Beekeeping in a natural area affects male fitness of a native plant

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Medero, Diego P. Vázquez This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4318764/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Biological invasions represent one of the main threats to biodiversity. The honeybee has been deliberately introduced into a wide range of habitats worldwide. Currently, beekeeping is turning to natural areas in search of better honey quality. This practice can boost honeybee abundance, with potential ecological consequences in the local ecosystems. Although previous studies have considered how female plant fitness responds to honeybees, we know little about their potential effects on male fitness. We studied experimentally the effect of increased honeybee abundance on male fitness of a dominant shrub, Larrea divaricata , in a dryland ecosystem in Villavicencio Nature Reserve, Mendoza, Argentina. In replicated study plots near and far from managed hives we estimated pollen removal and dispersal, self-pollination and outcrossing rates, the number of mating couples, and self-pollinated flowers. Honeybees restricted pollen dispersal distance, with a potential effect on male fitness. Our findings have important implications for maintaining the reproduction and persistence of wild plants exposed to nonnative pollinators and can serve as a guide to decision making about the introduction of managed honeybee hives in nature reserves. Drylands Honeybee introduction Male fitness Native plants Natural Reserves Pollination Figures Figure 1 Introduction Human-driven environmental change threatens biodiversity, especially through land transformation, climate change and biological invasions (Christian, 2023 ; Jaureguiberry et al., 2022 ). For example, global climate change has reduced the fitness of some plant species, potentially affecting their populations in the long term (Anderson, 2016 ). In turn, introduced species may disrupt species interactions through niche displacement or resource competition, ultimately affecting fitness (Geslin et al., 2017 ; Mooney & Cleland, 2001 ). To fully gasp the consequences of environmental change for biodiversity requires understanding how introduced species affect resident species in the invaded community. The honeybee ( Apis mellifera ), a bee introduced massively for beekeeping and pollination services, does not always contribute effectively to pollination and plant reproduction. This bee has become widely naturalized largely through deliberate human introduction (Crane, 1975 , 1999 ), with populations now present in many habitats across the globe. Although this bee provides an efficient pollination service to various crops and wild plants (Cunningham et al., 2016 ; Dick, 2001 ; Ramírez & Davenport, 2013 ; Stern et al., 2004 ; Sun et al., 2013 ), it does not always maximize pollination or replace the contributions of native pollinators due to low effectiveness in pollen transfer (Garibaldi et al., 2013 ; Magrach et al., 2017 ; Montalva et al., 2013 ). Recent studies on native species found conflicting effects of managed hives on nectar and pollen availability, and fruit and seed production, from negative (Gross & MacKay, 1998 ; Magrach et al., 2017 ; Page & Williams, 2023b , 2023a ; Pascual Tudanca et al., 2024 ; Torné-Noguera et al., 2015 ; Valido et al., 2011 ) to positive (Pascual Tudanca et al., 2024 ; Valido et al., 2011 , 2019 ), to nil (Dupont et al., 2004 ). Despite numerous studies on the effects of honeybees on female plant fitness, we know little about the effects of honeybees on male fitness components such as pollen removal, deposition, germination (Gross & MacKay, 1998 ; Magrach et al., 2017 ; Page & Williams, 2023b , 2023a ; Torné-Noguera et al., 2015 ), and pollen flow. This biased focus may reflect the fact that fruit and seed production (female fitness) are easier to quantify than pollen removal, movement and germination (male fitness). Despite this bias, honeybee behavior gives us an idea of the effect it can have on male fitness. Honeybee behavior may decrease male fitness of native plants by recruiting workers to forage in valuable floral resources, leading to a substantial increase in visits to abundant flowering plants (Afik et al., 2008 ; Visscher & Seeley, 1982 ; Von Frisch, 1974 ). Increased visits could in turn lead to increased pollen removal and decreased pollen availability for native pollinators. In addition, foraging honeybees tend to visit different flowers of the same plant individuals (Dupont et al., 2011 ), decreasing pollen flow among different individuals and increasing self-pollination, resulting in the loss of genetic variability and increased inbreeding rates in self-compatible species (Brunet & Sweet, 2006 ; Dupont et al., 2004 ; Karron et al., 2004 ) or interfering with pollination in self-incompatible species (Mitchell et al., 2009 ). We studied the effect of honeybees on the male fitness of Larrea divaricata , a dominant, self-compatible shrub species, in a dryland ecosystem in Villavicencio Nature Reserve, Mendoza, Argentina. Although the honeybee is naturalized in the Reserve (Chacoff et al., 2012 ), we introduced managed hives to cause a drastic increase in the abundance of worker bees in the field so as to assess the impact of this exotic species on male plant fitness. We hypothesized that the