Next Article in Journal
The Diversity of Larvae with Multi-Toothed Stylets from About 100 Million Years Ago Illuminates the Early Diversification of Antlion-like Lacewings
Previous Article in Journal
Effects of Clothianidin Pesticide Application on the Strength of Honey Bee Colonies and Stress-Related Genes in the Vicinity of Rice Fields in the Republic of Korea
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 15
Issue 12
10.3390/d15121218
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Identification of Floral Resources Used by the Stingless Bee Melipona beecheii for Honey Production in Different Regions of the State of Campeche, Mexico

by
Román Alberto León-Canul
1,
Juan Bautista Chalé-Dzul
2,
Arely Anayansi Vargas-Díaz
1,3,*,
Juan Javier Ortiz-Díaz
4,
Kelly Cristina Durán-Escalante
4,
Eugenio Carrillo-Ávila
1 and
Alberto Santillán-Fernández
1,3
1
Colegio de Postgraduados, Campus Campeche, Champotón 24450, Campeche, Mexico
2
Hospital de Especialidades 1, Centro Médico Nacional Ignacio García Téllez, Instituto Mexicano del Seguro Social, Unidad de Investigación Médica Yucatán, Merida 97200, Yucatán, Mexico
3
CONAHCYT (Consejo Nacional de Humanidades Ciencias y Tecnologías), Benito Juárez, Ciudad de México 03940, Mexico
4
Departamento de Botánica, Universidad Autónoma de Yucatán, Campus de Ciencias Biológicas y Agropecuarias, Mérida 97000, Yucatán, Mexico
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(12), 1218; https://doi.org/10.3390/d15121218
Submission received: 24 October 2023 / Revised: 14 November 2023 / Accepted: 16 November 2023 / Published: 14 December 2023
Browse Figures
Versions Notes

Abstract

:
The stingless bee Melipona beecheii is experiencing colony decline due to floral resource scarcity caused by deforestation. A study was conducted to identify the floral resources used by M. beecheii using honey samples collected in four regions of the state of Campeche, Mexico. A melissopalynological analysis of sixteen collected honey samples identified 69 plant species from 24 families, and established that Fabaceae was the main plant family visited. Based on botanical origin, seven samples were classified as monofloral and nine as multifloral. The predominant species were Bursera simaruba, Lonchocarpus longistylus, Piscidia piscipula, Senna pallida and Senna racemosa. Shannon diversity index values (2.06–2.55) indicated moderate diversity in floral resources and Simpson diversity index values (0.82–0.89) indicated a moderate dominance of plant species in the studied regions. The results suggest M. beecheii is polylectic with some degree of specialization. The plant species identified as predominant in the studied honey samples are candidates for use in strategies intended to conserve the food resources used by M. beecheii on the Yucatan Peninsula.

1. Introduction

Stingless bees are highly social bees native to tropical and sub-tropical ecosystems [1]. They feed on pollen and nectar from flowers in their habitat [1,2]. Though some are polylectic, they do not collect pollen and nectar from all available flowers. Polyfloral diets are healthier for bees than monofloral diets because they ensure that the bees consume a wide range of nutrients [1,3,4]. The floral diversity available to bees is determined by the environmental and landscape composition of the area surrounding a hive site [3]. In recent years, reductions in native plant diversity, due to deforestation and increasing areas used for intensive agriculture, have been affecting food source quality and availability for bee colonies [2,5]. Stingless bees are strongly affected by deforestation because their small body size reduces their maximum flight distance capacity for obtaining food and nesting resources [6,7]. Stingless bee populations have consequently exhibited substantial declines worldwide [5,8,9].
Deforestation is widespread and ongoing in Mexico. It is particularly notable on the Yucatan Peninsula in the country’s southeast. The principal causes in this region are mainly associated with livestock expansion, as well as the expansion of agricultural areas, the latter of which is observed mainly in the state of Campeche [10,11].
The purported human health benefits of honey consumption from the native bee Melipona beecheii have driven an increase in demand [12,13,14]. However, M. beecheii is among the stingless bee species experiencing colony decline due to factors such as reduced floral resources and a lack of nesting sites [11]. Stingless bee species tend to exploit the predominant tree species in their environment [15]. Identifying the nectar and pollen source preferences of stingless bees like M. beecheii in Campeche can help to promote the use of native plant species that provide floral resources as conservation tools to increase stingless bee populations [16].
Melissopalynological studies are vital to identifying the nectar and pollen sources of bees and supporting improvements in colony and landscape management [17]. Melissopalynological research focused on identifying the nectar and pollen resources used by M. beecheii has been limited. One study was conducted in Costa Rica [18] and another in Cuba [19]. Three studies have been conducted in Mexico [20,21,22], but only one in the state of Campeche [23]; this study focused on a single site, meaning it is unrepresentative of the state as a whole. Much broader melissopalynological analyses are needed to identify M. beecheii floral resource preferences and to promote native vegetation reserves for conservation on the Yucatan Peninsula. The present study’s objective was to analyze honey samples from four regions in the state of Campeche, Mexico, to identify the floral resources used by M. beecheii.

