https://doi.org/10.32854/agrop.v14i4.1932

The melliferous flora of Veracruz, Mexico

Real-Luna, Natalia1,2; Rivera-Hernández, Jaime E.3; Alcántara-Salinas, Graciela1; Zalazar-Marcial, Edgardo1; Pérez-Sato, Juan A.1*

1Colegio de Postgraduados Campus Córdoba. Carretera Federal Córdoba-Veracruz km 348, Manuel León, Amatlán de los Reyes, Veracruz, México. C. P. 94953. 2Doctorado en Ciencias Naturales para el Desarrollo (DOCINADE) Instituto Tecnológico de Costa Rica, Universidad Nacional, Universidad Estatal a Distancia, Costa Rica. 3Centro de Estudios Geográficos, Biológicos y Comunitarios, S.C. Córdoba, Veracruz, México. C. P. 94500. *Corresponding author: [email protected]

ABSTRACT Objective: To contribute to the knowledge of the situation of the melliferous flora in Veracruz for pollinators and to communicate it for the benefit of beekeepers and stingless beekeepers, as well as to develop comprehensive strategies with these activities. Design/Methodology/Approach: The information was obtained through a bibliographic review in reference databases such as Scopus, Web of Science Group, Academic Google, Elsevier and Springer Link, using the following keywords: flora, bees, pollinators, honey, pollen. Results: 63 families were recorded, with 176 genera and 216 of melliferous flora, finding that the largest number of species are found in the Fabaceae family (20%) and Asteraceae (16.55%). There were also 44 crops with 22 families. Study Limitations/Implications: There were no limitations in conducting this study. Findings/Conclusions: The greatest diversity of melliferous flora species is related to wild , and strategies need to be implemented for their protection and multiplication. For these actions, various actors must be involved at different levels of government, educational and private institutions, civil society, farmers, beekeepers, and stingless beekeeping. Conservation actions include the use of melliferous plants in gardens and their protection in crops, sites surrounding crops and on edges. It is necessary to preserve natural landscapes and restore damaged ones, as well as to lead favorable practices in pollinator-dependent crops.

Keywords: flora, bees, pollinators, honey, pollen.

INTRODUCTION maintain a close relationship with melliferous flora, since they depend on them for their food, when Bees consuming nectar and pollen obteined from the flowers. Likewise, they also collect resinous material that they use for the construction of their nest and for the elaboration of propolis, which serve as protection against pathogens and predators (Bonet and Vergara, 2016).

Agroproductividad: Vol. 14, Núm. 4, abril. 2021. pp: 65-80. Recibido: septiembre, 2020. Aceptado: marzo, 2021.

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Melliferous flora or honey flora is made up of plants that of Veracruz, Mexico, was obtained through the produce resins or whose flowers produce nectar and/ bibliographic review of the reference databases Scopus, or pollen; it is classified into polliniferous, nectariferous Web of Science Group, Academic Google, Elsevier or pollen-nectariferous (Montoya-Bonilla et al., 2017). In and Springer Link, using the following keywords: flora, exchange for food or resins that the bees receive from bees, pollinators, honey, pollen. The information was wild and cultivated plants, they pollinize their flowers systematized assigning categories of use, phenology, thus favoring the formation of fruits that serve as food and biology, in the following way: family, for human beings and other animals, contributing with scientific name, resource that bees are supplied with this to food security and ecological equilibrium of —nectar or pollen—, flowering period, status —whether ecosystems (Alquisira-Ramírez, 2019). native, exotic or naturalized—, and life form; in the case of crops pollinated by bees, the common name was The availability of flower resources for the development added. and reproduction of bee colonies is required during the whole year. This is achieved through short flowering RESULTS AND DISCUSSION periods that most agricultural crops have, as well as Flora in Mexico native plants of the Asteraceae and Fabaceae families, In Mexico there is a record of 23,314 species of vascular which are important to feed the populations of bees plants, among which 2,854 genera, 297 families and and other pollinators because they are the most visited 73 orders were included; in this flora there are 149 (González-Suárez et al., 2020). gymnosperms and 22,126 angiosperms (Ulloa et al., 2017; Villaseñor, 2016). The state of Veracruz occupies The conservation and multiplication of melliferous flora the third place in floristic richness of the country is of huge interest for beekeepers and meliponiculture (Martínez-Adriano et al., 2016), divided into 271 families, producers, because they ensure the production and 1,956 genera and 8,497 species (Villaseñor, 2016). quality of honey from their bee colonies (Araujo- Mondragón and Redonda-Martínez, 2019). In order to Despite the great floristic richness of Veracruz, it is achieve this, the following strategies have been applied: primarily threatened by deforestation, as shown in a use of melliferous plants in agroecologic gardens, or else study carried out by Von et al. (2021), in three regions of interspersed in the crops or on the edges of the paths the state of Veracruz from 2003 to 2013, in the region of (Kremen and M’Gonigle, 2015; Landaverde-González et the Tuxtlas, with a loss of natural coverage of 4.6% al., 2017). (3,516 ha), the old Antigua with 2% (1,634 ha) and Sierra de Otontepec with 1.4% (618 ha). This deforestation also The implementation of conservation strategies for both causes fragmentation of habitats, loss of soil fertility, loss melliferous flora and pollinators is vital, since the absence of biodiversity, and reduction of environmental services or decline of the populations of any of them can impact (Ramírez-Bravo and Hernández-Santin, 2016). their survival, in addition to reducing the production of fruits and seeds, which will have an environmental, social Additionally, erosion and genetic loss were caused by the and economic impact globally (Hipólito et al., 2016; loss of biodiversity, since angiosperms present reduced Wilson et al., 2017). germination and progeny of lower quality (Aguilar et al., 2019), because of the loss of biological corridors for their Therefore, the objective of this study was to understand pollinators (Gómez-Pompa et al., 2010), which has the the situation of the melliferous flora of the state of consequence of smaller, scarce and isolated populations Veracruz, Mexico, through a bibliographic review at the local scale, landscape and regional, with which with the aim of broadening knowledge about the their probability of extinction increases (Auffret et al., available flower resources for pollinators, in addition to 2017). contributing with this information to beekeepers and meliponiculture producers to develop integral strategies Bee-Plant Ecological Interactions in these activities. Bees have evolved with plants and present a complex network of inter-specific interactions where sight, smell, MATERIALS AND METHODS moisture detection, contact and weak electrostatic field The information of melliferous flora of the state between a flower and a bee are involved; through these

