement l’espèce eusociale Lasioglossum morio qui représentait 25,2% de l’abondance totale. D’un point de vue fonctionnel, seules deux espèces d’abeilles parasites ont été détectées, ce qui représente une très petite proportion de l’abondance totale (1,2%). La majorité des espèces non-parasites étaient polylectiques et terricoles. Cette étude souligne l’importance de la préservation et d’une gestion appropriée des parcs urbains et autres espaces verts pour encourager la préservation des abeilles sauvages et la viabilité du service de pollinisation dans les écosystèmes urbains. Keywords: wild bee assemblage; dominance; Lasioglossum; functional traits; urban ecology

Downloaded by [Aix-Marseille Université], [Benoit Geslin] at 08:29 11 April 2016 LeBuhn 2006; Fetridge et al. 2008; Matteson et al. 2008; There is growing evidence of a decline of bees, the most Osborne et al. 2008; Tonietto et al. 2011; Banaszak- important pollinator group worldwide (Potts et al. 2010; Cibicka & Żmihorski 2012). But, few studies have exam- Goulson et al. 2015). Increasing urbanisation is one of the ined the bee assemblages in urban parks in Europe (Saure major causes of this decline (Hernandez et al. 2009). But 1996; Fortel et al. 2014). As stressed by Brown and despite this overall negative impact of urbanisation, many Paxton (2009), information about bee species distribution bee species can persist in urban environments (e.g. Fortel is essential for assessing population status and setting up et al. 2014). Urban parks, recreation areas, private gar- conservation strategies. Here we explored for the ﬁrst time dens, and green roofs in particular may be favourable for the bee assemblage of urban parks in the city of Paris, bees because they can provide nesting sites and ﬂoral France. We aimed to answer the following questions: resources (e.g. Frankie et al. 2005; McFrederick &

*Corresponding author. Email: [email protected] Present afﬁliation for Michael Kuhlmann is Zoological Museum of Kiel University, Hegewischstraße 3, D-24105 Kiel, Germany. Benoît Geslin and Violette Le Féon contributed equally to this work.

