[en] Stingless bees are effective pollinators of native tropical flora. Their environmental service maintains flow of pollen through pollination, increase reproductive success and influence genetic structure in plants. The management of stingless bees "meliponiculture", is an activity limited to the countryside in Ecuador. The lack of knowledge of their managers about pollen resources can affect the correct maintenance/production of nests. The objective is to identify botanical families and genera of pollen grains collected by stingless bees by morphological features and differentiate potential species using geometric morphometry. Thirty-six pot pollen samples were collected from three Ecuadorian provinces located in two climatically different zones. Pollen type identification was based on the Number, Position, Character system. Using morphological features, the families and genera were established. Morphometry landmarks were used to show variation for species differentiation. Abundance, diversity, similarity and dominance indices were established by counting pollen grains, as well as spatial distribution relationships by means of Poisson regression. Forty-six pollen types were determined in two study areas, classified into 27 families and 18 genera. In addition, it was possible to identify more than one species, classified within the same family and genus, thanks to morphometric analysis. 1148 ± 799 (max 4211; min 29) pollen grains were counting in average. The diversity showed a high richness, low dominance and similarity between pollen resources. Families Melastomataceae and Asteraceae, genera Miconia and Bidens, were found as the main pollen resources. The stingless bee of this study are mostly generalist as shown the interaction network. The results of the present survey showed that stingless bees do not collect pollen from a single species, although there is evidence of a predilection for certain plant families. The diversity indexes showed high richness but low uniformity in the abundance of each family identified. The results of the study are also meaningful to the meliponiculture sector as there is a need to improve management practices to preserve the biodiversity and the environment.
Disciplines :
Veterinary medicine & animal health
Author, co-author :
Ocaña-Cabrera, Joseline Sofía; Laboratorio de Biotecnología Animal, Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador ; Grupo de Investigación en Sanidad Animal y Humana (GISAH), Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador ; Research Unit of Epidemiology and Risk analysis applied to Veterinary Sciences (UREAR- ULg), Fundamental and Applied Research for Animal and Health (FARAH) Center, Department of Infections and Parasitic Diseases, Faculty of Veterinary Medicine, University of Liege, Liege, Province of Liège, Belgium
Liria, Jonathan; Grupo de Investigación en Población y Ambiente, Universidad Regional Amazónica IKIAM, Tena, Napo, Ecuador
Vizuete, Karla; Laboratorio de Caracterización de Nanomateriales, Centro de Nanociencia y Nanotecnología, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador
Cholota-Iza, Cristina; Laboratorio de Biotecnología Animal, Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador ; Grupo de Investigación en Sanidad Animal y Humana (GISAH), Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador
Espinoza-Zurita, Fernando; Grupo de Investigación en Sanidad Animal y Humana (GISAH), Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador
Saegerman, Claude ; Université de Liège - ULiège > Département des maladies infectieuses et parasitaires (DMI) > Epidémiologie et analyse des risques appliqués aux sciences vétérinaires
Martin-Solano, Sarah; Laboratorio de Biotecnología Animal, Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador ; Grupo de Investigación en Sanidad Animal y Humana (GISAH), Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador
Debut, Alexis; Laboratorio de Caracterización de Nanomateriales, Centro de Nanociencia y Nanotecnología, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador
Ron-Román, Jorge; Laboratorio de Biotecnología Animal, Carrera de Ingeniería en Biotecnología, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador ; Grupo de Investigación en Sanidad Animal y Humana (GISAH), Carrera de Ingeniería Agropecuaria, Departamento de Ciencias de la Vida y de la Agricultura, Universidad de las Fuerzas Armadas ESPE, Sangolquí, Pichincha, Ecuador
Language :
English
Title :
Pollen preferences of stingless bees in the Amazon region and southern highlands of Ecuador by scanning electron microscopy and morphometry.
ARES - Académie de Recherche et d'Enseignement Supérieur ULiège - Université de Liège
Funding text :
This study was funded by: The Academy of Research and Higher Education (ARES) through the Synergy project entitled “Improvement of meliponiculture in Ecuador through applied scientific research, technology transfer and training” The University of Liège. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. This work would not have been accomplished without the help of Ecuadorian meliponicultors, regular and thesis students for the Ecuadorian universities.
Grüter C. Evolution and Diversity of Stingless Bees. In: Stingless Bees: Their Behaviour, Ecology and Evolution [Internet]. Cham: Springer International Publishing; 2020 [cited 2021 Sep 2]. (Fascinating Life Sciences). Available from: http://link.springer.com/10.1007/978-3-030-60090-7
Michener CD. The bees of the world. 2nd ed. Baltimore: Johns Hopkins University Press; 2007. 953 p.
Martins AC, Melo GAR, Renner SS. The corbiculate bees arose from New World oil-collecting bees: Implications for the origin of pollen baskets. Mol Phylogenet Evol. 2014; 80:88–94. https://doi.org/10.1016/j.ympev.2014.07.003 PMID: 25034728
Kerr WE, Maule V. Geographic Distribution of Stingless Bees and Its Implications (Hymenoptera: Apidae). J N Y Entomol Soc. 1964; 72(1):2–18.