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interactions flowers use bees as vehicles for the transport which studies the botanical and geographic origin of of pollen for fertilization (Thakur and Nanda, 2020), and honey, through the analysis of pollen in honey (Stephen, the bees benefit from nectar and pollen as sources of 2014). In palynological studies, there are records that food that plants provide, thus establishing an ecological bees, particularly Apis mellifera, visit approximately 2,000 relationship between them known as mutualism. plant species (Cadena et al., 2019). Therefore, bees are attracted by the nectar which is an aqueous substance, rich in sugars, which contributes Melliferous Plant Species in Veracruz, Mexico carbohydrates as main source of energy for the bees. Based on the information gathered through scientific During nectar collection, bees transport pollen from search engines, an inventory of 63 families were obtained, the anthers to the stigma of the plants, thus benefiting with 176 genera and 216 species of melliferous flora in a large number of species of angiosperms (Castellanos- the state of Veracruz, Mexico. The families that present Potenciano et al., 2012). the highest number of genera are Fabaceae with 20%, and Asteraceae with 16.55%, the same as the highest Bees, in addition to nectar, use the pollen that they number of species (Fabaceae 22.58% and Asteraceae find in the anthers (apical part) of the , both in 15.59%) (Table 1, Annex 1), as mentioned by González- angiosperms and in gymnosperms; during their visits, Suárez et al. (2020). foraging bees attract these grains of pollen through the generation of a weak electrostatic field generated Most of the species of melliferous flora reported for between the flower (with negative charge) and the bee’s the state of Veracruz are native (85.65%), exotic species body (positive charge) (Clarke et al., 2017). contribute 10.19% and naturalized 4.17%. Concerning their life form, 37.04% are , 33.80% are herbaceous, The way in which the bees harvest pollen from the 24.07% shrubs, 2.31% arborescent, 2.31% vines, and flowers is by scraping or licking the anther and then 0.46% liana. Most of the species of melliferous flora sticking it on the carbuncle (cavity that is found in the are nectar-producing (37.96%), followed by pollen- tibia of the third pair of legs), using nectar to stick the producing (32.87%) and, in lower numbers, there are pollen and thus transport it, accumulating it in form of pollen-nectariferous (29.17%) (Figure 1). granules; then, they take it to their nest and, generally, they deposit it around the breeding area where the larvae The Asteraceae family is one of the most diverse are developing, since it is the protein source for larvae plant families in Mexico, with around 392 genera and and adults, containing between 10 and 40% of protein approximately 3,005 species; several of its species are (Leonhardt et al., 2007; Vossler, 2015). of interest to beekeepers (Cadena et al., 2019), so they are considered as a nectar-polliniferous family. The Pollen is an indicator that allows understanding the botanical and geographic characteristics of beekeeping Table 1. The most representative melliferous flora families of products such as honey (Stephen, 2014; Thakur and Veracruz, Mexico. Nanda, 2020). In addition, bees collect resins from some Family % Species % plants for the production of propolis, which they use as Asteraceae 24 16.55 29 15.59 building material and defensive substance (Bankova et Combretaceae 4 2.76 4 2.15 al., 2018). Commelinaceae 4 2.76 4 2.15 Convolvulaceae 3 2.07 6 3.23 The interactions that happen between plant and Euphorbiaceae 6 4.14 7 3.76 pollinator play an important role in the structure of Fabaceae 29 20 42 22.58 communities, in addition to determining the diversity, Lamiaceae 6 4.14 9 4.84 wealth and persistence of species in a specific locality 8 5.52 10 5.38 (Martínez-Adriano et al., 2018). Entomopalynology Myrtaceae 4 2.76 5 2.69 studies pollen found in the body or in the intestine of 4 2.76 5 2.69 insects and provides information about the migration routes and their feeding, in addition to defining the Rubiaceae 4 2.76 4 2.15 pollination mechanisms and the foraging resources. 7 4.83 8 4.30 Another important research area is Melissopalynology, 4 2.76 4 2.15

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Figure 1. Main characteristics of melliferous flora: A) Status, B) Life form and C) Resource offered to pollinators.

