Body Size and Wing Asymmetry in Bees Along an Urbanization Gradient Weronika Banaszak-Cibicka, Monika Fliszkiewicz, Aleksandra Langowska, Michal Żmihorski

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Body Size and Wing Asymmetry in Bees Along an Urbanization Gradient Weronika Banaszak-Cibicka, Monika Fliszkiewicz, Aleksandra Langowska, Michal Żmihorski Body size and wing asymmetry in bees along an urbanization gradient Weronika Banaszak-Cibicka, Monika Fliszkiewicz, Aleksandra Langowska, Michal Żmihorski To cite this version: Weronika Banaszak-Cibicka, Monika Fliszkiewicz, Aleksandra Langowska, Michal Żmihorski. Body size and wing asymmetry in bees along an urbanization gradient. Apidologie, 2018, 49 (3), pp.297-306. 10.1007/s13592-017-0554-y. hal-02973376 HAL Id: hal-02973376 https://hal.archives-ouvertes.fr/hal-02973376 Submitted on 21 Oct 2020 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. Apidologie (2018) 49:297–306 Originala rticle * The Author(s), 2017. This article is an open access publication DOI: 10.1007/s13592-017-0554-y Body size and wing asymmetry in bees along an urbanization gradient 1 1 1 Weronika BANASZAK-CIBICKA , Monika FLISZKIEWICZ , Aleksandra LANGOWSKA , 2,3 MichałŻMIHORSKI 1Institute of Zoology, Poznań University of Life Sciences, Wojska Polskiego 71C, 60-625, Poznań, Poland 2Institute of Nature Conservation, Polish Academy of Sciences, al. A. Mickiewicza 33, 31-120, Kraków, Poland 3Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, SE 750 07, Uppsala, Sweden Received 11 May 2017 – Revised 8 October 2017 – Accepted 23 October 2017 Abstract – The global loss of bee diversity and abundance is a central issue in conservation biology. There is increasing evidence that cities may play an important role in bee conservation, although urbanization may also have negative impacts. Here, we investigate individual body size variation and wing asymmetry (based on 11 traits) in the solitary bee Anthophora plumipes along a rural-urban gradient in Poland. The body size of captured individuals did not show any changes along the gradient. Directional asymmetry was present, since differences between sides in 10 out of 11 traits deviated significantly from zero, with the right-side wing traits being generally larger. In contrast to our expectations, the forewing was more asymmetric in rural than in suburban and urban areas. Similarly, the absolute asymmetry of 11 wing traits (i.e. pooling differences but ignoring direction) was also significantly greater in rural than in suburban and urban landscapes. Since asymmetry may be attributed to environmental pollution and food shortages, we conclude that the urban landscape provides bees with habitats of higher quality and thus should be considered as an important habitat for bee conservation. hymenoptera / Apoidea / bees / city / directional asymmetry 1. INTRODUCTION 2050 (United Nations 2014). It is predicted that 77,500 km2 of the European landscape will have The urbanization process is an important an- been converted to urban areas between 2000 and thropogenic alteration of the modern landscape. 2030 (EEA 2016). There are over 800 cities in the EU with more than As a consequence, urbanization is considered to 50,000 inhabitants, and Europe annually lost over be the main cause of species extinction and a threat 1100 km2 of natural and semi-natural areas to to the highest number of species (Czech et al. urban or other artificial land (EEA 2016). Over 2000). We believe that, this process must have 73% of the European human population is urban- impacted bees as well. Urbanization is mainly as- ized, and this figure is expected to reach 82% by sociated with a decreasing coverage of natural veg- etation, a high proportion of artificial surfaces (con- Electronic supplementary material The online version of crete, asphalt), air pollution, and an impoverished this article (https://doi.org/10.1007/s13592-017-0554-y) vegetation composed mainly of exotic plant species contains supplementary material, which is available to dominating in urban parks and gardens (Blair and authorized users. Launer 1997; Williams et al. 2009). All of these Corresponding author: W. Banaszak-Cibicka, changes appear negative for bees since they impede [email protected] their breeding, foraging and may reduce survival of Manuscript editor: Stan Schneider urban-living bees. One may assume, therefore, that 298 W. Banaszak-Cibicka et al. urbanization causes a decline of bee diversity and In bees, body size is partly affected by food contributes to overall bee reduction in the modern resources available (Bosch and Vicens 2002). Si- landscape (McIntyre and Hostetler 2001). multaneously, body size of imagines determines In contrast to these predictions, several studies the amounts of pollen a bee may collect and is show surprisingly high diversity of Apidae in cities important when it comes to the sex ratio of their (Zapparoli 1997;Cane2005; Banaszak-Cibicka and offspring, since smaller individuals may produce Żmihorski 2012), and urban green areas are be- more sons (Seidelmann