Vit P, Pedro SRM, Maza F, Ramírez VM, Frisone V. Diversity of Stingless Bees in Ecuador, Pot-Pollen Standards, and Meliponiculture Fostering a Living Museum Meliponini of the World. In: Vit P, Pedro SRM, Roubik DW, editors. Pot-Pollen in Stingless Bee Melittology [Internet]. Cham: Springer International Publishing; 2018 [cited 2021 Jul 26]. p. 207–27. Available from: http://link.springer.com/10.1007/ 978-3-319-61839-5_15
Jørgensen PM, Ulloa C, Maldonado C. Riqueza de plantas vasculares. In: Botánica Económico de los Andes Centrales [Internet]. 2006. p. 35–50. Available from: https://isbn.cloud/9789995401214/botanica-economica-de-los-andes-centrales/
De la Torre L, Navarrete H, Muriel P, Macía, M, Balslev H. Resultados—Enciclopedia de las plantas útiles del Ecuador. In: Enciclopedia de las plantas útiles del Ecuador [Internet]. Quito & Aarhus.: Herbario QCA de la Escuela de Ciencias Biológicas de la Pontificia Universidad Católica del Ecuador & Herbario AAU del Departamento de Ciencias Biológicas de la Universidad de Aarhu; 2008 [cited 2021 Jul 26]. Available from: https://bibdigital.rjb.csic.es/records/item/16016-enciclopedia-de-las-plantasutiles-del-ecuador?offset=3
Giannini TC, Garibaldi LA, Acosta AL, Silva JS, Maia KP, Saravia AM, et al. Native and Non-Native Supergeneralist Bee Species Have Different Effects on Plant-Bee Networks. PLoS ONE. 2015; 10 (9):1–13. https://doi.org/10.1371/journal.pone.0137198 PMID: 26356234
Agüero J, Rollin O, Torretta J, Aizen M, Requier F, Garibaldi L. Impactos de la abeja melífera sobre plantas y abejas silvestres en hábitats naturales. Rev Científica Ecol Medio Ambiente. 2018; 27 (2):60–9.
Potts S. Recording pollinator behaviour on flowers. Dafini A, Keva P, Husband C, editors. Cambridge, Ontario: Practical Pollination Biology. UNSPECIFIED; 2005. 401– 434, 329–339 p.
Grüter C. Nesting Biology. In: Grüter C, editor. Stingless Bees: Their Behaviour, Ecology and Evolution [Internet]. Cham: Springer International Publishing; 2020 [cited 2021 Sep 2]. p. 87–130. (Fascinating Life Sciences). Available from: https://doi.org/10.1007/978-3-030-60090-7_3
Michener CD. The social behavior of the bees: a comparative study. Cambridge (Mass.): Harvard University Press; 1974. xii+404.
Chapuisat M, Oppliger A, Magliano P, Christe P. Wood ants use resin to protect themselves against pathogens. Proc Biol Sci. 2007; 274(1621):2013–7. https://doi.org/10.1098/rspb.2007.0531 PMID: 17535794
Massaro FC, Brooks PR, Wallace HM, Russell FD. Cerumen of Australian stingless bees (Tetragonula carbonaria): gas chromatography-mass spectrometry fingerprints and potential anti-inflammatory properties. Naturwissenschaften 2011; 98(4):329–37. https://doi.org/10.1007/s00114-011-0770-7 PMID: 21347735
Choudhari MK, Punekar SA, Ranade RV, Paknikar KM. Antimicrobial activity of stingless bee (Trigona sp.) propolis used in the folk medicine of Western Maharashtra, India. J Ethnopharmacol. 2012; 141 (1):363–7. https://doi.org/10.1016/j.jep.2012.02.047 PMID: 22425711
Messer AC. Fresh Dipterocarp Resins Gathered by Megachild Bees Inhibit Growth of Pollen-Associated Fungi. Biotropica. 1985; 17(2):175–6.
Chinh TX, Sommeijer MJ, Boot WJ, Michener CD. Nest and colony characteristics of three stingless bee species in Vietnam with the first description of the nest of Lisotrigona carpenteri (Hymenoptera: Apidae: Meliponini). J Kans Entomol Soc. 2005; 78(4):363–72.
Van Benthem FDJ, Imperatriz-Fonseca VL, Velthuis HHW. Biology of the stingless bee Plebeia remota (Holmberg): observations and evolutionary implications. Insectes Sociaux. 1995; 42(1):71–87.
Kerr WE, Sakagami SF, Zucchi R, Portugal-Araújo V de, Camargo J de. Observações sobre a arquitetura dos ninhos e comportamento de algumas espécies de abelhas sem ferrão das vizinhanças de Manaus, Amazonas (Hymenoptera, Apoidea). In: Atas do Simpósio sobre a biota Amazônica. Conselho Nacional de Pesquisa Rio de Janeiro; 1967. p. 255–309.
Crane E. The Past and Present Status of Beekeeping with Stingless Bees. Bee World. 1992; 73 (1):29–42.
Roubik DW. 100 Species of Meliponines (Apidae: Meliponini) in a Parcel of Western Amazonian Forest at Yasuní Biosphere Reserve, Ecuador. In: Vit P, Pedro SRM, Roubik DW, editors. Pot-Pollen in Stingless Bee Melittology [Internet]. Cham: Springer International Publishing; 2018 [cited 2021 Jul 26]. p. 189–206. Available from: http://link.springer.com/10.1007/978-3-319-61839-5_14
Chazdon RL, Harvey CA, Komar O, Griffith DM, Ferguson BG, Martínez-Ramos M, et al. Beyond Reserves: A Research Agenda for Conserving Biodiversity in Human-Modified Tropical Landscapes. Biotropica. 2009; 41(2):142–53.