which species are present in urban parks of this densely Regarding species richness, Halictidae and Andrenidae urbanised temperate area? What is the functional compo- both comprised 15 species, followed by Megachilidae sition of this urban bee assemblage? (eight species). The most abundant species, Lasioglossum morio, represented 25.2% of the total abundance (Table 1). The following most abundant species Material and methods were L. nitidulum (17.0% of specimens), L. laticeps (15.8%), Chelostoma campanularum (8.0%), and Bees were sampled in three large public parks located in the inner centre of Paris, one of the most densely populated area of Hylaeus communis (5.4%) (Table 1). However, most spe- France (>21,000 inhabitants km–2; INSEE 2009): the “Jardin du cies were represented by few specimens (32 species Luxembourg”, the “Jardin des Plantes”, and the “Cité included less than five specimens with 17 singletons Internationale Universitaire”. These parks cover 19.5, 21 and among them, i.e. 72.7% and 38.6% of the total number 24 ha, respectively. In accordance to biodiversity-friendly prac- of species, respectively). tices promoted in Paris, pesticide applications stopped in these parks about 10 years ago. In each park, bees were caught at one site with a set of three coloured pan traps (one blue, one white, and one yellow) laid down for 24 h under suitable weather Functional traits conditions following Westphal et al. (2008). Pan-trapping under- There were only two parasitic species (i.e. 4.5% of spe- estimates the occurrence of certain genera like Bombus or cies), Nomada flavoguttata and N. zonata, representing Colletes spp., but it is nevertheless recognised as the best method to assess the overall species richness of a site (Westphal et al. 1.2% of the specimens (Table 2). 2008). From mid-April to mid-July 2011, 15 sampling sessions Among the 42 non-parasitic species, seven were oli- were carried out on each site. Geographic coordinates of sam- golectic. Four species had a preference for Asteraceae, two pling sites were 48°50ʹ42”N, 2°20ʹ19”E in the “Jardin du for Campanulaceae, and one for Apiaceae. Oligolectic ” ʹ ” ʹ ” “ Luxembourg , 48°50 38 N, 2°21 40 E in the Jardin des species accounted for 10.5% of non-parasitic Plantes”, and 48°49ʹ14”N, 2°19ʹ52”E in the “Cité Internationale Universitaire”. The proportion of impervious sur- specimens, and they were represented by very few speci- faces (i.e. the proportion of area covered by buildings, parking mens (one to four), except Chelostoma campanularum (34 areas, and roads) in a 500-m radius around the sites ranged from specimens). 54% to 64%. Regarding nesting location, among the 42 non-para- Bees were stored in 70% ethanol before being processed, sitic species, 31 were below-ground nesting (representing mounted, and identified to species. Taxonomy followed the nomenclature of Kuhlmann et al. (2015). Species richness and 81.7% of specimens) and 11 were above-ground nesting. abundance were pooled over the three sites and the 15 sampling All these latter species were uncommon (< 5 specimens) sessions. We also calculated the estimated species richness using except Chelostoma campanularum and Hylaeus communis the Chao2 estimator (Colwell & Coddington 1994). (34 and 23 specimens, respectively). Information on ecological traits was compiled from the lit- erature (Westrich 1989; Amiet et al. 1999, 2001, 2004, 2007, 2010; Michener 2007). We described each species according to three functional traits, which have been shown to be important in Discussion bee ecology and to determine the response of bees to environ- Across 15 sampling sessions in one year, in three urban mental disturbances (e.g. Williams et al. 2010; Banaszak-Cibicka parks, with one pan trap triplet per park, our study Ż fi & mihorski 2012; Shef eld et al. 2013): reproductive strategy, revealed the presence of 44 wild bee species (for 425 trophic specialisation, and nest location. For the reproductive strategy, we separated non-parasitic (nest builder) from parasitic collected specimens) in the inner city of Paris. We thus species. Then, the subsequent classes were made for only non- provide a first assessment of bee species richness present parasitic species. For trophic specialisation, we distinguished in Paris urban parks. Our study completes other faunistic between polylectic species that collect pollen on several plant and floristic surveys recently made in Paris that taken Downloaded by [Aix-Marseille Université], [Benoit Geslin] at 08:29 11 April 2016 families and oligolectic ones that collect pollen on plant species together provide a global picture of the biodiversity in from a single family. For nesting location, below-ground nesting species were separated from above-ground nesting ones. this city (e.g. Shwartz et al. 2013 for plants, birds and butterflies; Jeanmougin et al. 2014 for Odonata). Given the relatively low sampling effort here (one single year and three pan trap triplets) and the high spatio-temporal Results variability in bee assemblages (Westphal et al. 2008), this Composition of bee fauna list is necessarily incomplete and should be extended by We collected 425 specimens from 44 species in 11 genera future studies. We can already cite two studies that inven- and five families (Table 1). The estimated species richness tory bees in Paris. First, Ferrand et al. (2014) present a bee was 61 species using the Chao2 index; the observed rich- census made in the Parc de la Villette in the northern part ness thus represented 72.1% of the estimated bee richness. of the city. Second, Stallegger (2015) sampled bees in 10 Regarding abundance, the family Halictidae largely domi- sites located along a former railway (called “ligne de la nated the captures (70.1% of specimens), followed by Petite Ceinture de Paris”). In these two studies, bees were Megachilidae (11.5%) and Andrenidae (10.3%). caught using nets, a method that is better than pan traps to Annales de la Société Entomologique de France (N.S.) 3

Table 1. Taxonomic and functional composition of the bee fauna in three large parks in downtown Paris, France.

Species Abundance Proportion Nesting location Reproductive strategy Trophic specialisation