2. Materials and Methods

2.1. Study Area

The state of Campeche is located in the north at 20°50′54″, in the south at 17°48′46″ latitude north, in the east at 89°07′16″ and in the west at 92°28′08″ longitude. Campeche borders, to the north, the Gulf of Mexico and Yucatan; Yucatan, Quintana Roo, and Belize to the east; the Republic of Guatemala and Tabasco to the south; and Tabasco and the Gulf of Mexico to the west. The predominant climate is warm–humid in 92.22% of the state, warm sub-wet in 7.73% of the state (eastern part), and semi-dry very warm and warm in 0.05% of the state (north region). The average annual temperature is 26 to 27 °C, and the annual rainfall is 1200 to 2000 mm from the north to the southeast of the state. The main types of vegetation are medium evergreen forest, medium sub evergreen forest, and medium sub deciduous forest, according to the CONABIO geoportal [24].

2.2. Sample Collection Sites

A total of sixteen samples were collected (Figure 1 and Table 1) from March to April 2021, in four regions in Campeche, Mexico: four in the southeast, seven in the north, three in the northeast, and two in the west. The largest number of samples was collected in the north because this is the area in which most of the meliponiculture activity is carried out in the state of Campeche [13]. Honey samples were removed from the honey pots in the hives with sterile Pasteur pipettes and transferred directly into amber-colored jars. Samples were stored at approximately 8 °C until analysis.

2.3. Palynological Analysis

The samples were processed following an established methodology [25]. Briefly, 10 g of each honey sample was diluted in 10 mL distilled water at near 40 °C. A total of 100 mL 95% EtOH was added and the mixture was centrifuged (5 min at 4000× g rpm). Samples were processed via acetolysis following the Erdtman method [26]. The pollen grains were mounted on glycerin–gelatin and the microscope slides were sealed with paraffin [27]. The slides were viewed using light microscopy with an optical microscope (40×) (Olympus BX41, Olympus Corporation, Tokyo, Japan) fitted with a camera (Amscope MU1803, China, United States of America). Images were processed using the AmScope v3.7 image software (AmScope, Irvine, CA, USA). Pollen grains in the honey samples were identified according to the taxonomic levels of family, genus and/or species. Unidentifiable grains were assigned an “sp.” designation. Pollen grains were identified based on morphological characteristics (polarity, size, shape, surface, and number of apertures) and a comparison with specimens in the Palynological Collection of Mesoamerica Floristic Diversity, Botany Department, Autonomous University of Yucatan (Universidad Autonoma de Yucatán—UADY). Palynological catalogs were also consulted [28,29,30].

2.4. Honey Botanical Origin

After pollen grain identification, the relative frequencies of the different pollen types or species were quantified by counting out 500 grains from each honey sample. Each sample composition could thus be analyzed in terms of (a) pollen frequency, (b) predominance by plant family and species (based on overall counts among all samples), and (c) species recurrence (number of times a species appears in all samples, divided by the total number of samples) [20]. Pollen frequency was used to classify pollen type dominance into four categories [31]: predominant (>45% total pollen in sample), secondary (15–45%), minor (3–15%), and residual (<3%). The honey samples were classified by botanical origin as either monofloral (dominated by one plant species at ≥45%) or multifloral (three or more secondary percentage pollen types) [31]. The predominance of the different plant families and species identified in the samples was calculated to determine which families were more important for M. beecheii, or whether any preference existed between plant families. Family and species recurrence was calculated to identify which species occurred in the largest number of samples, regardless of sampling site. Finally, the identified plant species were classified according to vegetation stratum (arboreal, shrub or herbaceous).

