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High Visitation Rate of Oil Bees May Increase Pollination Efficiency of Couepia Uiti in Pantanal Wetland

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High Visitation Rate of Oil Bees May Increase Pollination Efficiency of Couepia Uiti in Pantanal Wetland High visitation rate of oil bees may increase pollination efficiency of Couepia uiti in Pantanal wetland Samuel Boff, Gladys F. A. Melo-De-Pinna, Arnildo Pott, Andréa Cardoso Araujo To cite this version: Samuel Boff, Gladys F. A. Melo-De-Pinna, Arnildo Pott, Andréa Cardoso Araujo. High visitation rate of oil bees may increase pollination efficiency of Couepia uiti in Pantanal wetland. Apidologie, Springer Verlag, 2018, 49 (6), pp.747-758. 10.1007/s13592-018-0598-7. hal-02334981 HAL Id: hal-02334981 https://hal.archives-ouvertes.fr/hal-02334981 Submitted on 28 Oct 2019 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) 49:747–758 Original article * INRA, DIB and Springer-Verlag France SAS, part of Springer Nature, 2018 DOI: 10.1007/s13592-018-0598-7 High visitation rate of oil bees may increase pollination efficiency of Couepia uiti in Pantanal wetland 1,2 3 1 Samuel BOFF , Gladys F. A. MELO-DE-PINNA , Arnildo POTT , 4 Andréa Cardoso ARAUJO 1Programa de Pós-Graduação em Biologia Vegetal, Universidade Federal de Mato Grosso do Sul, Campo Grande, Brazil 2Department of Food, Environmental and Nutritional Sciences, University of Milan, Via Celoria 2, 20133, Milan, Italy 3Programa de Pós-Graduação em Botânica, Universidade de São Paulo, São Paulo, Brazil 4Laboratório de Ecologia, Instituto de Biociências, Universidade Federal de Mato Grosso do Sul, Campo Grande, Brazil Received6February2018– Revised 27 June 2018 – Accepted 7 August 2018 Abstract – Pollen transfer to the stigma is the primary mechanism of sexual reproduction in plants. Among bee species that act as pollen vectors and pollinators, attributes such as floral visitation rate, synchrony with the receptive phase of the flower, compatibility between flower shape and foraging behavior, and morphological traits are often used to infer pollination efficiency. Herein, we evaluate visitation frequency and behavior of bee species on Couepia uiti (Chrysobalanaceae) flowers in the southern Pantanal, Brazil. Additionally, after experimental manipulation of flower visitation and by accompanying pollen tube growth in the pistil after one single visit to the flowers, we were able to pinpoint the roles of Centris spilopoda and Apis mellifera on the pollination of C. uiti . Centris spilopoda was the most important pollinator of C. uiti in the study area. In fact, we found that this oil bee might enhance plant reproductive success by almost 40% after a single visit. In addition to its high abundance, the efficiency of C. spilopoda as pollinator may be explained by its tight synchrony with pollen liberation and stigmatic receptivity of flowers of C. uiti. bee activity and stigmatic receptivity / floodplain / Centridini / pollen tube / single visit 1. INTRODUCTION but many species depend on xenogamic pollen for reproduction (Vilas Boas et al. 2013; Sazan et al. Pollination is the mechanism whereby plants 2014). Xenogamic pollination, also known as with flowers are sexually reproduced (Endress cross-pollination, can influence fruit quality and 1994; Proctor et al. 2003). For pollination to be seed viability (Schneider et al. 2009; Chautá- effective (i.e., pollen tube growth occurs and Mellizo et al. 2012; Stein et al. 2017). reaches the ovules leading to their fertilization), Bees are one group of animals that are responsi- pollen grains need to be transferred to stigma(s) ble for increased plant reproduction success via that are reproductively compatible (Hiscock and cross-pollination (Ollerton et al. 2011) and pollinate Mcinnis 2003). Some plants are self-compatible several species, especially in tropical areas (Endress (Brauner and Gottlieb 1987;Torängetal.2017), 1994; Roubik 1989). An efficient bee pollinator may present, besides synchrony with the receptive Electronic supplementary material The online version of phase of the flower, morphological characteristics this article (https://doi.org/10.1007/s13592-018-0598-7) that are compatible with flower shape, while contains supplementary material, which is available to flowers offer resources that are compatible with authorized users. the physio-behavioral requirements of bees. Corresponding author: S. Boff, Centridini bees (Hymenoptera: Apidae) have pan- [email protected] tropical distribution (Moure et al. 2012) and present Manuscript editor: Alexandra Klein tight interaction with plants species that offer oil as 748 S. Boff et al. floral resource (Vogel 1974, 1990; Vinson et al. In the Pantanal, which is the world’s largest trop- 1997; Teixeira and Machado 2000; Martins et al. ical wetland (Assine et al. 2015), it grows as a 2013). These bees are potential pollinators of sev- pioneer treelet, with a height of 3–6 m and a wide eral wild nectariferous and polliniferous