increased abundance of Apis mellifera in Villavicencio Nature Reserve decreases male reproductive success of Larrea divaricata , decreasing the number of mating couples and increasing pollen removal and pollen movement between nearby individuals and between flowers of the same individual, ultimately increasing the self-pollination and inbreeding rates. Methods Study site We worked in Villavicencio Nature Reserve (32° 32’ S, 68° 57’ O), Mendoza, in the Monte desert ecoregion. The predominant vegetation is xerophytic, dominated by low shrubs such as Zuccagnia punctata , Larrea cuneifolia and L . divaricata (Chacoff et al., 2012 ). We selected the latter as the focus of this study because of its high abundance in the study site, its widespread use as floral resource by various floral visitors, including the honeybee, and its highly overlapping flowering period with the time in which the managed hives were in the Reserve. Larrea divaricata has bisexual yellow flowers and is self-compatible (Pascual Tudanca et al., 2024 ; Rossi et al., 1999 ). Experimental design To assess the effect of hives on the male fitness of Larrea divaricata , we distributed 125 hives among five beekeeping sites (25 hives per site) during the spring-summer of 2022. From each beekeeping site, we laid a 1000 m transect in which we established two sampling points: one near (200 m) and one far (1000 m) from the hives. In addition, we established a circular plot of 3 m in diameter at each sampling point. Pollen removal To evaluate the effect of the introduction of bee hives on pollen removal in L . divaricata , we selected 15 individuals at each sampling point. In each individual, we selected two branches with ten blossoms and applied a treatment: bagged (pollinator exclusion) and unbagged (open pollination). Once the flowers had opened, we collected five stamens per treatment and stored them in Eppendorf tubes with 70% alcohol. Once in the laboratory, we centrifuged the samples, separated the supernatant and added 0.2 ml of an alcoholic solution with detergent to separate the pollen grains (Dafni et al., 2005 ). Finally, we vortexed the samples for five minutes to release the pollen grains, took three subsamples, and counted the pollen grains in a Neubauer chamber under a microscope (Dafni et al., 2005 ). From these data we estimated the remaining pollen grains in each of the treatments. Pollen dispersal To assess the effect of the introduction of hives on pollen flow, we used fluorescent dye (Radha Colors) as pollen analogues to measure dispersal, as they are suitable for this type of study (Thomson et al., 1986 ; van Rossum et al., 2011 ; Waser & Price, 1982 ). In each plot, we tagged and geo-located all individuals of L . divaricata . When we found fewer than six flowering individuals within the plot at the time of the study, we selected the closest individuals to the plot until there were six flowering individuals. We marked and geo-located these new individuals. In addition, we counted the open flowers of each individual. On the morning, we applied the fluorescent dye with a brush to the anthers of 15 freshly opened flowers on five randomly selected individuals with one of the five colors and left exposed to pollinators. At dusk on the second day, we examined all open flowers of individuals of the same species within the plot with a UV lamp and quantified by color discrimination the number of flowers with fluorescent dye. From these data we estimated the self-pollination rate (percentage of flowers with fluorescent dye from the same individual), the outcrossing rate (percentage of flowers with fluorescent dye from another individual), the number of mating couples, the number of self-pollinated flowers, and the pollen dispersal distance. Data analysis To assess the effect of distance to hives on male fitness we used generalized linear mixed models (GLMM, Bolker et al., 2009 ) with the number of pollen grains remaining in the anthers, pollen dispersal distance, self-pollination rate, and outcrossing rate and, where appropriate, treatment and total number of flowers as response variables, distance to hives as a fixed predictor, and site as a random predictor. For the number of remaining pollen grains, self-pollination rate and outcrossing rate we fitted separate Poisson GLMMs; however, when we detected overdispersion we performed a Negative Binomial GLMM instead. For pollen dispersal distance we fitted three different models: Gaussian GLMM, Poisson GLMM, and Negative Binomial GLMM and selected the best model using Akaike’s Information Criterion (AIC). We performed GLMMs using the glmmTMB function of the glmmTMB package (Bates et al., 2015 ). Finally, to study the effect of distance to hives on the number of couples and the number of self-pollinated flowers we performed two-sample permutation tests (Manly, 2018 ) with the mean as the location parameter using the twoSamplePermutationTestLocation function of the EnvStats package of R statistical software (Millard et al., 2018 ). Results Pollen removal Flowers under pollinator exclusion had a higher number of remaining pollen grains compared to flowers exposed to pollinators (Fig. 1 a, Table S1 ). However, distance to hives and the distance-treatment interaction had no detectable effects on the number of remaining pollen grains (Fig. 1 a, Table S1 ), which indicates that pollen removal did not vary with distance to the