2.5. Ecological Analysis

The palynological data were analyzed using principal component analysis (PCA) and the ecological parameters were calculated. The Shannon–Wiener diversity index (H′) was used to determine the diversity of plants that M. beecheii visit. In this index, values less than 2 indicate low diversity, those from 2 to 3.5 indicate medium diversity, and those greater than 3.5 indicate high diversity [32]. The Simpson index (D) was used to measure the dominance of the species. Based on a range of 0 to 1, the index measures the probability of two taxa from the same sample, selected at random, belonging to the same species. A value of 0 represents equity (that is, species uniformity) and 1 represents the complete dominance of one taxon [33]. All analyses were run using the PAST program version 3.16 [22,34,35,36].

3. Results

3.1. Honey Botanical Origin

A total of 69 pollen types belonging to 24 plant families, with 12 indeterminate types, were identified in Melipona beecheii honey samples from the state of Campeche (Table 2). The most diverse family was Fabaceae (15 species), followed by Solanaceae (five species), Asteraceae (four species), Myrtaceae (four species), Sapindacea (four species), and Burseraceae (three species). Pollen grain frequency calculated for the samples as a whole showed Fabaceae (64.4% of samples), Myrtaceae (5.57%), Malvaceae (3.22%), and Asteraceae (3.21%) to be the most represented. Pollen types lacking botanical affinity occurred in six samples and were grouped into an unidentified class designated “sp.” (Table 2).
Of the sixteen analyzed honey samples, botanical origin was monofloral in seven (MC3, MC4, MC7, MC10, MC11, MC13, and MC14) and multifloral in the remaining nine. The M. beecheii that produced the honey samples had visited plants of various genera and with different growth modes or strata; the most visited were arboreal (54.04%) followed by bush (33.87%) and herbaceous (11.33 %) (Table 2).
Quantitative pollen analysis showed that the overall predominant pollen types were Senna racemosa (Mill.) H.S. Irwin and Barneby (16.9%), Piscidia piscipula (L.) Sarg. (13.9%), Lonchocarpus longistylus Pittier, (11.5%), Bursera simaruba (L.) Sarg. (9.3%), and Senna pallida (Vahl) H.S. Irwin and Barneby (6.9%) (Figure 2). In terms of occurrence in the honey samples, six pollen types were frequent: L. longistylus (94% of samples), S. racemosa (88%), P. piscipula (88%), Mimosa bahamensis Benth. (81%), B. simaruba (88%), and Eugenia axillaris (Sw.) Willd. (75%).

3.1.1. Southeast

In the four samples from the state’s southeast, a total of 32 pollen types were identified from thirteen families. The most frequent species were E. axillaris, L. longistylus, and S. racemosa (100% of samples) (Table 2). Two samples were considered monofloral: MC3 (B. simaruba) and MC4 (P. piscipula). Two samples were multifloral, one of which (MC1) contained Pimienta dioica (L.) Merr. and P. piscipula as a secondary pollen, while the other (MC2) contained S. racemosa and Viguiera dentata (Cavanilles) Spreng as a secondary pollen (Figure 3).

3.1.2. Northeast

In the three samples from the state’s northeast, 21 pollen types were identified from 12 families. The most frequent resources were B. simaruba, Leucaena leucocephala (Lam.) de Wit, L. longistylus, Mimosa bahamensis Benth., P. piscipula, and S. racemosa (Table 2). Botanical origin analyses showed one sample (MC7) to be monofloral (S. racemosa). Two samples were multifloral: MC5 contained secondary pollen from Boraginacea sp., P. piscipula, and V. dentata, and MC6 from L. longistylus, P. piscipula, and S. racemosa (Figure 3).

3.1.3. West

In the two samples from the west, 7 families and 16 pollen types were identified. The most frequent resources were B. simaruba, E. axillaris, L. leucocephala, M. bahamensis, S. pallida, and S. racemosa (Table 2). Both samples were multifloral: MC8 also contained Polygonaceae sp., M. bahamensis, and S. racemosa, and MC9 contained S. pallida and S. racemosa (Figure 3).

3.1.4. North

The seven samples from the north contained pollen from 14 families and from 37 pollen types. The most frequent resources were B. simaruba, L. longistylus, and P. piscipula. Four samples were considered monofloral: MC10 (S. palida), MC11 (L. longistylus), MC13 (Senna villosa (Mill.) H.S. Irwin and Barneby), and MC14 (P. piscipula) (Table 2). Three samples were multifloral: MC12 contained secondary pollen from B. simaruba and L. longistylus, MC15 from L. longistylus, S. racemosa, and Waltheria communis A.St.-Hil., and MC16 from L. longistilus and M. bahamensis (Figure 3).