Andrenidae Andrena anthrisci Blüthgen 1925 1 0.24 B NP P * Andrena bicolor Fabricius 1775 12 2.82 B NP P * Andrena cineraria (L. 1758) 1 0.24 B NP P Andrena curtula Pérez 1903 1 0.24 B NP P * Andrena dorsata (Kirby 1802) 1 0.24 B NP P * Andrena ﬂavipes (Panzer 1799) 3 0.71 B NP P * Andrena gravida Imhoff 1835 1 0.24 B NP P * Andrena minutula (Kirby 1802) 10 2.35 B NP P * Andrena minutuloides Perkins 1914 3 0.71 B NP P Andrena nigroaenea (Kirby 1802) 2 0.47 B NP P Andrena propinqua Schenck 1853 1 0.24 B NP P Andrena proxima (Kirby 1802) 1 0.24 B NP O(Apiaceae) Andrena semilaevis Pérez 1903 4 0.94 B NP P Andrena subopaca/minutula 1 0.24 B NP P Andrena sp.1 1 0.24 B NP Na * Panurgus dentipes Latreille 1811 1 0.24 B NP O(Asteraceae) Apidae * Bombus hypnorum (L. 1758) 1 0.24 A NP P * Bombus lucorum (L. 1761) 1 0.24 B NP P * Nomada ﬂavoguttata (Kirby 1802) 3 0.71 B Pa P * Nomada zonata Panzer 1798 2 0.47 B Pa P Colletidae * Hylaeus communis Nylander 1852 23 5.41 A NP P Hylaeus punctatus (Brullé 1832) 4 0.94 A NP P Halictidae * Halictus tumulorum (L. 1758) 7 1.65 B NP P Lasioglossum bluethgeni Ebmer 1911 1 0.24 B NP P * Lasioglossum calceatum (Scopoli 1763) 3 0.71 B NP P * Lasioglossum laticeps (Schenck 1868) 67 15.76 B NP P * Lasioglossum malachurum (Kirby 1802) 6 1.41 B NP P * Lasioglossum morio (Fabricius 1793) 107 25.18 B NP P Lasioglossum nitidiusculum (Kirby 1802) 1 0.24 B NP P * Lasioglossum nitidulum (Fabricius 1804) 72 16.94 B NP P * Lasioglossum pauxillum (Schenck 1853) 14 3.29 B NP P * Lasioglossum politum (Schenck 1853) 7 1.65 B NP P Lasioglossum pygmaeum (Schenk 1853) 2 0.47 B NP P Lasioglossum sabulosum (Warncke 1986) 2 0.47 B NP P * Lasioglossum sexnotatum (Kirby 1802) 1 0.24 B NP P * Lasioglossum villosulum (Kirby 1802) 6 1.41 B NP P Lasioglossum sp.1 2 0.47 B NP P Megachilidae * Chelostoma campanularum (Kirby 1802) 34 8.00 A NP O (Campanulaceae) * Chelostoma rapunculi Lepeletier 1841 2 0.47 A NP O (Campanulaceae) * Heriades crenulatus Nylander 1856 1 0.24 A NP O(Asteraceae) Downloaded by [Aix-Marseille Université], [Benoit Geslin] at 08:29 11 April 2016 * Heriades truncorum (L. 1758) 4 0.94 A NP O(Asteraceae) Heriades sp.1 1 0.24 A NP O(Asteraceae) * Megachile centuncularis (L. 1758) 2 0.47 A NP P Megachile willughbiella (Kirby 1802) 3 0.71 A NP P Megachile willughbiella/circumcincta 1 0.24 A NP P * Osmia bicornis (L. 1758) 1 0.24 A NP P

Abundance: total number of specimens. Proportion: % of the abundance for each species. Nesting location: A = above-ground nesting, B = below-ground nesting. Reproductive strategy: NP = non-parasitic, P = parasitic. Trophic specialisation: O = oligolectic, P = polylectic. Grey highlighting showstheﬁve most abundant species. Asterisks denote species present both in the three parks and in the Vexin français regional park (also see Table 3 for more information).

detect Bombus species. A total of eight Bombus species Since 1998, bees have been extensively studied in a were caught during these two studies, which is an example natural reserve located about 30 km from Paris downtown, of important information complementing our study based the Vexin français regional park. We gathered published on pan-trapping. data (Gadoum et al. 2005; Gadoum & Pauly 2006; Menut 4 B. Geslin et al.

Table 2. Species richness (number of species), abundance (number of specimens), and functional traits of the bee fauna in three large parks in downtown Paris, France.

Species richness % Abundance %

Reproductive strategy Non-parasitic 42 95.5 420 98.8 Parasitic 2 4.5 5 1.2 Nesting location Below ground 31 73.8 343 81.7 Above ground 11 26.2 77 18.3 Trophic specialisation Oligolectic 7 16.7 44 10.5 Polylectic 34 80.9 375 89.3 Unknown 1 2.4 1 0.24