hives. Pollen dispersal Pollen dispersal distance increased by 32% with distance to hives (Fig. 1 b, Tables S2-S3), while self-pollination and outcrossing rates did not vary with distance to hives (Fig. 1 c-d, Table S3). Finally, the number of mating couples (permutation test, p = 0.76) and the number of self-pollinated flowers (permutation test, p = 0.68) did not vary with distance to the hives. Discussion We have shown that the increased abundance of honeybees in Villavicencio Nature Reserve partially influenced the male fitness of Larrea divaricata . Thus, close to the hives pollen dispersed shorter distances than away from the hives, with potential consequences for gene flow. However, other aspects of male fitness did not vary with distance to the hives, suggesting a generally weak impact of honeybees on male fitness. We found that pollen dispersal distance decreased near honeybee hives, as expected. This negative effect of honeybee abundance may be attributed to the behavior of this bee when visiting a flower. Upon collecting pollen from the flower, the honeybee packs it into the corbicula, thereby reducing the pollen available for transfer to other flowers. This behavior, called grooming, leads to reduced pollen dispersal distance in other corbiculaate bees (Castellanos et al., 2003 ; Holmquist et al., 2012 ). Decreased pollen dispersal distance near honeybee hives could in turn lead to increased self-pollination and, as L . divaricata is a self-compatible species, increasing inbreeding (Dupont et al., 2004 ; England et al., 2001 ). In the long term, increased inbreeding could affect population persistence. However, we found no effects of hives on outcrossing and self-pollination rates, the number of mating couples and the number of self-pollinated flowers, which indicates only slight effects on male fitness and population persistence. Based on the behavior of Apis mellifera we also expected increased pollen removal near the hives. However, we found no such effects, in contrast to previous studies (Page & Williams, 2023b ; Torné-Noguera et al., 2015 ). This lack of effect of proximity to honeybee hives on pollen removal may be a consequence of our experimental design, as we had a low number of hives, compared with other studies (Page & Williams, 2023b , Torné-Noguera et al., 2015 ). In addition, sampling took place during the flowering peak, when the abundance of floral resources is at its highest. Thus, the increased number of honeybee visits resulting from the few introduced hives could have been insufficient to reduce pollen removal in Larrea divaricata during flowering peak. Honeybees are likely to have a stronger effect at the beginning and the end of flowering or in drought years, when floral resources are scarce. Despite the observed weak effects on male fitness, increased honeybee abundance could cascade through the community, affecting other species. For example, competition between honeybees and native pollinators for floral resources may lead to decreased frequency of visits by native pollinators and a shift in foraging to alternative plants (Dupont et al., 2004 ; Henry & Rodet, 2018 ; Sun et al., 2013 ; Torné-Noguera et al., 2015 ) that are sometimes taxonomically and phenotypically distant from their preferred plants (Roubik & Villanueva-Gutiérrez, 2009 ; Schaffer et al., 1993 ). Switching to nonpreferred resource plant species could ultimately affect the reproductive success of native pollinators. In conclusion, the increased abundance of the honeybee in an arid ecosystem partially influenced the male fitness of a dominant shrub, Larrea divaricata , by modifying pollen dispersal distance. This study advances our understanding about the potential ecological effects of the honeybee, a widespread nonnative species that has invaded many ecosystems throughout the world. Given the importance of nature reserves as reservoirs of biodiversity and that beekeeping has increasingly turned to protected areas, our study can contribute to guide decision making about the introduction of managed honeybee hives in nature reserves. Declarations Statements and declarations This work was supported by Fundación Villavicencio and Fondo para la Investigación Científica y Tecnológica (Grant number PICT-2018-1272) Competing interests The authors have no relevant financial or no-financial interests to disclose. Data availability statement: Data and code are provied as private-for-peer review via the following link: https://figshare.com/s/31b4610d33473261f14e Authors’ contributions María P. Pascual Tudanca and Diego P. Vázquez conceived the ideas and designed methodology; María P. Pascual Tudanca and Alejandra V. Medero conducted field and laboratory work; María P. Pascual Tudanca and Diego P. Vázquez analyzed the data; María P. Pascual Tudanca led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication. Acknowledgments We thank the administration of Villavicencio Nature Reserve and the Direction of Renewable Natural Resources of Mendoza for permission to conduct this study. We are also grateful to Villavicencio personnel for providing logistic assistance and supplies during the study. References Afik, O., Dag, A., & Shafir, S. (2008). Honeybee, Apis mellifera, round dance is influenced by trace components of floral nectar. 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A Comparison of Pollen and Fluorescent Dye Carry‐Over by Natural Pollinators of Ipomopsis. Ecology , 63 (4), 1168–1172. Supplementary Files supplementaryinformation.