3.2. Ecological Parameters

The Shannon diversity index values (H′) for M. beecheii honey samples collected in the four studied regions exhibited intermediate values (Southeast, 2.51; Northeast, 2.17; West, 2.06; and North, 2.55) (Margalef 1972), indicating that the bees visited several plant species. The Simpson index (D) values showed medium-level dominance in all four regions (Southeast, 0.88; Northeast, 0.82; West, 0.82; and North 0.89).

3.3. Principal Component Analysis (PCA)

The first principal component (PC1) represents 63.79% of the variance and the second (PC2) represents 18.58% (Figure 4); together, they explain 82.36% of the total variance, which is high (eigenvectors, Annex I). PC1 has a greater dimension on the biplot, representing the overall pollen type preference for the geographical region. PC2 is orthogonal to PC1, being the second most preferred. In the biplot, the points represent pollen types and the vectors (green lines) represent the geographical regions. A vector trending in the same direction represents a geographical region with similar pollen type preferences.
Based on PC1, it is clear that the samples from the west region are separated on the lower side of PC1, and are characterized by a preference for six pollen types: S. racemosa (most frequent), Poligonacea sp., L. leucocephala, M. bahamensis, S. pallida, and Solanum nudum Humb. and Bonpl. ex Dunal. The samples from the northeast and north regions are located on the upper side of PC1. The most frequent pollen types in the northeast samples were B. simaruba, L. leucocephala, L. longistylus, M. bahamensis, and P. piscipula, while in the samples from the north, the most frequent pollen types were B. simaruba, L. longistylus, and P. piscipula. The samples from the southeast are located between PC2 (main load) and PC1, and are characterized by pollen types from B. simaruba, E. axilaris, L. longistylus, P. dioica, P. piscipula, and V. dentata.
The presence of P. dioica was characteristic of samples from the southeast, and S. villosa was characteristic of those from the north. In contrast, the samples from the northeast were characterized by the presence of multiple pollen types: B. simaruba, M. bahamensis, P. piscipilua, S. racemosa, and V. dentata. The PCA results highlight the preference of M. beecheii for certain floral species, and these results coincide with the diversity and floristic composition values produced in the palynological analysis.
The dendrogram (Figure 5), generated based on the most frequent pollen types in each geographical region, classified the four regions into two groups. The first group corresponds to the honey samples from the southeast and north, and the second group includes the samples from the northeast and west. The pollen types among samples in the same group were similar, but differed from those in the other group.