et al. 2007; Gadoum & Legoff 2008; Gadoum 2010) and netting during three consecutive years in a single unpublished data (S. Gadoum, E. Dufrêne, personal com- Californian garden (Pawelek et al. 2009) to 262 when munications) concerning this 710-km2 area. This netting netting bees during about five years with a focus on a survey provides an assessment of the regional species pool large panel of ruderal areas in the city of Berlin (Saure in the surroundings of Paris (for some species groups like 1996). Andrena species, it is an underestimation as some speci- Availability of floral resources and nesting sites influ- mens remain to be identified at the species level; S. ence bee assemblage composition within urban areas Gadoum, personal communication). A total of 141 bee (Wray et al. 2014). For example, due to the high amount species have been recorded in the natural reserve, from of impervious surfaces and the induced lack of suitable 24 genera and six families (Table 3). Globally, the bee ground nesting sites, above-ground nesting bees may be fauna recorded in the three urban parks appears as a subset more represented than below-ground nesting ones in urban of this species pool. However 12 species have been bee assemblages (e.g. Matteson et al. 2008). In our study, recorded only in the urban parks, all represented by very below-ground nesting bees largely dominate the assem- few specimens (one to four) (Table 1). Notable differences blage, suggesting that suitable soil nesting sites still are between the “urban parks” and the “natural area” datasets available, probably along park lanes. are: (1) the lower number of large species (e.g. Regarding assemblage composition, a single species, Anthophora, Bombus,orXylocopa species) in the urban Lasioglossum morio, was dominant and represented parks that could be due at least partially to the use of pan 25.2% of the total abundance. The presence of a few traps; (2) the absence of many parasitic species in the very abundant and many rare species in biotic assem- urban parks (the genus Sphecodes in particular is totally blages is one of the universal laws in ecology and it has absent, whereas 12 species have been recorded in the been often noticed in bees (e.g. Williams et al. 2001). natural reserve); and (3) the absence of the Melittidae However, the degree of dominance of the most abundant family in the urban parks that could be explained by the taxa may vary, and in our case L. morio could be con- fact that species from this family have generally specific sidered as a highly dominant species. This could be due to feeding requirements (narrow oligolectic species and oil- its eusocial behaviour, but other species detected in our collecting ones). It is worth noting that species from parks are eusocial as well (e.g. L. laticeps, L. mala- Melittidae are also absent from the Parisian studies of churum). Also, we recorded a very small proportion of Ferrand et al. (2014) and Stallegger (2015). parasitic species (4.5% of species) as reported in some In other cities around the world, the composition of other urban bee assemblages (5.6% of parasitic species in Downloaded by [Aix-Marseille Université], [Benoit Geslin] at 08:29 11 April 2016 bee assemblages has been investigated: Berlin (Germany) Matteson et al. 2008). The two species we recorded in Saure 1996; Phoenix (USA) in McIntyre and Hostetler (Nomada flavoguttata and N. zonata) both lay their eggs (2001); Vancouver (Canada) in Tommasi et al. (2004); in nests of Andrena species. Rasmont et al. (2005) and New York (USA) in Matteson et al. (2008); San Luis Sheffield et al. (2013) suggest that the presence of para- Obispo (USA) in Pawelek et al. (2009); Poznan (Poland) sitic bees is a good indicator of the stability of bee assem- in Banaszak-Cibicka and Żmihorski (2012); Chicago blages. In contrast to our results, Oertli et al. (2005) for (USA) in Tonietto et al. (2011); and Lyon (France) in example recorded 17.8% of parasitic bee species in a Fortel et al. (2014). As in other types of habitat, the grassland-dominated landscape. Similarly, Fortel et al. observed bee species richness in an urban and suburban (2014) caught 17% of parasitic species in a set of 24 site greatly depends on regional (biogeographical) and sites located along an urbanisation gradient extending landscape conditions as well as on the sampling effort from Lyon core city to agricultural and semi-natural and method (Westphal et al. 2008). To provide examples, areas in nearby cities. Although it remains to be addressed species richness ranges from 40 when sampling bees by in future studies, these two features (large dominance of a Annales de la Société Entomologique de France (N.S.) 5