et al. 2010). There is also lieved to be important bee reservoirs (Tommasi a positive correlation between body size and flight et al. 2004). On the other hand, high species richness distances (Araújo et al. 2004). Individual variation or abundance confirmed in cities does not necessar- in body size may therefore be an important adap- ily mean that bees are not being impacted by urban- tation of bees to urban habitats. ization. This impact can alter species composition, The pattern of symmetry of body bilateral and change the biology or behaviour of city- structures can also be used as an indicator of dwelling individuals, while leaving overall abun- environmental conditions (Møller and Swaddle dance constant. Urban bees living in a completely 1997) and thus can potentially reflect an urbani- new habitat face different challenges compared to zation effect. Random deviation from bilateral those from natural habitats. Thus, different species symmetry, sometimes called ‘fluctuating asym- traits determining survival in urbanized areas can be metry’ (FA) (Polak and Triners 1994), reflects favoured by natural selection (Chapman et al. 2003; developmental stability and is considered an indi- Slabbekoorn and Peet 2003). Furthermore, since cator of environmentally induced stress in organ- urban habitats provide bees with different resources isms (Palmer and Strobeck 1992). FA is a measure (e.g., exotic plants) and threats (pollution), the biol- of the genome’s ability to successfully buffer de- ogy and ecology of urban bees are probably adapted velopment to achieve a normal phenotype under to these conditions. Thus, to understand the impact stressful environmental conditions (Waddington of urbanization on bees other elements of their 1942). This is why the genetic background of an ecology and biology also need to be examined. individual, population structure and levels of in- Unfortunately, the urbanization impact on bees has breeding may also play roles in susceptibility to not been explored extensively (McIntyre 2000; stress-induced asymmetry. An elevated level of Cane and Tepedino 2001) since most of the existing asymmetry may correlate with the fitness of an studies focused largely on taxonomic composition individual (Møller 1997) and commonly occur- and abundance (Zapparoli 1997;Tommasietal. ring stressors that increase asymmetry include air 2004; Ahrné et al. 2009), thus leaving open the and water pollution, pesticides, temperature, food question of the consequences of urbanization on deficiency and parasitism (De Anna et al. 2013). the ecology of bees. Directional asymmetry is another form of bilateral Our previous research has demonstrated that asymmetry which differs from fluctuating asym- interspecific differences in body size determine metry in that one side is consistently larger than the colonization of an urban environment by bees: the other (Van Valen 1962) and may also be a large-bodied species were more numerous in the potential indicator of developmental stability suburbs while small species dominated in the city (Graham et al. 1993, 1998). It is, therefore, likely centre (Banaszak-Cibicka and Żmihorski 2012). that the level of body asymmetry in bees can be The occurrence of small bee species in city centres shaped by urbanization, although to the best of may be related to a smaller amount of available our knowledge, this issue has not been investigat- food, thus urban areas may act as environmental ed in wild bees so far. filters (Tscharntke et al. 2012) which has been The potential differences in environmental observed for beetles and spiders (Weller and quality between urban and rural habitats may af- Ganzhorn 2004). To the best of our knowledge, fect not only the loss of bee diversity but also the there have been no studies investigating the im- quality of bees. In this study, we investigate body pact of urbanization on the size of bees within one size and wing asymmetry (as a measure of bee species (i.e. individual variation). quality) within one solitary-living wild bee Bee size and asymmetry on a urban gradient 299 species, Anthophora plumipes , in rural, suburban Taraxacum . C. japonica was the only species and urban landscapes. Following our previous among many other co-flowering Rosaceae plants findings that smaller bodied species preferred the that was visited by A. plumipes . Bees were also city centre (Banaszak-Cibicka and Żmihorski attracted to Pulmonaria obscura Dumort and 2012) we hypothesize that smaller individuals Glechoma hederacea L., plants common in some within the species will occur in the city centre rural plots, and some individuals of A. plumipes compared to rural areas. Secondly, we expect were spotted at Salix spp. higher body asymmetry in bees in urbanized land- scapes compared to suburban and rural land- 2.2. Study organism scapes, reflecting unfavourable urban conditions. Anthophora is a large genus of fast-flying, 2. MATERIALS AND METHODS robust bees occurring on all continents except Australia and South America.
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