Fabaceae family is also one of the most important in Mexico, since it presents social pollinators require accessible 139 genera and 1,850 species (Ramírez-Arriaga et al., 2016). floral resources throughout the year for survival of the colony. For that, On the other hand, there is a record of 44 plant species that are cultivated wild melliferous flora can provide and visited by bees to obtain their food; these crops belong to 23 botanical food and nesting sites, so changes families, of which 43.18% are nectariferous and the same percentage are also must be made in agricultural pollen-nectariferous, and only 9.09% are polliniferous (Annex 2, Figure 2). practices to foster biodiversity and restore, at least to a certain degree, The crops that depend on pollination are soybean, coffee, tomato and orange; the complexity of the ecosystem, the importance of pollinators in agricultural crops is that they improve the as well as its functionality and yield and quality of the seeds and fruits, so this service presents a social and sustainability (Kevan and Silva, 2020). economic impact (Giannini et al., 2020); however, some of the crops only provide food to pollinators during a few weeks, that is, during a short period, On the other hand, regional and and then they must survive a long scarcity, and although some may migrate, local crops could depend on more

A B C

D E F

Figure 2. Crops pollinated by bees: A) Persea americana Mill., B) Citrus limon (L.) Osbeck, C) Macadamia integrifolia Maiden & Betche D) Byrsonima crassifolia (L.) Kunth, E) Capsicum annuum L. y F) Zea mays L. Photographs: Diana Caballero Alvarado.

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specialized pollinators, although more research in this investigacion.uaem.mx/archivos/epub/practicas-agropecuarias- regard is required, particularly in small-scale agriculture, seguridad/practicas-agropecuarias-seguridad.pdf since this benefits the local and regional economy, in Araujo-Mondragón, F., y Redonda-Martínez, R. (2019). Flora melífera de la región centro-este del municipio de Pátzcuaro, Michoacán, addition to this knowledge being important in local México. Acta Botanica Mexicana, 126(e1444), 1–20. https://doi. communities (Giannini et al., 2020). org/10.21829/abm126.2019.1444 Auffret, A. G., Rico, Y., Bullock, J. M., Hooftman, D. A. P., Pakeman, R. Beekeeping and meliponiculture are important activities J., Soons, M. B., Suárez-Esteban, A., Traveset, A., Wagner, H. thanks to the pollination service that they provide, in H., y Cousins, S. A. O. (2017). Plant functional connectivity – addition to the products that bees provide to human integrating landscape structure and effective dispersal. Journal of Ecology, 105(6), 1648–1656. https://doi.org/10.1111/1365- beings, such as honey, pollen, wax and propolis, which 2745.12742 arise directly or indirectly from the melliferous flora from Badillo-Montaño, R., Aguirre, A., y Munguía-Rosas, M. A. (2019). which working bees feed (Kevan and Silva, 2020). Pollinator-mediated interactions between cultivated papaya and co- species. Ecology and Evolution, 9(1), CONCLUSIONS 587–597. https://doi.org/10.1002/ece3.4781 In Veracruz there is a great richness of melliferous flora Bankova, V., Popova, M., y Trusheva, B. (2018). The phytochemistry of the honeybee. Phytochemistry, 155, 1–11. https://doi. represented by 215 wild plant species, the vast majority org/10.1016/j.phytochem.2018.07.007 of species belong to Fabaceae (20%) and Asteraceae Bonet, F. M., y Vergara, C. H. (2016). 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AGRO 70 PRODUCTIVIDAD Real-Luna et al. (2021) Reference Villegas et al. (2000) (2018); Parra-Tabla et al. et al. (2018); Parra-Tabla Contreras-Oliva (2019); Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) y Espejo (2016); López-Ferrari Bonet y Vergara (1995) Villegas et al. (2000) (2018); Niembro-Rocas et et al. (2018); Niembro-Rocas Contreras-Oliva al. (2010); Villegas et (2000) et al. (2018) Ramírez-Arriaga Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Contreras-Oliva et al. (2018) Contreras-Oliva (2016) Bonet y Vergara Castellanos-Potenciano et al. (2012); Contreras- Castellanos-Potenciano et al. (2010) Oliva et al. (2018); Niembro-Rocas Villegas et al. (2000) et et al. (2015); Ramírez-Arriaga Niembro-Rocas al. (2018) Villegas et al. (2000) Castellanos-Potenciano et al. (2012);Niembro- Castellanos-Potenciano et al. (2010); Villegas (2000) Rocas Tree Tree Tree Tree Tree Tree Herb Shrub Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Arborescent Herbaceous Herbaceous Arborescent Arborescent Arborescent Arborescent Herbaceous Herbaceous Herbaceous Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native All year All year January May-July April-July April-May Flowering December September- September- May-August March-June January-May January-April January-April February-April February-April January-March January-March January-March January-March January-March May-November July-September December-April April-December March-September March-September December-August X X X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X X X X Pollen Plant species (L.) G. Don (L.) G. Bidens reptans (Kunth) H. H. (Kunth) salicifolius Barkleyanthus & Brettell Rob Bidens pilosa L. Baccharis conferta Kunth conferta Baccharis trinervis (Cham.) Pers. Baccharis L. recta Baltimora Ambrosia peruviana Willd. Ambrosia Ageratum houstonianum Mill. Ageratum Achillea millefolium L. Achillea millefolium Yucca gigantea Lem. gigantea Yucca (Kunth) Hemsl. Nolina parviflora (Kunth) Echeandia albiflora (Schltdl. & Cham.) Echeandia Martens & Galeotti M. Sabal mexicana Mart. Oreopanax sp. Oreopanax Wess. (Mutis ex L. f.) butyracea Attalea Boer Dendropanax arboreus (L.) Decne. & arboreus Dendropanax Planch. (Jacq.) Lodd. ex (Jacq.) Lodd. aculeata Acrocomia Mart. Plumeria rubra L. L. citrifolia Tabernaemontana Iresine diffusa Humb. & Bonpl. ex Iresine Willd. Asclepias curassavica L. Spondias mombin L. Liquidambar sp. (L.) Mosyakin Dysphania ambrosioides & Clemants altissima (Jacq.) Kunth (Spreng.) Standl. (Spreng.) Bravaisia integerrima Avicennia germinans (L.) L. Avicennia Family Araliaceae Arecaceae Asteraceae Altingiaceae Acanthaceae Apocynaceae Asparagaceae Anacardiaceae Appendix 1 . Melliferous flora in Veracruz state, Mexico