Table 3. Species recorded in a natural reserve located about Table 3. (Continued). 30 km from Paris downtown, the Vexin français regional park. Species Species Hylaeus brevicornis Nylander 1852 Andrenidae * Hylaeus communis Nylander 1852 Andrena barbilabris (Kirby 1802) Hylaeus confusus Nylander 1852 * Andrena bicolor Fabricius 1775 Hylaeus gredleri Förster 1871 Andrena chrysosceles (Kirby 1802) Hylaeus hyalinatus Smith 1842 * Andrena cineraria (L. 1758) Hylaeus nigritus (Fabricius 1798) Andrena decipiens Schenck 1861 Hylaeus pictipes Nylander 1852 * Andrena dorsata (Kirby 1802) Hylaeus signatus (Panzer 1798) * Andrena flavipes (Panzer 1799) Hylaeus variegatus (Fabricius 1798) Andrena florea Fabricius 1793 Halictidae * Andrena gravida Imhoff 1835 Halictus maculatus Smith 1848 Andrena haemorrhoa (Fabricius 1781) Halictus rubicundus (Christ 1791) Andrena hattorfiana (Fabricius 1775) Halictus scabiosae (Rossi 1790) * Andrena minutula (Kirby 1802) Halictus sexcinctus (Fabricius 1775) * Andrena minutuloides Perkins 1914 Halictus simplex/eurygnathus/langobardicus Andrena pandellei Pérez 1895 Halictus smaragdulus Vachal 1895 Panurgus calcaratus (Scopoli 1763) Halictus subauratus (Rossi 1792) * Panurgus dentipes Latreille 1811 * Halictus tumulorum (L. 1758) Apidae Lasioglossum albipes (Fabricius 1781) Anthophora furcata (Panzer 1798) Lasioglossum brevicorne (Schenck 1868) Anthophora plumipes (Pallas 1772) * Lasioglossum calceatum (Scopoli 1763) Anthophora retusa (L. 1758) Lasioglossum corvinum (Morawitz 1877) Bombus bohemicus Seidl 1838 Lasioglossum costulatum (Kriechbaumer 1873) Bombus cryptarum (Fabricius 1775) Lasioglossum fulvicorne (Kirby 1802) Bombus hortorum (L. 1761) Lasioglossum interruptum (Panzer 1798) * Bombus hypnorum (L. 1758) * Lasioglossum laticeps (Schenck 1868) Bombus lapidarius (L. 1758) Lasioglossum leucozonium (Schrank 1781) * Bombus lucorum (L. 1761) Lasioglossum limbellum (Morawitz 1876) Bombus pascuorum (Scopoli 1763) * Lasioglossum malachurum (Kirby 1802) Bombus pratorum (L. 1761) Lasioglossum minutissimum (Kirby 1802) Bombus ruderarius (Müller 1776) * Lasioglossum morio (Fabricius 1793) Bombus rupestris (Fabricius 1793) * Lasioglossum nitidulum (Fabricius 1804) Bombus sylvarum (L. 1761) Lasioglossum pallens (Brullé 1832) Bombus sylvestris (Lepeletier 1832) Lasioglossum parvulum (Schenck 1853) Bombus terrestris (L. 1758) * Lasioglossum pauxillum (Schenck 1853) Bombus vestalis (Geoffroy 1785) * Lasioglossum politum (Schenck 1853) Ceratina cucurbitina (Rossi 1792) Lasioglossum puncticolle (Morawitz 1872) Eucera longicornis (L. 1758) * Lasioglossum sexnotatum (Kirby 1802) Eucera nigrescens Pérez 1879 Lasioglossum sexstrigatum (Schenck 1868) Melecta luctuosa (Scopoli 1770) Lasioglossum subhirtum (Lepeletier 1841) Nomada atroscutellaris Strand 1921 * Lasioglossum villosulum (Kirby 1802) Nomada bifasciata Olivier 1811 Lasioglossum xanthopus (Kirby 1802) Nomada conjungens Herrich-Schäffer 1839 Lasioglossum zonulum (Schrank 1781) Nomada fabriciana (L. 1767) Sphecodes albilabris (Fabricius 1793) Nomada flava Panzer 1798 Sphecodes crassanus Warncke 1992

Downloaded by [Aix-Marseille Université], [Benoit Geslin] at 08:29 11 April 2016 * Nomada flavoguttata (Kirby 1802) Sphecodes crassus Thomson 1870 Nomada fucata Panzer 1798 Sphecodes ephippius (L. 1767) Nomada goodeniana (Kirby 1802) Sphecodes ferruginatus Hagens 1882 Nomada kohli Schmiedeknecht 1882 Sphecodes gibbus (L. 1758) Nomada lathburiana (Kirby 1802) Sphecodes monilicornis (Kirby 1802) Nomada panzeri Lepeletier 1841 Sphecodes niger Hagens 1874 Nomada ruficornis (L. 1758) Sphecodes puncticeps Thomson 1870 Nomada signata Jurine 1807 Sphecodes reticulatus Thomson 1870 Nomada succincta Panzer 1798 Sphecodes rufiventris (Panzer 1798) * Nomada zonata Panzer 1798 Sphecodes schenckii Hagens 1882 Xylocopa valga Gerstäcker 1872 Melittidae Xylocopa violacea (L. 1758) Dasypoda hirtipes (Fabricius 1793) Colletidae Macropis europaea Warncke 1973 Colletes cunicularius (L. 1761) Melitta nigricans Alfken 1905 Colletes hederae Schmidt & Westrich 1993 Melitta tricincta (Kirby 1802) (continued) (continued) 6 B. Geslin et al.