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4318764","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":299393165,"identity":"fbc67e60-4fa9-420a-81f4-05233036ce83","order_by":0,"name":"María Paula Pascual Tudanca","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAABOUlEQVRIie3SMUvDQBTA8VcOcsuLrikHzScQLgQKUk2+SkMgLi0GBBEsNFO6tLgG/BRSqGvkIE4NuFUsVMmoi7i06OBpq0jaqqNg/kOOEH6E9ziAoqK/3AYN5FP5eOXzg3xHFIxzBH8kWv0rgfVk67R38ThtCV0p3zuZf7hjbwbkLvN9q2IDvcp8sPZzpDpOXYaJMELW7JtR6hEtVkwz4q6JgAdmBO52kCOjBmelQJQkGTA1FApMHhSGPHa6gB5DIDz/l1HDnM0CYYfl4fmzJKjH+E7aC9JeQaqaGggn1NQBkUTjC1JHoIkkYomMU6+GyZ4bYrPPMPW48TYLctfoCiRyqMslctMT19NWbfeEDs+eUG6sEsuN4Yul005Hru7oOE9AwxWrn0eQf16DXxKgt+u/FRUVFf2jXgGxoGLXmCB+zQAAAABJRU5ErkJggg==","orcid":"https://orcid.org/0000-0002-3777-1330","institution":"IADIZA: Instituto Argentino de Investigaciones de las Zonas Aridas","correspondingAuthor":true,"prefix":"","firstName":"María","middleName":"Paula Pascual","lastName":"Tudanca","suffix":""},{"id":299393166,"identity":"8e9907d5-08ee-4991-939e-eeae61642a6e","order_by":1,"name":"Alejandra V. Medero","email":"","orcid":"","institution":"IADIZA: Instituto Argentino de Investigaciones de las Zonas Aridas","correspondingAuthor":false,"prefix":"","firstName":"Alejandra","middleName":"V.","lastName":"Medero","suffix":""},{"id":299393167,"identity":"c9f1e5f1-5d91-4a06-8d70-371ace1c7765","order_by":2,"name":"Diego P. Vázquez","email":"","orcid":"","institution":"IADIZA: Instituto Argentino de Investigaciones de las Zonas Aridas","correspondingAuthor":false,"prefix":"","firstName":"Diego","middleName":"P.","lastName":"Vázquez","suffix":""}],"badges":[],"createdAt":"2024-04-24 14:03:21","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4318764/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4318764/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":56405815,"identity":"e0e66ec1-ddb5-46a7-a830-593fde8dd248","added_by":"auto","created_at":"2024-05-13 18:25:53","extension":"jpg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":141293,"visible":true,"origin":"","legend":"\u003cp\u003eMale fitness of \u003cem\u003eLarrea\u003c/em\u003e \u003cem\u003edivaricata\u003c/em\u003e as a function of distance to honeybee hives. (a-d) Model predictions for (a) number of remaining pollen grains as a function of two different treatments (PE: pollinator exclusion, OP: open pollination), (b) pollen dispersal distance measured in meters, (c) self-pollination rate and (d) outcrossing rate. Black dots represent the model prediction, errorbars the confidence interval and red and blue dots the data. Significance of GLMM: *: p\u0026lt;0.05. See Appendix: Tables S1-S3 for more information on GLMM. (e-f) Boxplots for (e) number of couples and (f) number of self-pollinated flowers as a function of distance to honeybee hives\u003c/p\u003e","description":"","filename":"Fig1.jpg","url":"https://assets-eu.researchsquare.com/files/rs-4318764/v1/bd1b9f98a09f624fb5467196.jpg"},{"id":58315715,"identity":"7a602e51-1b8d-4f5a-b594-26b9c1b0c059","added_by":"auto","created_at":"2024-06-13 20:59:00","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":437772,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4318764/v1/d2f2cfb5-1c78-4709-8b58-d2afce38d82f.pdf"},{"id":56405816,"identity":"f6e5cef9-405c-4b7f-8c44-901ed6f79d71","added_by":"auto","created_at":"2024-05-13 18:25:55","extension":"docx","order_by":7,"title":"","display":"","copyAsset":false,"role":"supplement","size":8050,"visible":true,"origin":"","legend":"","description":"","filename":"supplementaryinformation.docx","url":"https://assets-eu.researchsquare.com/files/rs-4318764/v1/649d1593408855e629278d25.docx"}],"financialInterests":"","formattedTitle":"Beekeeping in a natural area affects male fitness of a native plant","fulltext":[{"header":"Introduction","content":"\u003cp\u003eHuman-driven environmental change threatens biodiversity, especially through land transformation, climate change and biological invasions (Christian, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2023\u003c/span\u003e; Jaureguiberry et al., \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). For example, global climate change has reduced the fitness of some plant species, potentially affecting their populations in the long term (Anderson, \u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). In turn, introduced species may disrupt species interactions through niche displacement or resource competition, ultimately affecting fitness (Geslin et al., \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Mooney \u0026amp; Cleland, \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2001\u003c/span\u003e). To fully gasp the consequences of environmental change for biodiversity requires understanding how introduced species affect resident species in the invaded community.