4. Discussion

The pollen content in M. beecheii honey samples from the state of Campeche comprised 69 pollen types belonging to 24 plant families. This total is within the 4 to 71 pollen type range reported in previous melissopalynological analyses of M. beecheii honey samples [18,19,20,21,22,23]. The pollen types identified in the present results are similar to those reported in most of these studies [18,19,20,21,22]. Although a large number of plant species were identified in the present results, of the 69 pollen types, only 14 had relative frequency values greater than 15%, the threshold for deeming a pollen source as being important [31].
Fabaceae was clearly the main plant family visited by M. beecheii in the four studied regions. This is to be expected, since Melipona sp. bees generally exhibit, across different biomes, an affinity for plants within the Fabaceae, Melastomataceae, Myrtaceae, and Solanaceae families [37,38,39,40]. Fabaceae family plants have also occurred at high levels in M. beecheii honey in other studies [18,19,20,21,22,41]. In addition, this family has been reported in honey from the stingless bee Tetragonisca angustula [42]. Fabaceae is the third most diverse angiosperm family in the world with over 19,400 species and 730 genera [43]. It is one of the most abundant families in Mexico, with 93 genera and 1274 species; the Yucatan Peninsula alone is home to 78 genera and 228 species [44]. In the present results, the Fabaceae genera Lonchocarpus, Mimosa, Piscidia, and Senna were the most frequent pollen species in the honey samples. The Mimosa genus has been reported as a predominant pollen in M. beecheii honey [18,19,20,21,22] and is cited as an important pollen resource on the Yucatan Peninsula [45]. The Lonchorcapus genus has also been reported in M. beecheii honey and is considered a nectar source [20,21]. The genera Piscidia and Senna have been reported in M. beecheii honey [20] and are nectar-pollen sources on the Yucatan Peninsula [45]. It would be safe to infer that the Fabaceae family is a vital food source for M. beecheii in Campeche.
Another predominant pollen type in M. beecheii honey is Bursera simaruba. It has been identified frequently in M. beecheii honey in the state of Quintana Roo, Mexico [20]. It grows in a variety of habitats and is cited as a nectar-pollen resource on the Yucatan Peninsula [45]. The genera Bursera, Lonchocarpus, and Piscidia are considered abundant in the state of Campeche [46,47]. They belong to the arboreal stratum, considered typical of semi-evergreen tropical forests [48], which was the predominant strata identified in the pollen types in the M. beecheii honey samples (Table 2).
The floral resource analysis by geographic region indicates medium floral diversity, as corroborated by the medium-level Shannon–Wiener diversity index values (2.06–2.55) [32]. These values are similar to those reported elsewhere [18,19,20,21,22]. The Simpson index values (0.82–0.89) showed moderate plant species dominance in the studied regions, a result corroborated by the variable botanical origins in the four regions based on established criteria [31]; this can be seen in the fact that nine of the honey samples were multifloral and seven monofloral. Two of the monofloral samples were from the southeast region, one from the northeast, and four from the north. In previous studies, monofloral M. beecheii honeys were based on Eugenia sp., Andira inermis (W. Wright) DC, Mimosa pudica L., and Tabebuia ochracea A.H. Gentry [21,22,49]. In the present study, the monofloral samples were based on B. simaruba (southeast), L. longistylus (north), S. racemosa (northeast), S. palida (north), S. villosa (north), and P. piscipula (southeast and north). These results indicate regional similarities in vegetation. The southeast and north regions shared P. piscipula, suggesting they have similar plant community profiles. The PCA corroborated this, in that both regions were found on the positive axis and shared species such as B. simaruba, L. longistylus, and P. piscipula. Both also have a high degree of vegetation conservation; the samples in the southeast were collected from an area adjacent to the Calakmul Biosphere Reserve [50], and those in the north were collected near the Los Petenes Biosphere Reserve [13]. In contrast, the samples from the northeast and west regions were collected near agricultural areas [51]. Of particular note is that floral resources in the samples from the southeast and north regions, in which anthropogenic activity is minimal, exhibited greater diversity, as shown in their relatively higher Shannon–Wiener values (2.51 and 2.55, respectively) compared to the those from the northeast and west (2.17 and 2.06, respectively). These results support the conclusion that M. beecheii is a polylactic or generalist species, as previously reported [22]. However, some floral resources are fairly constant, though observed in different proportions in the samples; for example, B. simaruba, L. longistylus, P. piscipula, Mimosa, and Senna. Initially, it may seem contradictory that a generalist like M. beecheii would specialize, but some generalists do just that [52]. Stingless bees can be generalists in their search for resources, but they tend to consistently visit the same flower species, particularly those with dense flowers that offer high rewards [53]. The present results support this in that the different regions had medium-level Simpson index values, indicating a moderate plant species dominance. A diversity of native plant species dominated the resources identified in the M. beecheii honey analyzed here, but no cultivated forage plants were found, in contrast to previous reports [19,22]. The present study is the first to address the feeding habits of M. beecheii in different regions of the State of Campeche, Mexico, and the results strongly suggest a close relationship between M. beecheii and the native flora.

5. Conclusions

Melipona beecheii visited several floral resources. Overall, the predominant pollen types in the honey samples were B. simaruba, L. longistylus, P. piscipula, S. pallida, and S. racemosa. However, M. beecheii can apparently expand or alter its feeding niches in response to resource availability, since both the Shannon–Wiener diversity and Simpson indices indicated that floral resource variability was moderate in the studied geographic regions. The results confirm M. beecheii as being polylactic, with a preference for vegetation of the tree stratum. Especially important to note is that the M. beecheii honey samples indicated that this bee collects from a diversity of native plants, suggesting it has a close relationship with the native flora. The plant species identified as predominant in this study could be promising candidates for use in promoting vegetation that supports M. beecheii feeding strategies, and thus its conservation on the Yucatan Peninsula, specifically in the state of Campeche.