AGRO PRODUCTIVIDAD 71 Agro productividad 14 (4): 65-80. 2021 Reference Villegas et al. (2000) Villegas et al. (2000) (2018); Niembro-Rocas et et al. (2018); Niembro-Rocas Contreras-Oliva al. (2010); Villegas et (2000) Bonet y Vergara(2016) Canto et al. (2017) Villegas et al. (2000) et al. , (2010; Villegas Niembro-Rocas (2000) Villegas et al. (2000) et al. (2010; Villegas Niembro-Rocas (2000) Villegas et al. (2000) Villegas et al. (2000) Gónzalez(2014) Villegas et al. (2000) Villegas et al. (2000) Contreras-Oliva et al. (2018) Contreras-Oliva Villegas et al. (2000) et al. (2018) Contreras-Oliva Hernández-Villa et al. (2020) Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Hernández-Villa et al. (2020) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) et al. (2018) Contreras-Oliva Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Contreras-Oliva et al. (2018) Contreras-Oliva Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Villegas et al. (2000) Tree Tree Tree Tree Tree Tree Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized All year All year Flowering December December December September- September- September- August-April January-April February-May January-June February-April January-March January-March January-March December-May August-October August- January August-February December-March December-March December-March August-December August-December October-December X X X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X X X X X X X X Pollen Plant species S.F. Blake S.F. megalantha Cordia Cordia dentata Poir. dentata Cordia Cochlospermum vitifolium (Willd.) vitifolium Cochlospermum Spreng. Oken alliodora (Ruiz & Pav.) Cordia Berberis trifolia Schult. & f. Berberis trifolia Tecoma stans (L.) Juss. ex Kunth Tecoma Impatiens walleriana Hook. f. Impatiens (Jacq.) S. (Jacq.) S. chrysanthus Handroanthus Grose O. (Bertol.) DC. rosea Tabebuia Viguiera grammatoglossa D.Viguiera grammatoglossa C. (Cav.) Spreng. (Cav.) Viguiera dentata (Kunth) H. Rob. H. (Kunth) patens Vernonanthura Verbesina sp. Verbesina sp. Vernonia Tridax procumbens L. procumbens Tridax Tithonia tubiformis (Jacq.) Cass. Tithonia tubiformis (Cav.) H. Rob. H. (Cav.) maculatus Smallanthus S. F. Blake F. Simsia eurylepis S. (Cav.) Pers. Simsia amplexicaulis (Cav.) Montanoa grandiflora Alamán ex DC. Montanoa Less. Parthenium fruticosum (L.) Cass Pluchea odorata Lam. Sanvitalia procumbens Melampodium divaricatum (Rich.) DC. Melampodium divaricatum Heliopsis buphthalmoides (Jacq.) Heliopsis buphthalmoides Dunal Helianthus sp. Helianthus (L.) R.M. King & (L.) R.M. odorata Chromolaena Rob. H. mollis Kunth Elephantopus Bidens triplinervia Kunth Family Bixaceae Asteraceae Bignoniaceae Boraginaceae Berberidaceae Balsaminaceae