\u003c/p\u003e \u003cp\u003eThe honeybee (\u003cem\u003eApis mellifera\u003c/em\u003e), a bee introduced massively for beekeeping and pollination services, does not always contribute effectively to pollination and plant reproduction. This bee has become widely naturalized largely through deliberate human introduction (Crane, \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e1975\u003c/span\u003e, \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1999\u003c/span\u003e), with populations now present in many habitats across the globe. Although this bee provides an efficient pollination service to various crops and wild plants (Cunningham et al., \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2016\u003c/span\u003e; Dick, \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2001\u003c/span\u003e; Ram\u0026iacute;rez \u0026amp; Davenport, \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Stern et al., \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Sun et al., \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2013\u003c/span\u003e), it does not always maximize pollination or replace the contributions of native pollinators due to low effectiveness in pollen transfer (Garibaldi et al., \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Magrach et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Montalva et al., \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Recent studies on native species found conflicting effects of managed hives on nectar and pollen availability, and fruit and seed production, from negative (Gross \u0026amp; MacKay, \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e1998\u003c/span\u003e; Magrach et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Page \u0026amp; Williams, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2023b\u003c/span\u003e, \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2023a\u003c/span\u003e; Pascual Tudanca et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2024\u003c/span\u003e; Torn\u0026eacute;-Noguera et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2015\u003c/span\u003e; Valido et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2011\u003c/span\u003e) to positive (Pascual Tudanca et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2024\u003c/span\u003e; Valido et al., \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2011\u003c/span\u003e, \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), to nil (Dupont et al., \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2004\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eDespite numerous studies on the effects of honeybees on female plant fitness, we know little about the effects of honeybees on male fitness components such as pollen removal, deposition, germination (Gross \u0026amp; MacKay, \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e1998\u003c/span\u003e; Magrach et al., \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Page \u0026amp; Williams, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2023b\u003c/span\u003e, \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2023a\u003c/span\u003e; Torn\u0026eacute;-Noguera et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), and pollen flow. This biased focus may reflect the fact that fruit and seed production (female fitness) are easier to quantify than pollen removal, movement and germination (male fitness). Despite this bias, honeybee behavior gives us an idea of the effect it can have on male fitness. Honeybee behavior may decrease male fitness of native plants by recruiting workers to forage in valuable floral resources, leading to a substantial increase in visits to abundant flowering plants (Afik et al., \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2008\u003c/span\u003e; Visscher \u0026amp; Seeley, \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e1982\u003c/span\u003e; Von Frisch, \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e1974\u003c/span\u003e). Increased visits could in turn lead to increased pollen removal and decreased pollen availability for native pollinators. In addition, foraging honeybees tend to visit different flowers of the same plant individuals (Dupont et al., \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), decreasing pollen flow among different individuals and increasing self-pollination, resulting in the loss of genetic variability and increased inbreeding rates in self-compatible species (Brunet \u0026amp; Sweet, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Dupont et al., \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Karron et al., \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2004\u003c/span\u003e) or interfering with pollination in self-incompatible species (Mitchell et al., \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2009\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eWe studied the effect of honeybees on the male fitness of \u003cem\u003eLarrea divaricata\u003c/em\u003e, a dominant, self-compatible shrub species, in a dryland ecosystem in Villavicencio Nature Reserve, Mendoza, Argentina. Although the honeybee is naturalized in the Reserve (Chacoff et al., \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2012\u003c/span\u003e), we introduced managed hives to cause a drastic increase in the abundance of worker bees in the field so as to assess the impact of this exotic species on male plant fitness. We hypothesized that the increased abundance of \u003cem\u003eApis mellifera\u003c/em\u003e in Villavicencio Nature Reserve decreases male reproductive success of \u003cem\u003eLarrea divaricata\u003c/em\u003e, decreasing the number of mating couples and increasing pollen removal and pollen movement between nearby individuals and between flowers of the same individual, ultimately increasing the self-pollination and inbreeding rates.