Author Contributions

Conceptualization, A.A.V.-D. and J.B.C.-D.; methodology, R.A.L.-C., K.C.D.-E. and J.B.C.-D.; software, E.C.-Á. and A.S.-F.; validation, J.B.C.-D., K.C.D.-E. and J.J.O.-D.; formal analysis, J.B.C.-D.; investigation, R.A.L.-C.; resources, A.A.V.-D. and J.B.C.-D.; data curation, J.B.C.-D.; writing—original draft preparation, R.A.L.-C. and A.A.V.-D.; writing—review and editing, A.A.V.-D.; visualization, A.A.V.-D. and E.C.-Á.; supervision, A.A.V.-D.; project administration, J.B.C.-D. and A.A.V.-D.; funding acquisition, A.A.V.-D. and J.B.C.-D. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by Estrategia Nacional para la Conservación y Uso Sustentable de los Polinizadores (Proyect CONV_ENCUSP_2023_04) and CONAHCYT (Proyect A1-S-38721).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author. The data are attributed to the project (CONV_ENCUSP_2023-04 and A1-S-38721) and therefore not publicly available without permission.

Acknowledgments

The authors are grateful to the producers of Campeche Mexico who kindly donated their honey for this study. We also want to thank the CONAHCYT for their scholarships (No. 765787), one of which was awarded to the first author to obtain their Master´s degree, and for their support for 364 research projects in Mexico.

Conflicts of Interest

The authors declare that they have no conflict of interest.