Delgado C, Mejía K, Rasmussen C. Management practices and honey characteristics of Melipona eburnea in the Peruvian Amazon. Ciênc Rural [Internet]. 2020 Oct 23 [cited 2021 Jul 26]; 50. Available from: http://www.scielo.br/j/cr/a/JJqTZV9FVfYVCFLPTvYwSCf/?lang=en
Giacobino A, Bulacio Cagnolo N, Merke J, Orellano E, Bertozzi E, Masciangelo G, et al. Risk factors associated with the presence of Varroa destructor in honey bee colonies from east-central Argentina. Prev Vet Med. 2014; 115(3–4):280–7. https://doi.org/10.1016/j.prevetmed.2014.04.002 PMID: 24794646
Maggi M, Antúnez K, Invernizzi C, Aldea P, Vargas M, Negri P, et al. Honeybee health in South America. Apidologie. 2016; 47(6):835–54.
Kremen C, Williams NM, Thorp RW. Crop pollination from native bees at risk from agricultural intensification. Proc Natl Acad Sci. 2002 Dec 24; 99(26):16812–6. https://doi.org/10.1073/pnas.262413599 PMID: 12486221
Buchmann SL. Bees Use Vibration to Aid Pollen Collection from Non-Poricidal Flowers. J Kans Entomol Soc. 1985; 58(3):517–25.
Nates Parra G. Abejas silvestres y polinización [Internet]. Manejo Integrado de Plagas y Agroecología. 2005 [cited 2021 Sep 25]. Available from: http://orton.catie.ac.cr/repdoc/A1865e/A1865e.pdf
Roubik DW. Foraging and pollination. In: Ecology and Natural History of Tropical Bees [Internet]. Cambridge: Cambridge University Press; 1989 [cited 2021 Sep 15]. p. 25–160. (Cambridge Tropical Biology Series). Available from: https://www.cambridge.org/core/books/ecology-and-natural-historyof-tropical-bees/foraging-and-pollination/D366A460F5A6C9C82BDB63DD8004A34D
Ollerton J. Pollinator Diversity: Distribution, Ecological Function, and Conservation. Annu Rev Ecol Evol Syst. 2017; 48(1):353–76
Jaffé R, Pope N, Carvalho AT, Maia UM, Blochtein B, Carvalho CAL de, et al. Bees for Development: Brazilian Survey Reveals How to Optimize Stingless Beekeeping. PLOS ONE. 2015; 10(3):e0121157. https://doi.org/10.1371/journal.pone.0121157 PMID: 25826402
Guerrero S. Competencia o partición de nicho por los recursos en abejas nativas Melipona mimetica y Scaptotrigona sp. En un bosque seco al sur de Ecuador. [Internet] [Tesis de pregrado]. [ Ecuador]: Universidad Técnica Particular de Loja 2016 [cited 2021 Sep 25]. Available from: http://dspace.utpl.edu.ec/handle/123456789/14588
Ramalho M, Giannini TC, Malagodi-Braga KS, Imperatriz-Fonseca VL. Pollen Harvest by Stingless Bee Foragers (Hymenoptera, Apidae, Meliponinae). Grana. 1994; 33(4–5):239–44.
Aizen M, Harder L. Expanding the limits of the pollen-limitation concept: Effects of pollen quantity and quality. Ecology. 2007; 88(2):271–81. https://doi.org/10.1890/06-1017 PMID: 17479745
Traveset A, Richardson DM. Biological invasions as disruptors of plant reproductive mutualisms. TRENDS Ecol Evol. 2006; 21(4):208–16. https://doi.org/10.1016/j.tree.2006.01.006 PMID: 16701087
Whelan RJ, Ayre DJ, Beynon FM. The birds and the bees: pollinator behaviour and variation in the mating system of the rare shrub Grevillea macleayana. Ann Bot. 2009;1395–401 https://doi.org/10.1093/aob/mcp091 PMID: 19403627
Stanley RG, Linskens HF. Development. In: Stanley RG, Linskens HF, editors. Pollen: Biology Biochemistry Management [Internet]. Berlin, Heidelberg: Springer; 1974 [cited 2021 Sep 27]. p. 3–12. Available from: https://doi.org/10.1007/978-3-642-65905-8_1
Cobo A. Alimentación de las Abejas. In: Publicaciones de Extension Agraria [Internet]. España; 2011 [cited 2021 Sep 25]. p. 19. Available from: https://www.miteco.gob.es/ministerio/pags/biblioteca/hojas/hd_1977_22.pdf
Solomon J, Stimmel H. Tropicos Specimen Data [Internet]. Tropicos Specimen Data. Missouri Botanical Garden. 2021 [cited 2021 Oct 25]. Available from: https://www.gbif.org/es/dataset/7bd65a7a-f762-11e1-a439-00145eb45e9a
Bittrich V, Hartmann H. The Aizoaceae—a new approach. Bot J Linn Soc. 1988; 97(3):239–54.
Hartmann HEK. Aizoaceae. In: Hartmann HEK, editor. Illustrated Handbook of Succulent Plants: Aizoaceae A-E [Internet]. Berlin, Heidelberg: Springer; 2002 [cited 2022 Jan 9]. p. 9–268. (Illustrated Handbook of Succulent Plants). Available: from: https://doi.org/10.1007/978-3-642-56306-5_2
Jaramillo P, Trigo M del M. Guía rápida de Polen de las Islas Galápagos [Internet]. Parque Nacional Galápagos. Universidad de Málaga.; 2011 [cited 2021 Aug 18]. Available from: https://www.darwinfoundation.org/en/publications/identification-guides/guia-rapida-de-polen-de-las-islasgalapagos
Caccavari De Filice M. Polen de Alismataceae y Butomaceae de la flora bonaerense. 1983; 22(1–4):237–53.
Haynes RR, Holm-Nielsen LB. The Alismataceae. Flora Neotropica. 1994; 64:1–112.