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eStudy site\u003c/p\u003e \u003cp\u003eWe worked in Villavicencio Nature Reserve (32\u0026deg; 32\u0026rsquo; S, 68\u0026deg; 57\u0026rsquo; O), Mendoza, in the Monte desert ecoregion. The predominant vegetation is xerophytic, dominated by low shrubs such as \u003cem\u003eZuccagnia punctata\u003c/em\u003e, \u003cem\u003eLarrea cuneifolia\u003c/em\u003e and \u003cem\u003eL\u003c/em\u003e. \u003cem\u003edivaricata\u003c/em\u003e (Chacoff et al., \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). We selected the latter as the focus of this study because of its high abundance in the study site, its widespread use as floral resource by various floral visitors, including the honeybee, and its highly overlapping flowering period with the time in which the managed hives were in the Reserve. \u003cem\u003eLarrea divaricata\u003c/em\u003e has bisexual yellow flowers and is self-compatible (Pascual Tudanca et al., \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2024\u003c/span\u003e; Rossi et al., \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e1999\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eExperimental design\u003c/p\u003e \u003cp\u003eTo assess the effect of hives on the male fitness of \u003cem\u003eLarrea divaricata\u003c/em\u003e, we distributed 125 hives among five beekeeping sites (25 hives per site) during the spring-summer of 2022. From each beekeeping site, we laid a 1000 m transect in which we established two sampling points: one near (200 m) and one far (1000 m) from the hives. In addition, we established a circular plot of 3 m in diameter at each sampling point.\u003c/p\u003e \u003cp\u003ePollen removal\u003c/p\u003e \u003cp\u003eTo evaluate the effect of the introduction of bee hives on pollen removal in \u003cem\u003eL\u003c/em\u003e. \u003cem\u003edivaricata\u003c/em\u003e, we selected 15 individuals at each sampling point. In each individual, we selected two branches with ten blossoms and applied a treatment: bagged (pollinator exclusion) and unbagged (open pollination). Once the flowers had opened, we collected five stamens per treatment and stored them in Eppendorf tubes with 70% alcohol. Once in the laboratory, we centrifuged the samples, separated the supernatant and added 0.2 ml of an alcoholic solution with detergent to separate the pollen grains (Dafni et al., \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). Finally, we vortexed the samples for five minutes to release the pollen grains, took three subsamples, and counted the pollen grains in a Neubauer chamber under a microscope (Dafni et al., \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). From these data we estimated the remaining pollen grains in each of the treatments.\u003c/p\u003e \u003cp\u003ePollen dispersal\u003c/p\u003e \u003cp\u003eTo assess the effect of the introduction of hives on pollen flow, we used fluorescent dye (Radha Colors) as pollen analogues to measure dispersal, as they are suitable for this type of study (Thomson et al., \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e1986\u003c/span\u003e; van Rossum et al., \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Waser \u0026amp; Price, \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e1982\u003c/span\u003e). In each plot, we tagged and geo-located all individuals of \u003cem\u003eL\u003c/em\u003e. \u003cem\u003edivaricata\u003c/em\u003e. When we found fewer than six flowering individuals within the plot at the time of the study, we selected the closest individuals to the plot until there were six flowering individuals. We marked and geo-located these new individuals. In addition, we counted the open flowers of each individual. On the morning, we applied the fluorescent dye with a brush to the anthers of 15 freshly opened flowers on five randomly selected individuals with one of the five colors and left exposed to pollinators. At dusk on the second day, we examined all open flowers of individuals of the same species within the plot with a UV lamp and quantified by color discrimination the number of flowers with fluorescent dye. From these data we estimated the self-pollination rate (percentage of flowers with fluorescent dye from the same individual), the outcrossing rate (percentage of flowers with fluorescent dye from another individual), the number of mating couples, the number of self-pollinated flowers, and the pollen dispersal distance.\u003c/p\u003e \u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eData analysis\u003c/h2\u003e \u003cp\u003eTo assess the effect of distance to hives on male fitness we used generalized linear mixed models (GLMM, Bolker et al., \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2009\u003c/span\u003e) with the number of pollen grains remaining in the anthers, pollen dispersal distance, self-pollination rate, and outcrossing rate and, where appropriate, treatment and total number of flowers as response variables, distance to hives as a fixed predictor, and site as a random predictor. For the number of remaining pollen grains, self-pollination rate and outcrossing rate we fitted separate Poisson GLMMs; however, when we detected overdispersion we performed a Negative Binomial GLMM instead. For pollen dispersal distance we fitted three different models: Gaussian GLMM, Poisson GLMM, and Negative Binomial GLMM and selected the best model using