species canopy that nearly reaches the ground. It flowers (e.g., Fischer and Gordo 1993; Aguiar et al. 2003; between August and November (Pott and Pott Aguiar and Gaglianone 2008), including some eco- 1994), and fruits, which are consumed by humans nomically important plant crops such as (Bortolotto et al. 2018), birds, and other animal Anacardium occidentale (Freitas and Paxton species, are produced around April–May during 1998; Holanda-Neto et al. 2002), Bertholletia flood season in the Southern Pantanal. Flowers are excelsa (Cavalcante et al. 2018), Malpighia polystemonous and uniovulate. A previous study punicifolia and M. emarginata (Raw 1979; about the breeding system of C. uiti reported Oliveira and Schlindwein 2009, respectively), continuous nectar production with increased sugar Passiflora alata and Solanum lycopersicum concentration around 10:00 am. Pollen liberation (Gaglianone et al. 2010;Gaglianoneetal.2018), starts around 9:30 am and stigmatic receptivity at Psidium guajava (Giannini et al. 2015), and Trifo- 12:00 am. Manual cross-pollination resulted in lium pratense (Macfarlane 2018). 11% fruit set (xenogamy). In natural conditions, Plants attract pollinators at a long distance where flowers are mostly visited by honeybees, through scents/odors as well as by the number fruit set did not exceed 15% (Paulino-Neto 2007). of flowers, known as floral display. Other traits Herein, we present data about the foraging be- such as flower shape, flower color(s), and sugar havior of several bee species and evaluate the concentration in the nectar may work as short visitation rates of the most frequent species. Fur- distances attractants (e.g., Waser and Ollerton thermore, as Couepia uiti presents several different 2006; Ebeling et al. 2008). By presenting a floral visitors (Paulino-Neto 2007), we test if pollen greater floral display, plants may receive more transfer efficiency differs between two frequent bee floral visitors and, consequently, enhance fruit species. To answer this question, we carried out a andseedproduction(KearnsandInouye1993; field experiment to evaluate the pollination success Mayfield et al. 2001). Information on fruit/seed of a native solitary oil bee and the exotic eusocial set, as well as analysis of pollen tube growth in honeybee by detection of pollen tube growth in the the style and ovary, are measurements employed style after one single flower visit. to evaluate pollinator efficiency in several plant species (e.g., Motten 1986;Richards1986; Zhang et al. 2015). 2. MATERIAL AND METHODS Pollen tube growth in the pistil results from the deposition of compatible pollen grains onto the 2.1. Study area stigmatic region of the flower. Despite polarized and continuing growth towards the ovule after This study was carried out in the southern emergence in the stigma, pollen tube growth can Pantanal, sub-regions of Miranda and Abobral, be interrupted a posteriori due to late acting self- in a partially flooded area of the Abobral river incompatibility (Seavey and Bawa 1986). How- (19° 28′ 34.7″ S, 57° 02′ 37.8″ W) where trees of ever, even with late incompatibility, the presence C. uiti are naturally intermingled with the shrub of a pollen tube indicates the pollinators’ efficien- Byrsonima cydoniifolia A. Juss. (Malpighiaceae). cy in carrying pollen to the stigma. Field observations took place between the 18th Couepia uiti (Mart. and Zucc.) Benth. and 21st of October 2007 between 07:00 am and (Chrysobalanaceae) is a self-incompatible plant 4:00 pm. From the 16th–19th of September 2008, species relying in cross-pollination to produce we carried out additional observations of the same fruits (Paulino-Neto 2007). This plant species pre- population of C. uiti , but we did not evaluate sents wide distribution in Brazil (Grandtner and visitor frequencies. During both years, field ob- Chevrette 2013), usually occurring on floodplains servations coincided with the end of the dry sea- of small rivers and streams (Pott and Pott 1994). son in the area. Pollination efficiency of oil bees in wetlands 749 2.2. Floral visitors and pollinators After we recorded visitation and behavior, we collected bees using an entomological net. All col- First, flower visitors were sampled and recog- lected specimens were killed in a jar with ethyl nized for 2 h during 4 days (total 8 h) before acetate vapor, mounted, and deposited into the starting the experiment. Once we identified the zoological collection at the Universidade Federal four most frequent bee species visiting the de Mato Grosso do Sul (ZUFMS). Some speci- flowers, we started recording their visitation fre- mens were deposited into the Coleção quencies. We recorded visitation between 7:00 am Entomológica Paulo Nogueira Neto, Departamento and 16:00, with 10 min of focal observations de Ecologia, Instituto de Biociências, Universidade during each hour, totaling 100 min day−1,andin de São Paulo. We also collected bees that we 4 days totaling 400 min of observation.
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