Haynes RR, Les DH, Holm-Nielsen LB. Alismataceae. In: Kubitzki K, editor. Flowering Plants Monocotyledons: Alismatanae and Commelinanae (except Gramineae) [Internet]. Berlin, Heidelberg: Springer; 1998 [cited 2021 Aug 18]. p. 11–8. (The Families and Genera of Vascular Plants; vol. 4). Available from: https://doi.org/10.1007/978-3-662-03531-3_4
Heard TA. The role of stingless bees in crop pollination. Annu Rev Entomol. 1999; 44(1):183–206. https://doi.org/10.1146/annurev.ento.44.1.183 PMID: 15012371
Chakraborty P, Gupta-Bhattacharya S, Roy I, Chanda S. Identification of shared allergenic components from four common and dominant pollen taxa of Arecaceae. Curr Sci. 2004; 86(11):1539–43.
Basu S, Sengupta R, Zandi P. Arecaceae: The Majestic Family of Palms [Internet]. Encyclopedia of Earth. 2014. Available from: http://www.eoearth.org/view/article/53dc075c0cf2541de6d02774
Hou D. Anacardiaceae. Flora Malesiana—Ser 1 Spermatophyta. 1974; 8(1):395–548.
Pell SK, Mitchell JD, Miller AJ, Lobova TA. Anacardiaceae. In: Kubitzki K, editor. Flowering Plants Eudicots: Sapindales, Cucurbitales, Myrtaceae [Internet]. Berlin, Heidelberg: Springer; 2011 [cited 2021 Aug 18]. p. 7–50. (The Families and Genera of Vascular Plants). Available from: https://doi.org/10.1007/978-3-642-14397-7_3
Beltrán H, Granda A, León B, Sagástegui A, Sánchez I, Zapata M. Asteraceae endémicas del Perú. Rev Peru Biol. 2006; 13(2):64s–164s
Moreira-Muñoz A, Muñoz-Schick M. Classification, diversity, and distribution of Chilean Asteraceae: implications for biogeography and conservation. Divers Distrib. 2007; 13(6):818–28
Berberidaceae Loconte H. In: Kubitzki K, Rohwer JG, Bittrich V, editors. Flowering Plants ∙ Dicotyledons: Magnoliid, Hamamelid and Caryophyllid Families [Internet]. Berlin, Heidelberg: Springer; 1993 [cited 2021 Aug 18]. p. 147–52. (The Families and Genera of Vascular Plants). Available from: https://doi.org/10.1007/978-3-662-02899-5_14
Landrum LR. Revision of Berberis (Berberidaceae) in Chile and Adjacent Southern Argentina. Ann Mo Bot Gard. 1999; 86(4):793–834.
Daly DC de B, Fine PVA, Martínez-Habibe MC. Burseraceae: a model for studying the Amazon flora. Rodriguésia. 2012; 63:021–30.
Goetghebeur P. Cyperaceae. In: Kubitzki K, editor. Flowering Plants Monocotyledons: Alismatanae and Commelinanae (except Gramineae) [Internet]. Berlin, Heidelberg: Springer; 1998 [cited 2021 Aug 18]. p. 141–90. (The Families and Genera of Vascular Plants). Available from: https://doi.org/10.1007/978-3-662-03531-3_15
Van Wichelen J, Camelbeke K, Chaerle P, Goetghebeur P, Huysmans S. Comparison of different treatments for LM and SEM studies and systematic value of pollen grains in Cyperaceae. Grana. 1999; 38(1):50–8.
Alvarado-Cárdenas LO. Sistemática del género Bdallophytum (Cytinaceae). Acta Bot Mex. 2009; (87):1–21.
Fernández-Alonso JL, Cuadros-Villalobos H. Sanguisuga, a neotropical new genus of Cytinaceae and a South American connection in the family. Caldasia. 2012; 34(2):291–308.
Engel MS, Dingemans-Bakels F. Nectar and Pollen Resources for Stingless Bees (meliponinae, Hymenoptera) in Surinam (south America). Apidologie. 1980; 11(4):341–50
Mihoc M a. K, Morrone JJ, Negritto MA, Cavieres LA. Evolución de la serie Microphyllae (Adesmia, Fabaceae) en la Cordillera de los Andes: una perspectiva biogeográfica. Rev Chil Hist Nat. 2006; 79 (3):389–404.
Duno de Stefano R, Cetzal—Ix W. Fabaceae (Leguminosae) en la Península de Yucatán, México. 2016; 8:111–6.
Kubitzki K, Rohwer JG, Bittrich V, editors. Aizoaceae. In: Flowering Dicotyledons: Magnoliid, Hamamelid and Caryophyllid Families [Internet]. 1st ed. Berlin Heidelberg: Springer-Verlag; 1993 [cited 2021 Aug 18]. P. 37–69. (The Families and Genera of Vascular Plants; vol. 2). Available from: https://www.springer.com/gp/book/9783540555094
Christenhusz MJM. An Overview of Lardizabalaceae. Curtiss Bot Mag. 2012; 29(3):235–76.
Kuijt J, Hansen B. Loranthaceae. In: Flowering Plants Eudicots [Internet]. Cham: Springer International Publishing; 2015 [cited 2022 Jan 11]. p. 73–119. Available from: http://link.springer.com/10.1007/978-3-319-09296-6_14
Graham S. A revision of Ammannia (Lythraceae) in the Western Hemisphere. J Arnold Arbor [Internet]. 1985 [cited 2022 Jan 11]; Available from: https://scholar.google.com/scholar_lookup?title=A+revision+of+Ammannia+%28Lythraceae%29+in+the+Western+Hemisphere.&author=Graham+S.A. &publication_year=1985
Renner SS. Phylogeny and classification of the Melastomataceae and Memecylaceae. Nord J Bot. 1993; 13(5):519–40.