Akaike\u0026rsquo;s Information Criterion (AIC). We performed GLMMs using the glmmTMB function of the glmmTMB package (Bates et al., \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Finally, to study the effect of distance to hives on the number of couples and the number of self-pollinated flowers we performed two-sample permutation tests (Manly, \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) with the mean as the location parameter using the twoSamplePermutationTestLocation function of the EnvStats package of R statistical software (Millard et al., \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2018\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cp\u003ePollen removal\u003c/p\u003e \u003cp\u003eFlowers under pollinator exclusion had a higher number of remaining pollen grains compared to flowers exposed to pollinators (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ea, Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e). However, distance to hives and the distance-treatment interaction had no detectable effects on the number of remaining pollen grains (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ea, Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e), which indicates that pollen removal did not vary with distance to the hives.\u003c/p\u003e \u003cp\u003ePollen dispersal\u003c/p\u003e \u003cp\u003ePollen dispersal distance increased by 32% with distance to hives (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003eb, Tables S2-S3), while self-pollination and outcrossing rates did not vary with distance to hives (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003ec-d, Table S3). Finally, the number of mating couples (permutation test, p\u0026thinsp;=\u0026thinsp;0.76) and the number of self-pollinated flowers (permutation test, p\u0026thinsp;=\u0026thinsp;0.68) did not vary with distance to the hives.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eWe have shown that the increased abundance of honeybees in Villavicencio Nature Reserve partially influenced the male fitness of \u003cem\u003eLarrea divaricata\u003c/em\u003e. Thus, close to the hives pollen dispersed shorter distances than away from the hives, with potential consequences for gene flow. However, other aspects of male fitness did not vary with distance to the hives, suggesting a generally weak impact of honeybees on male fitness.\u003c/p\u003e \u003cp\u003eWe found that pollen dispersal distance decreased near honeybee hives, as expected. This negative effect of honeybee abundance may be attributed to the behavior of this bee when visiting a flower. Upon collecting pollen from the flower, the honeybee packs it into the corbicula, thereby reducing the pollen available for transfer to other flowers. This behavior, called grooming, leads to reduced pollen dispersal distance in other corbiculaate bees (Castellanos et al., \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Holmquist et al., \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). Decreased pollen dispersal distance near honeybee hives could in turn lead to increased self-pollination and, as \u003cem\u003eL\u003c/em\u003e. \u003cem\u003edivaricata\u003c/em\u003e is a self-compatible species, increasing inbreeding (Dupont et al., \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; England et al., \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2001\u003c/span\u003e). In the long term, increased inbreeding could affect population persistence. However, we found no effects of hives on outcrossing and self-pollination rates, the number of mating couples and the number of self-pollinated flowers, which indicates only slight effects on male fitness and population persistence.\u003c/p\u003e \u003cp\u003eBased on the behavior of \u003cem\u003eApis mellifera\u003c/em\u003e we also expected increased pollen removal near the hives. However, we found no such effects, in contrast to previous studies (Page \u0026amp; Williams, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2023b\u003c/span\u003e; Torn\u0026eacute;-Noguera et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). This lack of effect of proximity to honeybee hives on pollen removal may be a consequence of our experimental design, as we had a low number of hives, compared with other studies (Page \u0026amp; Williams, \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2023b\u003c/span\u003e, Torn\u0026eacute;-Noguera et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). In addition, sampling took place during the flowering peak, when the abundance of floral resources is at its highest. Thus, the increased number of honeybee visits resulting from the few introduced hives could have been insufficient to reduce pollen removal in \u003cem\u003eLarrea divaricata\u003c/em\u003e during flowering peak. Honeybees are likely to have a stronger effect at the beginning and the end of flowering or in drought years, when floral resources are scarce.