AGRO 72 PRODUCTIVIDAD Real-Luna et al. (2021) Reference Villegas et al. (2000) Canto et al. 2017) Villegas et al. (2000) Canto et al. (2017) Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Bonet y Vergara (2016); López-Ferrari et al. (2016); López-Ferrari Bonet y Vergara (2014) Bonet y Vergara, 2016; Hernández-Villa et al. , Bonet y Vergara, 2020 Bonet y Vergara (2016); López-Ferrari et al. (2016); López-Ferrari Bonet y Vergara (2014) Bonet y Vergara (2016); López-Ferrari et al. (2016); López-Ferrari Bonet y Vergara (2014) Villegas et al. (2000) Niembro-Rocas et al. (2010); Villegas Niembro-Rocas (2000) et al. (2018) Ramírez-Arriaga et al. (2019) Parra-Tabla Villegas et al. (2000) et al. (2010); Villegas Niembro-Rocas (2000) Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Villegas et al. (2000) (2018); Herrera-López et et al. (2018); Herrera-López Contreras-Oliva al. (2019); Villegas et (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Tree Tree Tree Tree Tree Tree Vine Vine Vine Shrub Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Exotic Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized Naturalized Naturalized All year All year All year All year All year February Flowering April-June December- January-April January-April February-May February-May February-April February-April November-May May-December May-December February-March September-May February-August January-February December-March December-March October-February August-November X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X X X X Pollen Plant species Merremia dissecta (Jacq.) Hallier f. Merremia A. DC. Sedum praealtum Ipomoea triloba L. Ipomoea indica (Burm.) Merr. Ipomoea arborescens (Humb. & Ipomoea arborescens Don Bonpl. ex Willd.) G. Ipomoea carnea subsp. fistulosa (Mart. Austin ex Choisy) D.F. Convolvulus nodiflorus Desv. Convolvulus (Vahl) Handlos (Vahl) serrulata Tripogandra Tinantia erecta (Jacq.) Schltdl. erecta Tinantia (M. Martens & Gibasis pellucida (M. Hunt Galeotti) D.R. Burm. f. diffusa Burm. f. Commelina C. Cordem. Hedyosmum mexicanum C. Gaertn. (L.) C.F. Laguncularia racemosa L. catappa Terminalia Combretum farinosum Kunth Combretum Trema micrantha (L.) Blume micrantha Trema L. erectus Conocarpus Lobelia xalapensis Kunth Lobelia Opuntia huajuapensis Bravo Opuntia Haw. stricta (Haw.) Opuntia Bursera simaruba (L.) Sarg. F.M. (Haw.) imbricata Cilindropuntia Knuth Raphanus raphanistrum L. (L.) W.D.J. Koch Brassica nigra (L.) W.D.J. Brassica rapa L. Family Cactaceae Burseraceae Brassicaceae Crassulaceae Cannabaceae Combretaceae Chloranthaceae Convolvulaceae Campanulaceae Commelinaceae

AGRO PRODUCTIVIDAD 73 Agro productividad 14 (4): 65-80. 2021 Reference Contreras-Oliva et al. (2018) Contreras-Oliva Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) et al. (2018) Contreras-Oliva Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Niembro-Rocas et al. (2010); Villegas Niembro-Rocas (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) et al. (2018) Ramírez-Arriaga Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Niembro-Rocas et al. (2010); Villegas Niembro-Rocas (2000) Villegas et al. (2000) et et al. (2010); Ramírez-Arriaga Niembro-Rocas al. (2018) Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Vine Vine Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Exotic Exotic Exotic Exotic Exotic Exotic Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized All year All year All year All year February February April-July Flowering April-June December December November- September- September- September- March-June February-July February-May February-April February-April February-April February-April January-March December-May December-April April-December December-March October-February X X X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X X X X Pollen Plant species (Sw.) DC. (Sw.) Desmodium adscendens (Bojer ex Hook.) Raf. (Bojer ex Hook.) Raf. Delonix regia Dalea botterii (Rydb.) Barneby Dalea botterii Cassia grandis L. f. Chamaecrista sp. (L.) Britton & Rose arborea Cojoba (Jacq.) Schinz brownei Dalbergia Cajanus cajan (L.) Huth Cassia fistula L. Caesalpinia cacalaco Bonpl. Caesalpinia cacalaco Bauhinia divaricata L. Bauhinia divaricata Vachellia farnesiana (L.) Wight & Arn. Vachellia (Schltdl. & Cham.) pennatula Vachellia Seigler & Ebinger Acacia sp. (L.) Seigler & cornigera Vachellia Ebinger Ricinus communis L. Ricinus communis Euphorbia schlechtendalii Boiss. schlechtendalii Euphorbia Euphorbia heterophylla L. heterophylla Euphorbia Croton reflexifolius Kunth reflexifolius Croton (Pax) I.M. (Pax) I.M. multilobus Cnidoscolus Johnst. Schltdl. & Cham. draco Croton M. Martens & Galeotti M. tinifolia Ehretia Sw.Alchornea latifolia Rhynchospora radicans (Schltdl. & Pfeiff. Cham.) H. (Terán & Berland.) I.M. & Berland.) I.M. anacua (Terán Ehretia Johnst. Sicyos microphyllus Kunth Sicyos microphyllus Momordica charantia L. charantia Momordica Luffa aegyptiaca Mill. Family Fabaceae Ehretiaceae Cyperaceae Cucurbitaceae Euphorbiaceae