Table 3. (Continued). park. We thank E. Dufrêne, R. Fonfria†, S. Gadoum, D. Genoud, G. Mahé, A. Pauly, and E. Scheuchl for bee identi- Species fications, C. Chassignet, M. Folschweiller, L. Guilbaud, F. Flacher, G. Fras, A. Khamphone, and J. Roman for help Megachilidae during field and laboratory work, H. Blanchard, L. Fortel, Anthidium manicatum (L. 1758) D. Martinière, and P. Stallegger for providing useful informa- Anthidium oblongatum Illiger 1806 tion. We also thank P. Rasmont and two anonymous referees Anthidium punctatum Latreille 1809 for helpful comments. * Chelostoma campanularum (Kirby 1802) Chelostoma distinctum Stoeckhert 1929 * Chelostoma rapunculi Lepeletier 1841 * Heriades crenulatus Nylander 1856 Funding * Heriades truncorum (L. 1758) Hoplitis adunca (Panzer 1798) This work was supported by the Région Île-de-France through Hoplitis leucomelana (Kirby 1802) DIM Astréa [ASTREA 2009-01-22] and R2DS programs. Hoplitis tridentata (Dufour & Perris 1840) * Megachile centuncularis (L. 1758) Megachile ericetorum Lepeletier 1841 Megachile lagopoda (L. 1761) References Megachile ligniseca (Kirby 1802) Amiet F, Herrmann M, Müller A, Neumeyer R 2001. Apidae 3: Megachile rotundata (Fabricius 1793) Halictus, Lasioglossum. 208 pp. Megachile versicolor Smith 1844 Amiet F, Herrmann M, Müller A, Neumeyer R 2004. Apidae 4: Osmia aurulenta (Panzer 1799) Anthidium, Chelostoma, Coelioxys, Dioxys, Heriades, Osmia bicolor (Schrank 1781) Lithurgus, Megachile, Osmia, Stelis. Centre Suisse de * Osmia bicornis (L. 1758) Cartographie de la Faune. 273 pp. Osmia caerulescens (L. 1758) Amiet F, Herrmann M, Müller A, Neumeyer R 2007. Apidae 5: Osmia cornuta Latreille 1805 Ammobates, Ammobatoides, Anthophora, Biastes, Ceratina, Osmia leaiana (Kirby 1802) Dasypoda, Epeoloides, Epeolus, Eucera, Macropis, Melecta, Osmia rufohirta Latreille 1811 Melitta, Nomada, Pasites, Tetralonia, Thyreus, Xylocopa. Osmia spinulosa (Kirby 1802) 356 pp. Pseudoanthidium nanum (Mocsary 1879) Amiet F, Herrmann M, Müller A, Neumeyer R 2010. Apidae 6: Stelis punctulatissima (Kirby 1802) Andrena, Melitturga, Panurginus, Panurgus. 316 pp. Amiet F, Müller A, Neumeyer R 1999. Apidae 2: Colletes, Data come from Gadoum et al. (2005), Gadoum and Pauly (2006), Dufourea, Hylaeus, Nomia, Nomioides, Rhophitoides, Gadoum and Legoff (2008), S. Gadoum and E. Dufrêne (personal com- Rophites, Sphecodes, Systropha. 219 pp. munications). Asterisks denote species present both in the Vexin français Banaszak-Cibicka W, Żmihorski M. 2012. Wild bees along an regional park and in the three urban parks considered in this study. urban gradient: winners and losers. Journal of Insect Conservation. 16:331–343. Brown MJF, Paxton RJ. 2009. The conservation of bees: a global – single species and low abundance of parasitic species) perspective. Apidologie. 40:410 416. Colwell RK, Coddington JA. 1994. Estimating terrestrial biodi- suggest that bee assemblages in downtown Paris may versity through extrapolation. Philosophical Transactions of suffer from environmental stressors even in large parks the Royal Society of London Series B-Biological Sciences. (from 19.5 to 24 ha in this study). 345:101–118. Coupey C, Mouret H, Fortel L, Visage C, Vyghen F, Aubert M, Vaissiere BE 2015. Helping wild bees and nature find a – Conclusion home in the city a guide for ecological green space management in urban and peri-urban areas. 128 pp. Our results confirmed that large cities in temperate cli- Ferrand M, Garrin M, Mériguet B, Gadoum S 2014. Réalisation