Melastomataceae Almeda F. In: Davidse G, Sousa M, Knapp S, Chiang F, editors. Flora Mesoamericana, Volume 4 (Part 1): Cucurbitaceae a Polemoniaceae [Internet]. Missouri Botanical Garden Press; 2009 [cited 2022 Jan 11]. p. 855. Available from: https://www.nhbs.com/flora-mesoamericanavolume-4-part-1-cucurbitaceae-a-polemoniaceae-spanish-book
Endress ME, Bittrich V. Molluginaceae. In: Kubitzki K, Rohwer JG, Bittrich V, editors. Flowering Plants ∙ Dicotyledons: Magnoliid, Hamamelid and Caryophyllid Families [Internet]. Berlin, Heidelberg: Springer; 1993 [cited 2021 Jul 28]. p. 419–26. (The Families and Genera of Vascular Plants; vol. 2). Available from: https://doi.org/10.1007/978-3-662-02899-5_49
Green PS. Oleaceae. In: Kadereit JW, editor. Flowering Plants ∙ Dicotyledons: Lamiales (except Acanthaceae including Avicenniaceae) [Internet]. Berlin, Heidelberg: Springer; 2004 [cited 2022 Jan 11]. p. 296–306. (The Families and Genera of Vascular Plants). Available from: https://doi.org/10.1007/978-3-642-18617-2_16
Kalis AJ. Papaveraceae. Rev Palaeobot Palynol. 1979; 28(3–4):A209–60.
Kadereit JW. A revision of Papaver sect. Carinatae (Papaveraceae). Nord J Bot. 1987; 7(5):501–4.
Yuncker TG. The Piperaceae—A family profile. Brittonia. 1958; 10(1):1–7.
Tebbs MC. Piperaceae. In: Kubitzki K, Rohwer JG, Bittrich V, editors. Flowering Plants ∙ Dicotyledons: Magnoliid, Hamamelid and Caryophyllid Families [Internet]. Berlin, Heidelberg: Springer; 1993 [cited 2022 Jan 11]. p. 516–20. (The Families and Genera of Vascular Plants). Available from: https://doi.org/10.1007/978-3-662-02899-5_60
Albach DC, Utteridge T, Wagstaff SJ. Origin of Veroniceae (Plantaginaceae, Formerly Scrophulariaceae) on New Guinea. Syst Bot. 2005; 30(2):412–23.
Xu Z, Chang L. Plantaginaceae. In: Xu Z, Chang L, editors. Identification and Control of Common Weeds: Volume 3 [Internet]. Singapore: Springer; 2017 [cited 2022 Jan 11]. p. 339–74. Available from: https://doi.org/10.1007/978-981-10-5403-7_15
Prieto-Baena JC, Hidalgo PJ, Domínguez E, Galán C. Pollen production in the Poaceae family. Grana. 2003; 42(3):153–9.
Judd W, Campbell C, Kellogg E, Stevens P, Donoghue M. Poaceae. In: Plant Systematics: A Phylogenetic Approach. Fourth Edition. Oxford, New York: Oxford University Press; 2015.
Eriksen B, Persson C. Polygalaceae. In: Kubitzki K, editor. The Families and Genera of Vascular Plants. Berlin: Springer-Verlag; 2007. p. 345–63.
Banks H, Klitgaard B, Claxton F, Forest F, Crane P. Pollen morphology of the family Polygalaceae (Fabales). Bot J Linn Soc. 2008; 156(2):253–89.
Hebda RJ, Chinnappa CC, Smith BM. Pollen morphology of the Rosaceae of western Canada. Can J Bot. 1988; 66(4):595–612.
Rosaceae Kalkman C. In: Kubitzki K, editor. Flowering Plants ∙ Dicotyledons [Internet]. Berlin, Heidelberg: Springer Berlin Heidelberg; 2004 [cited 2022 Jan 11]. p. 343–86. Available from: http://link.springer.com/10.1007/978-3-662-07257-8_39
Licht LA. Salicaceae family trees in sustainable agroecosystems. For Chron. 1992; 68(2):214–7.
Kopp RF, Maynard CA, Rocha de Niella P, Smart LB, Abrahamson LP. Collection and storage of pollen from Salix (Salicaceae). Am J Bot. 2002; 89(2):248–52. https://doi.org/10.3732/ajb.89.2.248 PMID: 21669733
Vitaceae Wen J. In: Kubitzki K, editor. Flowering Plants ∙ Eudicots: Berberidopsidales, Buxales, Crossosomatales, Fabales p.p, Geraniales, Gunnerales, Myrtales p.p, Proteales, Saxifragales, Vitales, Zygophyllales, Clusiaceae Alliance, Passifloraceae Alliance, Dilleniaceae, Huaceae, Picramniaceae, Sabiaceae [Internet]. Berlin, Heidelberg: Springer; 2007 [cited 2022 Jan 11]. P. 467–79. (The Families and Genera of Vascular Plants). Available from: https://doi.org/10.1007/978-3-540-32219-1_54
Britannica TE of E. Vitaceae [Internet]. Encyclopedia Britannica. 2010 [cited 2022 Jan 11]. Available from: https://www.britannica.com/plant/Vitaceae
Galimberti A, Mattia FD, Bruni I, Scaccabarozzi D, Sandionigi A, Barbuto M, et al. A DNA Barcoding Approach to Characterize Pollen Collected by Honeybees. PLOS ONE. 2014; 9(10):e109363. https://doi.org/10.1371/journal.pone.0109363 PMID: 25296114
Ferguson DK, Zetter R, Paudayal KN. The need for the SEM in palaeopalynology. Comptes Rendus Palevol. 2007; 6(6):423–30.