AGRO 74 PRODUCTIVIDAD Real-Luna et al. (2021) Reference Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) (2010); Contreras-Oliva et et al. (2010); Contreras-Oliva Niembro-Rocas al. (2018); Villegas et (2000) Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) et al. (2010); Canto (2017); Niembro-Rocas Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) et al. (2018) Ramírez-Arriaga Villegas et al. (2000) et al. 2018) Ramírez-Arriaga Niembro-Rocas et al. (2010); Villegas Niembro-Rocas (2000) et al. (2010); Villegas Niembro-Rocas (2000) Gónzalez, (2014) Villegas et al. (2000) Niembro-Rocas et al. 2010: Villegas (2000) Niembro-Rocas Villegas et al. (2000) Niembro-Rocas et al. , (2010); Villegas Niembro-Rocas (2000) Villegas et al. (2000) Contreras-Oliva et al. (2018) Contreras-Oliva Bonet y Vergara (2016) Bonet y Vergara Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Shrub Shrub Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Exotic Exotic Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized All year January January October May-July April-July April-May Flowering November March-July March-May March-May November- December- December- September- September- January-April February-May February-may February-April January-March January-March November-May February-March December-April September-April August-November August-December X X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X X X X X X X X X X X Pollen Plant species (Rose) Seigler & pringlei (Rose) Vachellia Ebinger Kunth turbacensis Verbesina L. Vicia sativa Trifolium repens L. repens Trifolium Pithecellobium insigne Micheli ex Pithecellobium Donn. Sm. DC. juliflora (Sw.) Prosopis Mimosa scabrella Benth. Mimosa scabrella Piscidia piscipula (L.) Sarg. Benth. (Roxb.) dulce Pithecellobium Mimosa pudica L. Mimosa albida Humb. & Bonpl. ex Willd. Mimosa pigra L. S. Watson S. lanceolata Leucaena sp. Leucaena Benth. guatemalensis Lonchocarpus sp. Lonchocarpus Benth. (Kunth) acapulcense Lysiloma Inga vera Willd. (Schltdl.) Benth. diversifolia Leucaena Schltdl. & Cham. ex G. Don Inga inicuil Schltdl. & Cham. ex G. H. Karst. brasiletto H. Haematoxylum campechianum L. Haematoxylum Eysenhardtia polystachya (Ortega) Eysenhardtia Sarg. ex Gliricidia sepium (Jacq.) Kunth Walp. Enterolobium cyclocarpum (Jacq.) Enterolobium Griseb. (Sw.) DC. Desmodium tortuosum (Sw.) Desmodium canescens (L.) DC. Desmodium canescens Family Fabaceae

AGRO PRODUCTIVIDAD 75 Agro productividad 14 (4): 65-80. 2021 Reference Niembro-Rocas et al. (2010); Villegas Niembro-Rocas (2000) Villegas et al. (2000) et al. (2018) Ramírez-Arriaga Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) (2016) Bonet y Vergara Niembro-Rocas et al. (2010); Villegas Niembro-Rocas (2000) (2017); Parra-Tabla et al. (2019) Canto et al. (2017); Parra-Tabla Villegas et al. (2000) Contreras-Oliva et al. (2018); Villegas Contreras-Oliva (2000) et al. (2018) Ramírez-Arriaga Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) et al. (2010); Villegas Niembro-Rocas (2000) Bonet y Vergara (2016) Bonet y Vergara Ramírez-Arriaga et al. (2018) Ramírez-Arriaga Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Ramírez-Arriaga et al. (2018) Ramírez-Arriaga Bonet y Vergara(2016) Villegas et al. (2000) Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Exotic Exotic Exotic Exotic Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized June All year All year All year January January February Flowering November November- September- September- September- February-May January-June February-May June-October November-May November-May December-April February-March August-October December-March October-February August-December X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X Pollen Plant species Trichilia hirta L. Trichilia Miconia sp. Miconia Trichilia havanensis Jacq. Trichilia Sida acuta Burm. f. L. Sida rhombifolia (Kunth) Pseudobombax ellipticum (Kunth) Dugand Pachira aquatica Aubl. Pachira aquatica Heliocarpus appendiculatus Turcz. Heliocarpus appendiculatus Cav. Malvaviscus arboreus Hampea nutricia Fryxell Heliocarpus pallidus Rose Salvia rubiginosa Benth. C.K. Blake) Nectandra ambigens (S.F. Allen wallichii (Lindl.) Baill. (Kunth) Britten & (Kunth) aesculifolia Ceiba f. Baker Salvia purpurea Cav. Salvia purpurea Ginoria nudiflora (Hemsl.) Koehne M. Martens & Galeotti Salvia albiflora M. Ocimum sp.  piperita L. Mentha (Vahl) chamaedrys (Vahl) Marsypianthes Kuntze Marrubium vulgare L. Marrubium vulgare Hyptis suaveolens (L.) Poit. Quercus sp. Quercus Juglans pyriformis Liebm. Juglans pyriformis Hypoxis decumbens L. Hypoxis Hyptis mutabilis (Rich.) Briq. Family Fagaceae Meliaceae Lauraceae Malvaceae Lamiaceae Juglandaceae Hypoxidaceae Melastomataceae