Downloaded by [Aix-Marseille Université], [Benoit Geslin] at 08:29 11 April 2016 mates could support relatively diverse bee assemblages. d’un inventaire-diagnostic entomologique dans le cadre ’ However, although many bee species can persist in urban d une démarche Oasis-nature (portée par Humanité & Biodiversité) dans le parc de la Villette (75). Rapport ﬁnal environments, the taxonomic and functional diversity in 2012‐2014. Établissement public du parc et de la grande cities can be low compared to the surrounding natural halle de la Villette (EPPGHV), Ofﬁce pour les insectes et areas. Given the worldwide trend of increased urbanisa- leur environnement (OPIE). 90 pp + annexes. tion, bee-friendly park management (see e.g. Coupey et al. Fetridge ED, Ascher JS, Langellotto GA. 2008. The bee fauna of 2015) should be promoted to preserve wild pollinator residential gardens in a suburb of New York City (Hymenoptera: Apoidea). Annals of the Entomological assemblages and, ultimately, the functionality of pollina- Society of America. 101:1067–1077. tion service in urban ecosystems. Fortel L, Henry M, Guilbaud L, Guirao AL, Kuhlmann M, Mouret H, Rollin O, Vaissière BE. 2014. Decreasing abundance, increasing diversity and changing structure of the wild bee community (Hymenoptera: Anthophila) along an Acknowledgements urbanization gradient. PLoS ONE. 9:e104679. We greatly thank S. Gadoum and E. Dufrêne for helping us Frankie GW, Thorp RW, Schindler M, Hernandez J, Ertter B, to complete the species list of the Vexin français regional Rizzardi M. 2005. Ecological patterns of bees and their host Annales de la Société Entomologique de France (N.S.) 7