Mander L, Li M, Mio W, Fowlkes CC, Punyasena SW. Classification of grass pollen through the quantitative analysis of surface ornamentation and texture. Proc R Soc B Biol Sci. 2013; 280 (1770):20131905 https://doi.org/10.1098/rspb.2013.1905 PMID: 24048158
Louveaux J, Maurizio A, Vorwohl G. Methods of Melissopalynology. Bee World. 1978; 59(4):139–57
Erdtman G. Pollen Morphology and Plant Taxonomy: Angiosperms. Brill Archive; 1986. 576 p.
Caser M. Pollen Grains and Tubes. In: Reference Module in Life Sciences [Internet]. Elsevier; 2017 [cited 2021 Jul 26]. Available from: https://www.sciencedirect.com/science/article/pii/ B9780128096338050779
Costa CM, Yang S. Counting pollen grains using readily available, free image processing and analysis software. Ann Bot. 2009; 104(5):1005–10. https://doi.org/10.1093/aob/mcp186 PMID: 19640891
Mercado Gomez J, Solano L, Sánchez L. Morfología Polínica para Especies de 5 Géneros de Melastomataceae Registradas para Norte de Santandes (Colombia). Bistua Rev Fac Cienc Básicas. 2007; 5(1):71–86.
Punt W, Bos JAA, Hoen PP. Oleaceae. Rev Palaeobot Palynol. 1991; 69(1):23–47.
Godwin H. An Introduction to Pollen Analysis. Nature. 1944; 154(3898):67–67
Shivanna KR, Rangaswamy NS. Pollen Biology [Internet]. Berlin, Heidelberg: Springer Berlin Heidelberg; 1992 [cited 2021 Jul 26]. Available from: http://link.springer.com/10.1007/978-3-642-77306-8
Durre I, Morrill C, Bauer B, Gille E, Gross W. Pollen | National Centers for Environmental Information (NCEI) formerly known as National Climatic Data Center (NCDC) [Internet]. NOAA Paleoclimatology Program. 1993 [cited 2021 Jul 26]. Available from: https://www.ncdc.noaa.gov/data-access/paleoclimatologydata/datasets/pollen
Kirk W, Aupinel P, Ancelin J. Apibotanica. Inventaire Palynologique et Botanique Apicole. [Internet]. 1989 [cited 2021 Jul 28]. Available from: http://apibotanica.inra.fr/
Martin AC, Harvey WJ. The Global Pollen Project: a new tool for pollen identification and the dissemination of physical reference collections. Goslee S, editor. Methods Ecol Evol. 2017; 8(7):892–7.
Bremond Laurent, Muller Serge, Rouland Sylvie, et al. ISEM reference palynological database. 2018 [cited 2021 Jul 28]; Available from: https://doi.oreme.org/bca4022a-4db1-48ec-a212-8bd28c4cb2df
Bourgeois Y, Pham P, Jalali A, Norris D, Sai Santhosh V, Patchalla P, et al. Pollen RCN. Integrative Pollen Biology Research Coordination Network. [Internet]. PalDat—Palynological Database. 2010. Available from: http://pollennetwork.org/news/paldat-palynological-database
Rohlf FJ. tpsDig, Digitize Landmarks and Outlines. Stony Brook, NY: Department of Ecology and Evolution, State University of New York.; 2006.
Klingenberg CP. MorphoJ: an integrated software package for geometric morphometrics. Mol Ecol Resour. 2011; 11(2):353–7. https://doi.org/10.1111/j.1755-0998.2010.02924.x PMID: 21429143
Bookstein FL. Combining the Tools of Geometric Morphometrics. In: Marcus LF, Corti M, Loy A, Naylor GJP, Slice DE, editors. Advances in Morphometrics [Internet]. Boston, MA: Springer US; 1996 [cited 2021 Jul 28]. p. 131–51. (NATO ASI Series). Available from: https://doi.org/10.1007/978-1-4757-9083-2_12
Douglas L, Marchal W, Wathen S. Distribuciones de Probabilidad Discreta. In: Estadistica aplicada a los negocios y la economia [Internet]. México: McGraw—Hill/Interamericana Editores, S.A. de C.V.; 2012 [cited 2021 Sep 29]. p. 207–11. Available from: https://www.academia.edu/16035082/ Estadistica_aplicada_a_los_negocios_y_la_economia_15_edicion
Pla L. Biodiversidad: Inferencia basada en el Índice de Shannon y la riqueza. 2006; 31:9.
Escalante T, Morrone JJ. Métodos para medir la biodiversidad. Acta Zool Mex. 2002;(85):195–6.
Reyes PR, Torres-Florez JP. Diversidad, distribución, riqueza y abundancia de condrictios de aguas profundas a través del archipiélago patagónico austral, Cabo de Hornos, Islas Diego Ramírez y el sector norte del paso Drake. Rev Biol Mar Oceanogr. 2009; 44(1):243–51.
Prado A, García C, Araujo P, Hernández A, Ron Román J, Saegerman C, et al. Diversidad de abejas sin aguijón (Hymenoptera: Meliponini) en las provincias de Orellana, Sucumbíos y Loja–Ecuador. In: Taxonomía y Diversidad. México: UDLAP; 2020. p. 117.
Palacios E. Determinación de la diversidad genética mediante caracterización molecular y análisis filogenético de abejas nativas sin aguijón (Hymnóptera: Meliponini) de las provincias de Orellana y Loja, Ecuador. [Tesis de pregrado]. [ Ecuador]: Universidad de las Fuerzas Armadas ESPE; 2020.