AGRO 76 PRODUCTIVIDAD Real-Luna et al. (2021) Reference Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Contreras-Oliva et al. (2018); Villegas Contreras-Oliva (2000) Villegas et al. (2000) et al. (2018) Ramírez-Arriaga et al. (2010); Villegas Niembro-Rocas (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Bonet y Vergara (2016) Bonet y Vergara Bonet y Vergara (2016) Bonet y Vergara Bonet y Vergara (2016) Bonet y Vergara Bonet y Vergara (2016) Bonet y Vergara Bonet y Vergara (2016) Bonet y Vergara Villegas et al. (2000) Ramírez-Arriaga et al. (2018) Ramírez-Arriaga et al. (2018) Ramírez-Arriaga Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000)) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) et al. (2018) Contreras-Oliva Villegas et al. (2000) Niembro-Rocas et al. (2010); Villegas Niembro-Rocas (2000) Tree Tree Tree Tree Tree Tree Tree Tree Tree Vine Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Exotic Exotic Exotic Exotic Exotic Exotic Exotic Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized June All year All year All year All year January January May-July Flowering December November November- March-April November- September- September- May-August March-June January-May January-April January-April February-July February-April January-March January-March May-November December-April October- January August-December X X X X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X X Pollen Plant species Grevillea robusta A. Cunn. ex R. Br. robusta Grevillea Prunus serotina Ehrh. Prunus serotina C. Presl C. sagittata Pontederia L. Reseda odorata lupuloides (L.) Urb. Ziziphus sp. mangle L. Rhizophora candidissimum (Vahl) Calycophyllum DC. L. coccinea Ixora Coccoloba uvifera (L.) L. uvifera Coccoloba Antigonon leptopus Hook. & Arn Antigonon (Kunth) Pseudechinolaena polystachya (Kunth) Stapf Paspalum virgatum L. Paspalum virgatum P.J. Bergius P.J. Paspalum conjugatum Panicum sp. Piper sp. mexicana Moric. Platanus (Link) Hitchc. Brachiaria plantaginea Argemone platyceras Link & Otto platyceras Argemone Argemone mexicana L. Argemone W. T. Aiton T. Ligustrum lucidum W. Pisonia aculeata L. Pisonia aculeata Lopezia hirsuta Jacq. Lopezia Eucalyptus globulus Labill. Eucalyptus capuli (Schltdl. & Cham.) Eugenia Hook. & Arn. mexicana Steud. Eugenia jambos (L.) Alston Syzygium Callistemon citrinus (Curtis) Skeels Muntingia calabura L. Muntingia Family Poaceae Oleaceae Rosaceae Rubiaceae Myrtaceae Piperaceae Proteaceae Resedaceae Platanaceae Onagraceae Papaveraceae Polygonaceae Muntingiaceae Nyctaginaceae Pontederiaceae Rhizophoraceae

AGRO PRODUCTIVIDAD 77 Agro productividad 14 (4): 65-80. 2021 Reference Villegas et al. (2000) Parra-Tabla et al. (2019) Parra-Tabla Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Ramírez-Arriaga et al. (2018) Ramírez-Arriaga Contreras-Oliva et al. (2018) Contreras-Oliva Villegas et al. (2000) Villegas et al. (2000) (2018); Niembro-Rocas et et al. (2018); Niembro-Rocas Contreras-Oliva al. (2010) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. , (2000) et al. (2010); Villegas Niembro-Rocas (2000) et al. (2010); Villegas Niembro-Rocas (2000) Villegas et al. (2000) et al. (2010); Villegas Niembro-Rocas (2000) et al. (2018) Ramírez-Arriaga Villegas et al. (2000) et al. (2018) Contreras-Oliva Villegas et al. (2000) Villegas et al. (2000) et al. (2018) Ramírez-Arriaga Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Shrub Shrub Shrub Shrub Life-form Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Herbaceous Exotic Exotic Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized May August All year All year All year All year All year January January Flowering April-June December November- September- September- January-April February-May February-April August-March June-October January-March March-October February-March May-September September-March X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X Pollen Plant species Tribulus terrestris L. terrestris Tribulus Tribulus cistoides L. Tribulus Lippia myriocephala Schltdl. & Cham. Lippia myriocephala ex (Mill.) K. Kenn. Phyla fruticosa Hansen & B.F. Wunderlin Lantana camara L. Lantana (Ruiz & Pav.) Pers. (Ruiz & Pav.) virgata Cecropia obtusifolia Bertol. obtusifolia Cecropia Waltheria indica L. Waltheria Solanum sp. L. peltata Cecropia Pouteria sp. Kunth Buddleja cordata Dunal Solanum rostratum (L.) P. Royen (L.) P. zapota Manilkara Spermacoce confusa Rendle confusa Spermacoce negundo L. Acer Cupania sp. Sapindus saponaria L. Serjania sp. Schumach. Serjania racemosa Radlk. (Kunth) oliviformis Talisia Radlk. Thouinia paucidentata Thouinidium decandrum (Bonpl.) Radlk. Murraya paniculata (L.) Jack Murraya paniculata Family Rubiaceae Malvaceae Urticaceae Solanaceae Sapotaceae Sapindaceae Verbenaceae Zygophyllaceae Scrophulariaceae