ornamental flowers in two northern California cities. Journal and comparing bumblebee nest densities in gardens and of the Kansas Entomological Society. 78:227–246. countryside habitats. Journal of Applied Ecology. 45:784– Gadoum S. 2010. Inventaire des insectes pollinisateurs sauvages 792. du Centre d’Ecodéveloppement de Villarceaux (Chaussy, Pawelek J, Frankie GW, Thorp RW, Przybylski M. 2009. 95). Guyancourt: Office pour les insectes et leur environne- Modification of a community garden to attract native bee ment (OPIE); 48 pp. pollinators in urban San Luis Obispo, California. Cities and Gadoum S, Iserbyt S, Michez D, Terzo M, Rasmont P. 2005. Les the Environment. 2:21. abeilles sauvages du Parc naturel régional du Vexin français. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Courrier scientifique du Parc naturel régional du Vexin Kunin W. 2010. Global pollinator declines: trends, impacts français. 1:28–33. and drivers. Trends in Ecology and Evolution. 25:345–353. Gadoum S, Legoff G. 2008. Les abeilles sauvages du Parc Rasmont P, Pauly A, Terzo M, Patiny S, Michez D, Iserbyt S, naturel régional du Vexin français. III: les Megachilidae Barbier Y, Haubruge E. 2005. The survey of wild bees (Hymenoptera: apoidea). Courrier scientifique du Parc nat- (Hymenoptera, Apoidea) in Belgium and France. Rome: urel régional du Vexin français. 4:34–41. Food and Agriculture Organisation; p. 18. Gadoum S, Pauly A. 2006. Les abeilles sauvages du Parc naturel Saure C. 1996. Urban habitats for bees: the example of city of régional du Vexin français. II: les Halictes (Hymenoptera: Berlin. In: Matheson A, Buchmann S L, O’toole C, Westrich apoidea: Halictidae: Halictus et Lasioglossum). Courrier P and Williams I H, editors. The conservation of bees. scientifique du Parc naturel régional du Vexin français. London: Academic Press; p. 47–52. 2:36–40. Sheffield CS, Pindar A, Packer L, Kevan PG. 2013. The potential Goulson D, Nicholls E, Botias C, Rotheray EL. 2015. Bee of cleptoparasitic bees as indicator taxa for assessing bee declines driven by combined stress from parasites, pesti- communities. Apidologie. 44:501–510. cides, and lack of flowers. Science. 2010:1–16. Shwartz A, Muratet A, Simon L, Julliard R. 2013. Local and Hernandez JL, Frankie GW, Thorp RW. 2009. Ecology of urban management variables outweigh landscape effects in enhan- bees: a review of current knowledge and directions for future cing the diversity of different taxa in a big metropolis. study. Cities and the Environment. 2:15. Biological Conservation. 157:285–292. [INSEE] Institut National de la Statistique et des Etudes Stallegger P 2015. Inventaire et analyse du peuplement d’abeilles Economiques. 2009. Présentation de la ville de Paris. [cited sauvages (Hymenoptera Apoidea Anthophila) de la Petite 2015 Mar 21]. Available from: http://www.insee.fr/fr/bases- Ceinture ferroviaire de Paris. In: Institut d’Ecologie de-donnees/esl/comparateur.asp?codgeo=dep-75 Appliquée & SETEC Environnement 2015. Étude des ser- Jeanmougin M, Leprieur F, Loïs G, Clergeau P. 2014. Fine-scale vices écologiques rendus par la Petite Ceinture ferroviaire de urbanization affects Odonata species diversity in ponds of a Paris, Lot 2 - Biodiversité et continuités écologiques, Phase megacity (Paris, France). Acta Oecologica. 59:26–34. 2: Inventaire des espèces présentes. Rapport d’étude pour la Kuhlmann M, Ascher JS, Dathe HH, Ebmer AW, Hartmann P, Ville de Paris, Direction des Espaces Verts et de Michez D, Müller A, Patiny S, Pauly A, Praz C, et al. 2015. l’Environnement; 171 pp. Checklist of the Western Palaearctic bees (Hymenoptera: Tommasi D, Miro A, Higo HA, Winston ML. 2004. Bee diver- apoidea: anthophila). [cited 2015 Feb 17]. Available from: sity and abundance in an urban setting. The Canadian http://westpalbees.myspecies.info Entomologist. 136:851–869. Matteson K, Ascher J, Langellotto GA. 2008. Bee richness and Tonietto R, Fant J, Ascher J, Ellis K, Larkin D. 2011.A abundance in New York City urban gardens. Annals of the comparison of bee communities of Chicago green roofs, Entomological Society of America. 101:140–150. parks and prairies. Landscape and Urban Planning. McFrederick Q, LeBuhn G. 2006. Are urban parks refuges for 103:102–108. bumble bees Bombus spp. (Hymenoptera: Apidae)? Westphal C, Bommarco R, Carré G, Lamborn E, Morison N, Biological Conservation. 129:372–382. Petanidou T, Potts SG, Roberts SPM, Szentgyörgyi H, McIntyre NE, Hostetler ME. 2001. Effects of urban land use on Tscheulin T, et al. 2008. Measuring bee diversity in different pollinator (Hymenoptera: apoidea) communities in a desert European habitats and biogeographical regions. Ecological metropolis. Basic and Applied Ecology. 218:209–218. Monographs. 78:653–671. Menut T, Hubert E, Barbut J, Leveque A, Gadoum S, Horellou A Westrich P. 1989. Die Wildbienen Baden-Württembergs 2007. Butte du Hutrel à Saint-Martin-la-Garenne. Inventaire Spezieller Teil. Germany: Eugen Ulmer; 536 pp. des odonates, des orthoptères, des lépidoptères rhopalocères Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L,

Downloaded by [Aix-Marseille Université], [Benoit Geslin] at 08:29 11 April 2016 et hétérocères, des hyménoptères et des coléoptères. Biotope Potts SG. 2010. Ecological and life-history traits predict bee & Conseil Général des Yvelines. 127 pp. species responses to environmental disturbances. Biological Michener CD. 2007. The bees of the world. Baltimore (MD): Conservation. 143:2280–2291. Hopkins University Press; 953 pp. Williams NM, Minckley RL, Silveira FA. 2001. Variation in Oertli S, Mueller A, Dorn S. 2005. Ecological and seasonal native bee faunas and its implications for detecting commu- patterns in the diversity of a species-rich bee assemblage nity changes. Ecology and Society. 5:1–21. (Hymenoptera: apoidea: apiformes). European Journal of Wray JC, Neame LA, Elle E. 2014. Floral resources, body size, Entomology. 102:53–63. and surrounding landscape inﬂuence bee community assem- Osborne JL, Martin AP, Shortall CR, Todd AD, Goulson D, blages in oak-savannah fragments. Ecological Entomology. Knight ME, Hale RJ, Sanderson RA. 2008. Quantifying 39:83–93.