Antoniazzi R, Dáttilo W, Rico-Gray V. A Useful Guide of Main Indices and Software Used for Ecological Networks Studies. In: Dáttilo W, Rico-Gray V, editors. Ecological Networks in the Tropics: An Integrative Overview of Species Interactions from Some of the Most Species-Rich Habitats on Earth [Internet]. Cham: Springer International Publishing; 2018 [cited 2021 Oct 25]. P. 185–96. Available from: https://doi.org/10.1007/978-3-319-68228-0_13
ASPA. Bidens pilosa Asteraceae. Australasian Pollen and Spore Atlas. 2019.
Kaltenrieder P, Von Ballmoos P. Introduction to pollen analysis. Which of the following descriptions fits best? 2003.
Akram M, Zafar M, Ahmad M, Amina S. Morpho-palynologycal study of Cyperaceae from wetlans of Azad Jammu and Kashmir using Sem and LM. Microsc Res Tec. 2018; 81(3):1–11.
León-Yánez S, Valencia R, Pitman N, Endara C, Ulloa C, Navarrete H. Libro rojo de Plantas Endémicas del Ecuador. Publicaciones del Herbario QCA. 2019
Taisma M, Lasser T. Caracterización de políades en especies venezolanas del género Inga Mill (Fabaceae—Mimosoideae). Acta Botánica Venezuelica. 2013; 36(1):1–14.
da Luz CFP, Maki ES, Horák-Terra I, Vidal-Torrado P, Mendonça Filho CV. Pollen grain morphology of Fabaceae in the Special Protection Area (SPA) Pau- de-Fruta, Diamantina, Minas Gerais, Brazil. An Acad Bras Cienc. 2013; 85(4):1329–44. https://doi.org/10.1590/0001-3765201380511 PMID: 24346795
Kriebel R, Khabbazian M, Sytsma K. A continuous morphological approach to study the evolution of pollen in a phylogenetic context: An example with the order Myrtales. PlosOne. 2017; 12(12):1–27
Ferrero V, De Vega C, Stanfford G, Johnson S. Heterostyly and pollinators in Plumbago auriculata (Plumbaginaceae). South Afr J Bot. 2009; 75(4):778–84.
Hebda R, Chinnappa C. Studies on pollen morphology of Rosaceae. Acta Bot Gallica. 1995; 141 (2):183–93.
Nuñez P. Flora palinológica de Guerrero. UNAM; 1998. 22 p.
Hans B. Chimborazoa (Sapindaceae), a new genus from Ecuador. Brittonia. 1992; 44(3):306–11
Cartaxo-Pinto S, Barbieri C, Mendonça F, Conrado R, Gonçalves-Esteves V. Pollen morphology of species of Cissus (Vitaceae): an evaluation of ornamentation. Palynology. 2016; 6122:27.
Heslop-Harrison J, editor. The Pollen Wall: Structure and Development. In: Pollen: development and physiology. London: Butterworths; 1971.
Espinoza N. Caracterización de la Flora Apícola visitada por cinco especies de abejas sin aguijón en el Meliponario Sinai, Aldea San Antonio de las Flores Pajapita, San Marcos. [Internet] [Tesis de pregrado]. [ Guatemala]: Universidad de San Carlos de Guatemala; 2004. Available from: http://biblioteca.usac.edu.gt/tesis/01/01_2060.pdf
Sáenz C. Polen y esporas: (introducción a la Palinología y Vocabulario palinológico) [Internet]. H. Blume Ediciones, D.L. España; 1978 [cited 2021 Jul 28]. Available from: https://dialnet.unirioja.es/servlet/libro?codigo=19466
Marticorena C. Material Para Una Monografia De La Morfologia Del Polen De Cucurbitaceae. Grana Palynol. 1963; 4(1):78–91
Wilms W, Wiechers B. Floral resource partitioning between native Melipona bees and the introduced Africanized honey bee in the Brazilian Atlantic rain forest. Apidologie. 1997; 28(6):339–55
Rao GM, Suryanarayana MC. Studies on the foraging behaviour of honey bees and its effect on the seed yield in niger. Indian Bee J. 1990; 52(1–4):31–3
León Yánez SDC. Libro rojo de las plantas endémicas del Ecuador [Internet]. 2011 https://isbn.cloud/9789942033932/libro-rojo-de-las-plantas-endemicas-del-Ecuador/
Patiny S. Pollen resources of non-Apis bees in southern Africa. In: Evolution of Plant-Pollinator Relationships. Cambridge University Press; 2011.
Judd WS, Skean JD. Taxonomic studies in the Miconieae (Melastomataceae): IV. generic realinments among terminal-flowered taxa. Biol Sci [Internet]. 1991 [cited 2021 Jul 28]; Available from: https://agris.fao.org/agris-search/search.do?recordID=US9513402
Goldenberg R. O gênero Miconia (Melastomataceae) no Estado do Paraná, Brasil. Acta Bot Bras. 2004 Dec; 18:927–47.
Fierro AF, Fernández D, Quintana C. Usos de Melastomataceae en el Ecuador. SIDA Contrib Bot. 2002; 20(1):233–60.