References

  1. Grüter, C. Stingless Bees; Springer International Publishing: Cham, Switzerland, 2020; Volume 109, pp. 1182–1186. [Google Scholar]
  2. Bueno, F.G.B.; Kendall, L.; Alves, D.A.; Tamara, M.L.; Heard, T.; Latty, T.; Gloag, R. Stingless bee floral visitation in the global tropics and subtropics. Glob. Ecol. Conserv. 2023, 43, e02454. [Google Scholar] [CrossRef]
  3. Donkersley, P.; Rhodes, G.; Pickup, R.W.; Jones, K.C.; Wilson, K. Honeybee Nutrition Is Linked to Landscape Composition. Ecol. Evol. 2014, 4, 4195–4206. [Google Scholar] [CrossRef] [PubMed]
  4. Roulston, T.A.H.; Cane, J.H. The effect of diet breadth and nesting ecology on body size variation in bees (Apiformes). J. Kans. Entomol. Soc. 2000, 73, 129–142. [Google Scholar]
  5. Toledo-Hernández, E.; Peña-Chora, G.; Hernández-Velázquez, V.M.; Lormendez, C.C.; Toribio-Jiménez, J.; Romero-Ramírez, Y.; Léon-Rodríguez, R. The stingless bees (Hymenoptera: Apidae: Meliponini): A review of the current threats to their survival. Apidologie 2022, 53, 8. [Google Scholar] [CrossRef]
  6. Araújo, E.D.; Costa, M.; Chaud-Netto, J.; Fowler, H.G. Body size and flight distance in stingless bees (Hymenoptera: Meliponini): Inference of flight range and possible ecological implications. Braz. J. Biol. 2004, 64, 563–568. [Google Scholar] [CrossRef]
  7. Cab-Baqueiro, S.; Ferrera-Cerrato, R.; Quezada-Euán, J.J.; Moo-Valle, H.; Vargas-Díaz, A.A. Nesting substrates and nest density of stingless bees in the Petenes Biosphere Reserve, Mexico. Acta Biol. Colomb. 2022, 27, 61–69. [Google Scholar]
  8. Requier, F.; Leonhardt, S.D. Beyond flowers: Including non-floral resources in bee conservation schemes. J. Insect Conserv. 2020, 24, 5–16. [Google Scholar] [CrossRef]
  9. Cairns, C.E.; Villanueva-Gutiérrez, R.; Koptur, S.; Bray, D.B. Bee populations, forest disturbance, and Africanization in Mexico. Biotropica 2005, 37, 686–692. [Google Scholar] [CrossRef]
  10. Ellis, E.A.; Hernández-Gómez, I.U.; Romero-Montero, J.A. Processes and causes of forest cover change in the Yucatan Peninsula. Ecosistemas 2017, 26, 101–111. [Google Scholar] [CrossRef]
  11. Villanueva-G, R.; Roubik, D.W.; Colli-Ucán, W. Extinction of Melipona beecheii and traditional beekeeping in the Yucatán peninsula. Bee World 2005, 86, 35–41. [Google Scholar] [CrossRef]
  12. Moo-Huchin, V.M.; Sauri-Duch, E.; Moo-Huchin, M.; Estrada-León, R.J.; Estrada-Mota, I.; Pérez-Pacheco, E. Antioxidant Activity of stingless bee honey. In Stingless Bee’s Honey from Yucatán: Culture, Traditional Uses and Nutraceutical Potential; Ortiz-Vázquez, E.L., Ruiz Ruiz, J.C., Magaña Ortiz, D.I., Ramon Sierra, J.M., Eds.; Nova Science Publishers: New York, NY, USA, 2016; pp. 77–90. [Google Scholar]
  13. Pat-Fernández, L.A.; Anguebes Franceschi, F.; Pat Fernández, J.M.; Hernández-Bahena, P.; Ramos-Reyes, R. Condition and perspectives of meliponiculture in mayan communities at Los Petenes biosphere reserve in Campeche, Mexico. Estud. Cult. Maya 2018, 52, 227–254. [Google Scholar] [CrossRef]
  14. Quezada-Euán, J.J.G. Taxonomy and diversity of the stingless bees. In Stingless Bees of Mexico; Quezada-Euán, J.J.G., Ed.; Springer: Cham, Switserland, 2018; pp. 1–40. [Google Scholar]
  15. Antonini, Y.; Martins, P.R. The value of tree species (Caryocar brasiliense) for a stingless bee Melipona quadrifasciata quarifaciata. J. Insect Conserv. 2003, 7, 167–174. [Google Scholar] [CrossRef]
  16. Van Drunen, S.G.; Linton, J.E.; Kuwahara, G.; Norris, D.R. Flower plantings promote insect pollinator abundance and wild bee richness in Canadian agricultural landscapes. J. Insect Conserv. 2022, 26, 375–386. [Google Scholar] [CrossRef] [PubMed]
  17. Guimarães, J.T.F.; Costa, L.; Zappi, D.C.; Batista, W.F., Jr.; da Lopes, K.S.; de Alves, R.C.O.; de Romeiro, L.A.; da Silva, E.F.; Carreira, L.M.M.; Rodrigues, T.M.; et al. Melissopalynology reveals the foraging preferences of the stingless bee Melipona seminigra pernigra Moure & Kerr 1950 (Apidae: Meliponini) in cangas of Serra dos Carajás, southeastern Amazonia. Biota Neotrop. 2021, 21, e20201004. [Google Scholar]
  18. Leal-Ramos, D.A.; León-Sánchez, D.L.E. Antagonism of Apis mellifera and Melipona beecheii for the sources of feeding. Rev. Cub. Cienc. For. 2013, 1, 102–109. [Google Scholar]
  19. Alvarez-Suarez, J.M.; Giampieri, F.; Brenciani, A.; Mazzoni, L.; Gasparrini, M.; González-Paramás, A.M.; Battino, M. Apis melifera vs. Melipona beecheii cuban polifloral honeys: A comparison based on their physicochemical parameters, chemical composition and biological properties. LWT-Food Sci. Technol. 2018, 87, 272–279. [Google Scholar]