\u003c/p\u003e \u003cp\u003eDespite the observed weak effects on male fitness, increased honeybee abundance could cascade through the community, affecting other species. For example, competition between honeybees and native pollinators for floral resources may lead to decreased frequency of visits by native pollinators and a shift in foraging to alternative plants (Dupont et al., \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Henry \u0026amp; Rodet, \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Sun et al., \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Torn\u0026eacute;-Noguera et al., \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2015\u003c/span\u003e) that are sometimes taxonomically and phenotypically distant from their preferred plants (Roubik \u0026amp; Villanueva-Guti\u0026eacute;rrez, \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Schaffer et al., \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e1993\u003c/span\u003e). Switching to nonpreferred resource plant species could ultimately affect the reproductive success of native pollinators.\u003c/p\u003e \u003cp\u003eIn conclusion, the increased abundance of the honeybee in an arid ecosystem partially influenced the male fitness of a dominant shrub, \u003cem\u003eLarrea divaricata\u003c/em\u003e, by modifying pollen dispersal distance. This study advances our understanding about the potential ecological effects of the honeybee, a widespread nonnative species that has invaded many ecosystems throughout the world. Given the importance of nature reserves as reservoirs of biodiversity and that beekeeping has increasingly turned to protected areas, our study can contribute to guide decision making about the introduction of managed honeybee hives in nature reserves.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003eStatements and declarations\u003c/p\u003e\n\u003cp\u003eThis work was supported by Fundaci\u0026oacute;n Villavicencio and Fondo para la Investigaci\u0026oacute;n Cient\u0026iacute;fica y Tecnol\u0026oacute;gica (Grant number PICT-2018-1272)\u003c/p\u003e\n\u003cp\u003eCompeting interests\u003c/p\u003e\n\u003cp\u003eThe authors have no relevant financial or no-financial interests to disclose.\u003c/p\u003e\n\u003cp\u003eData availability statement:\u003c/p\u003e\n\u003cp\u003eData and code are provied as private-for-peer review via the following link: https://figshare.com/s/31b4610d33473261f14e\u003c/p\u003e\n\u003cp\u003eAuthors\u0026rsquo; contributions\u003c/p\u003e\n\u003cp\u003eMar\u0026iacute;a P. Pascual Tudanca and Diego P. V\u0026aacute;zquez conceived the ideas and designed methodology; Mar\u0026iacute;a P. Pascual Tudanca and Alejandra V. Medero conducted field and laboratory work; Mar\u0026iacute;a P. Pascual Tudanca and Diego P. V\u0026aacute;zquez analyzed the data; Mar\u0026iacute;a P. Pascual Tudanca led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.\u003c/p\u003e\n\u003cp\u003eAcknowledgments\u003c/p\u003e\n\u003cp\u003eWe thank the administration of Villavicencio Nature Reserve and the Direction of Renewable Natural Resources of Mendoza for permission to conduct this study. We are also grateful to Villavicencio personnel for providing logistic assistance and supplies during the study.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAfik, O., Dag, A., \u0026amp; Shafir, S. (2008). 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A Comparison of Pollen and Fluorescent Dye Carry‐Over by Natural Pollinators of Ipomopsis. \u003cem\u003eEcology\u003c/em\u003e, \u003cem\u003e63\u003c/em\u003e(4), 1168\u0026ndash;1172.\u003c/li\u003e\n\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Drylands, Honeybee introduction, Male fitness, Native plants, Natural Reserves, Pollination","lastPublishedDoi":"10.21203/rs.3.rs-4318764/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4318764/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eBiological invasions represent one of the main threats to biodiversity. The honeybee has been deliberately introduced into a wide range of habitats worldwide. Currently, beekeeping is turning to natural areas in search of better honey quality. This practice can boost honeybee abundance, with potential ecological consequences in the local ecosystems. Although previous studies have considered how female plant fitness responds to honeybees, we know little about their potential effects on male fitness. We studied experimentally the effect of increased honeybee abundance on male fitness of a dominant shrub, \u003cem\u003eLarrea divaricata\u003c/em\u003e, in a dryland ecosystem in Villavicencio Nature Reserve, Mendoza, Argentina. In replicated study plots near and far from managed hives we estimated pollen removal and dispersal, self-pollination and outcrossing rates, the number of mating couples, and self-pollinated flowers. Honeybees restricted pollen dispersal distance, with a potential effect on male fitness. Our findings have important implications for maintaining the reproduction and persistence of wild plants exposed to nonnative pollinators and can serve as a guide to decision making about the introduction of managed honeybee hives in nature reserves.\u003c/p\u003e","manuscriptTitle":"Beekeeping in a natural area affects male fitness of a native plant","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-05-13 18:25:35","doi":"10.21203/rs.3.rs-4318764/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"dda871f4-045a-4d02-b9b7-9f4648b19f1f","owner":[],"postedDate":"May 13th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-06-13T20:50:54+00:00","versionOfRecord":[],"versionCreatedAt":"2024-05-13 18:25:35","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-4318764","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4318764","identity":"rs-4318764","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}