Higuita H, Rivas AC. Estudio de la familia Melastomataceae en el área de jurisdicción de Corantioquia: informe final. Corantioquia; 2007
Fernández V. La Restauración Ecológica es clave para la recuperación de ecosistemas degradados. [Internet]. Territorio Geoinnova—SIG y Medio Ambiente. 2017 [cited 2021 Jul 28]. Available from: https://geoinnova.org/blog-territorio/restauracion-ecologica/
Villa J, Bustamante D. Amenazas a la integridad ecológica del bosque de miconia del sector media luna en la Isla Santa-Galápagos [Internet] [Tesis de pregrado]. [ Ecuador]: Universidad Central del Ecuador; 2018 [cited 2021 Jul 28]. Available from: http://www.dspace.uce.edu.ec/handle/25000/ 15101
Silva GR da, Pereira F de M, Souza B de A, Lopes MT do R, Campelo JEG, Diniz FM. Aspectos bioecológicos e genético-comportamentais envueltos na [cited 2021 Jul 28]. 957 p. Available from conservação da abelha Jandaíra, Melipona subnitida Ducke (Apidae, Meliponini), e o uso de ferramentas moleculares nos estudos de diversidade. Arq Inst Biológico 2014 Sep;81:299–308.
Minga D, Verdugo A. Árboles y arbustos de los ríos de Cuenca [Internet] [Tesis de pregrado]. [ Ecuador]: Universidad del Azuay; 2016 [cited 2021 Jul 28]. Available from: http://dspace.uazuay.edu.ec/handle/datos/8784
Berlanga Sanz L. Caracterización fenólica de las especies Bidens aurea (Aiton) Sherff Compositae y Daphne gnidium L. (Thymelaeaceae) [Internet] [Tesis de maestría]. [ Portugal]: Instituto Politécnico de Bragança; 2018 [cited 2021 Jul 28]. Available from: https://bibliotecadigital.ipb.pt/handle/10198/ 18300
Sanford M. Beekeeping: Florida Bee Botany [Internet]. University of Florida; 2003. Available from: https://entnemdept.ufl.edu/media/entnemdeptifasufledu/honeybee/pdfs/Beekeeping—Florida-BeeBotany.pdf
Mambrín M, Avanza M, Ferrucci M. Análisis morfológico y morfométrico del polen de Corchorus, Heliocarpus, Luehea, Mollia y Triumfetta (Malvaceae, Grewioideae) en la región Austral de América del sur. Darwiniana. 2010; 48(1):45–58.
Hernández FJ, Navarro Mata CB, Peña Montañez R, Nájera Luna A. Patrón de distribución espacial de las especies arbóreas de la región de El Salto, Durango. Rev Mex Cienc For. 2018; 9(47):169–86
Montañez Valencia RA, Escudero Vásquez CY, Duque Montoya ÁJ. Patrones de Distribución Espacial de Especies Arbóreas en Bosques de Alta Montaña del Departamento de Antioquia, Colombia. Rev Fac Nac Agron–Medellín. 2010; 63(2):5629–38.
López JF. Manual de ecología [Internet]. Editorial Trillas. Universidad de Cornell; 1985. 266 p. Available from: https://books.google.com.ec/books/about/Manual_de_ecolog%C3%ADa.html?id=jRFAAAAYAAJ&redir_esc=y
Inoue T, Sakagami SF, Salmah S, Nukmal N. Discovery of Successful Absconding in the Stingless Bee Trigona (Tetragonula) Laeviceps. J Apic Res. 1984; 23(3):136–42
Koptur S. Flowering Phenology and Floral Biology of Inga (Fabaceae: Mimosoideae). Syst Bot. 1983; 8(4):354–68.
Torres C, Galetto L. Flowering phenology of co-occurring Asteraceae: a matter of climate, ecological interactions, plant attributes or of evolutionary relationships among species? Org Divers Evol. 2011; 11(1):9–19.
Zimmerman JK, Wright SJ, Calderón O, Pagan MA, Paton S. Flowering and fruiting phenologies of seasonal and aseasonal neotropical forests: the role of annual changes in irradiance. J Trop Ecol. 2007; 23(2):231–51.
Brito VLG, Maia FR, Silveira F a. O, Fracasso CM, Lemos-Filho JP, Fernandes GW, et al. Reproductive phenology of Melastomataceae species with contrasting reproductive systems: contemporary and historical drivers. Plant Biol Stuttg Ger 2017; 19(5):806–17. https://doi.org/10.1111/plb.12591 PMID: 28627760
Ramalho M, Imperatriz-Fonseca VL, Kleinekt-Giovannini A, Cortopassi-Laurino M. Exploitation of floral resources by Plebeia remota Holmberg (Apidae, Meliponinae). Apidologie. 1985; 16(3):307–30
Kleinert-Giovannini A, Imperatriz-Fonseca VL. Aspects of the Trophic niche of Melipona Marginata Marginata Lepeletier (Apidae, Meliponinae). Apidologie. 1987; 18(1):69–100
Moreno J. Social bees and palm trees: What do pollen diets tell us? In: Social insects and the environment [Internet]. New Delhi: Oxford & IBH Pub. Co.; 1990 [cited 2021 Jul 28]. Available from: http://books.google.com/books?id=hzEgAQAAMAAJ
Inoue T, Salmah S, Abbas I, Yusuf E. Foraging behavior of individual workers and foraging dynamics of colonies of three Sumatran stingless bees. Res Popul Ecol. 1985; 27(2):373–92.
Skorbiłowicz M, Skorbiłowicz E, Cieśluk I. Bees as Bioindicators of Environmental Pollution with Metals in an Urban Area. J Ecol Eng. 2018; 19(3):229–34.
Girotti S, Ghini S, Ferri E, Bolelli L, Colombo R, Serra G, et al. Bioindicators and biomonitoring: honeybees and hive products as pollution impact assessment tools for the Mediterranean area. Euro-Mediterr J Environ Integr. 2020 Oct.; 5(3):62.