AGRO 78 PRODUCTIVIDAD Real-Luna et al. (2021) Reference Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) (eléndez et al. (2018) Villegas et al. (2000) Badillo-Montaño et al. (2019) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Meléndez et al. (2018); Villegas (2000) Villegas et al. (2000) et al. (2012); Meléndez Castellanos-Potenciano et al. (2018); Villegas (2018); Ramírez-Arriaga (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Meléndez et al. (2018); Villegas (2000) Villegas et al. (2000) Villegas et al. (2000) Canto et al. (2017) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Exotic Exotic Exotic Exotic Exotic Exotic Exotic Exotic Status Native Native Native Native Native Native Native Native Native Native Native Native Native Native Naturalized Naturalized Naturalized Naturalized Naturalized May All year All year All year All year All year All year July-April Flowering April-June December March-July March-May July-August September- May-August May-August March-June March-June February-May January-June January-June February-April January-March May-November February-March, August, February, August, February, November-March December-March September-October X X X X X X X X X X X X X X X X X X X X X X X X X X Nectar X X X X X X X X X X X X X X X Pollen “hule” “jobo” “maíz” “alfalfa” “sandía” “melón” “girasol” “canola” “ciruelo” “pepino” “papaya” “mango” “plátano” “nanche” “camote” “chayote” “ayocote” “algodón” “guayaba” “calabaza” “calabaza” “calabaza” “aguacate” “cocotero” “tamarindo” “macadamia” “zapote negro” “frijol colorado” Common name Crop Cucumis melo L. Cucurbita maxima Duchesne Cucurbita moschata Cucurbita moschata Duchesne L. Cucumis sativus Ipomoea batatas (L.) Lam. Ipomoea batatas Carica papaya L. Citrullus lanatus (Thunb.)Citrullus lanatus & Nakai Matsum. Bouché Cucurbita ficifolia Sechium edule (Jacq.) Sw. Mangifera indica L. Mangifera Spondias mombin L. Cocos nucifera L. nucifera Cocos Helianthus annuus L. Helianthus Brassica napus L. Diospyros digyna Jacq. Diospyros Persea americana Mill. Gossypium hirsutum L. Medicago sativa L. Medicago sativa Hevea brasiliensis (Willd. ex A. Juss.) Müll. Arg. L. Phaseolus coccineus indica L. Tamarindus Byrsonima crassifolia (L.) Kunth Byrsonima crassifolia Spondias purpurea L. Spondias purpurea Musa paradisiaca L. Psidium guajava L. Zea mays L. Zea Macadamia integrifolia Maiden Macadamia integrifolia & Betche Family Poaceae Fabaceae Musaceae Lauraceae Myrtaceae Arecaceae Malvaceae Asteraceae Ebenaceae Caricaceae Proteaceae Brassicaceae Malpighiaceae Cucurbitaceae Anacardiaceae Euphorbiaceae Convolvulaceae Appendix 2 . Crops pollinated by bees in Mexico.

AGRO PRODUCTIVIDAD 79 Agro productividad 14 (4): 65-80. 2021 Reference Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Ramírez-Arriaga et al. (2018); Villegas (2000) Ramírez-Arriaga Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Villegas et al. (2000) Meléndez et al. (2018) Meléndez et al. (2018); Villegas (2000) Meléndez et al. (2018) Exotic Exotic Exotic Exotic Exotic Exotic Exotic Status Exotic Exotic Exotic Exotic Native Native Native Native Native Naturalized All year All year Flowering April-June March-May February-April February-April June-February June-February January-March January-March February-March February-March January-February December-February December-February X X X X X X X X X X X X X X Nectar X X X X X X X X X Pollen “lichi” “café” “pera” “chile” “mora” “ciruelo” “toronja” “naranja” “níspero” “jitomate” “durazno” “tejocote” “manzana” “rambután” “mandarina” “zarzamora”, “limón agrio” “zapote blanco” Common name Crop Prunus domestica L. Prunus persica (L.) Batsch Crataegus mexicana DC.Crataegus Eriobotrya japonica (Thunb.)Eriobotrya Lindl. Malus pumila Mill. Pyrus communis L. Pyrus communis Rubus eriocarpus Liebm. arabica L. Coffea Casimiroa edulis La Llave Casimiroa aurantiifolia (Christm.) Citrus  aurantiifolia Swingle Citrus maxima (Burm.) Merr. Citrus reticulata Blanco Citrus reticulata Citrus  sinensis (L.) Osbeck Litchi chinensis Sonn. L. Nephelium lappaceum Capsicum annuum L. Solanum lycopersicum L. Solanum lycopersicum Family Rutaceae Rosaceae Rubiaceae Solanaceae Sapindaceae

AGRO 80 PRODUCTIVIDAD