  20. Villanueva-Gutiérrez, R.; Roubik, D.W.; Colli-Ucán, W.; Tuz-Novelo, M. The value of plants for the mayan stingless honey bee Melipona beecheii (Apidae: Meliponini): A pollen-based study in the Yucatán peninsula, Mexico. In Pot-Pollen in Stingless Bee Melittology; Vit, P., Pedro, S., Roubik, D., Eds.; Springer: Cham, Switzerland, 2018; pp. 67–76. [Google Scholar]
  21. Sánchez-Chino, X.M.; Jiménez-Martínez, C.; Ramírez-Arriaga, E.; Martínez-Herrera, J.; Corzo-Rios, L.J.; Godínez, G.L.M. Antioxidant and metal chelating activities of honeys of Melipona beecheii and Frieseomelitta nigra from Tabasco, Mexico. Tip Rev. Espec. Cienc. Quím. Biol. 2019, 22, 1–7. [Google Scholar]
  22. López-Roblero, E.; Espinosa, C.T.; López, J.A.G.; Grajales, J.C.; Quiroz-García, D.L. Floral resources collected by four native bees species in southern Mexico. Grana 2021, 60, 57–68. [Google Scholar] [CrossRef]
  23. Ramírez-Arriaga, E.; Pacheco-Palomo, K.G.; Moguel-Ordoñez, Y.B.; Zepeda García Moreno, M.; Godínez-García, L.M. Angiosperm resources for stingless bees (Apidae, Meliponini): A pot-pollen melittopalynological study in the Gulf of Mexico. In Pot-Pollen in Stingless Bee Melittology; Vit, P., Pedro, S., Roubik, D., Eds.; Springer: Cham, Switzerland, 2018; pp. 111–130. [Google Scholar]
  24. CONABIO. Portal de Información Geográfica—CONABIO. Available online: http://www.conabio.gob.mx/informacion/gis/ (accessed on 7 September 2023).
  25. Jones, G.D.; Bryant, V.M., Jr. The use of ETOH for the dilution of honey. Grana 2004, 43, 174–182. [Google Scholar] [CrossRef]
  26. Erdtman, G. The acetolysis method a revised description. Sven. Bot. Tidskr. 1960, 54, 561–564. [Google Scholar]
  27. Kisser, J. Bemerkungen zum Einschluss in Glycerin-Gelatine. Z Wiss Mikrosk Mikrosk Tecch 1935, 51, 372–374. [Google Scholar]
  28. Alfaro-Bates, R.G.; González-Acereto, J.A.; Ortiz-Díaz, J.J.; Viera-Castro, F.A.; Burgos-Pérez, A.I.; Martínez-Hernández, E.; Ramírez-Arriaga, E. Caracterización Palinológica de las Mieles de la Península de Yucatán, 1st ed.; Universidad Autónoma de Yucatán: Mérida, Mexico, 2010; 156p. [Google Scholar]
  29. Roubik, D.W.; Moreno, P.J.E. Pollen and Spores of Barro Colorado Island. Kew Bull. 1991, 47, 791. [Google Scholar] [CrossRef]
  30. Sánchez-Dzib, Y.D.L.A.; Sosa-Nájera, S.; Lozano-García, M.D.S. Pollen morphology of species from the tropical forest of the Candelaria River Basin, Campeche. Bol. Soc. Bot. 2009, 84, 83–104. [Google Scholar]
  31. Louveaux, J.; Maurizio, A.; Vorwohl, G. Methods of melissopalynology. Bee World 1978, 59, 139–157. [Google Scholar] [CrossRef]
  32. Margalef, R. Homage to Evelyn Hutchison, or why is there an upper limit to diversity. Trans. Conn. Acad. Arts. Sci. 1972, 44, 211–235. [Google Scholar]
  33. Simpson, E.H. Measurement of diversity. Nature 1949, 163, 688. [Google Scholar] [CrossRef]
  34. da Luz, C.F.P.; Fidalgo, A.O.; Silva, S.A.; Rodríguez, S.S.; Nocelli, R.C.F. Comparative floral preferences in nectar and pollen foraging by Scaptotrigona postica (Latreille 1807) in two different biomes in São Paulo (Brazil). Grana 2019, 58, 200–226. [Google Scholar] [CrossRef]
  35. Hanifa, H.S.; Sartiami, D.; Priawandiputra, W.; Buchori, D. Characteristics of apiculture and meliponiculture in Banten province, Indonesia: Profile of beekeepers, bee and pollen diversity. IOP Conf. Ser. Environ. Earth Sci. 2021, 948, 12050. [Google Scholar] [CrossRef]
  36. Pinto, R.S.; Silva, A.G.; Rêgo, M.M.C.; Albuquerque, P.M.C. Pollen analysis of the post-emergence residue of Euglossa bees (Apidae: Euglossini) nesting in an urban fragment. Sociobiology 2019, 66, 88–96. [Google Scholar] [CrossRef]
  37. Ramalho, M.; Kleinert-Giovannini, A.; Imperatriz-Fonseca, V.L. Important bee plants for stingless bees (Melipona and Trigonini) and africanized honeybees (Apis mellifera) in neotropical habitats: A review. Apidologie 1990, 21, 469–488. [Google Scholar] [CrossRef]
  38. Carvalho, C.A.L.; Moreti, A.D.C.; Marchini, L.C.; Alves, R.D.O.; Oliveira, P.C.F. Pollen spectrum of honey of “Uruçu” bee (Melipona scutellaris Latreille, 1811). Rev. Bras. Biol. 2001, 61, 63–67. [Google Scholar] [CrossRef] [PubMed]
  39. Martins, A.C.L.; Rêgo, M.M.C.; Carreira, L.M.M.; Albuquerque, P.M.C. Pollen spectrum of honey of Tiúba (Melipona fasciculata Smith, 1854, Hymenoptera, Apidae). Acta Amaz. 2011, 41, 183–190. [Google Scholar] [CrossRef]
  40. Matos, V.R.; Santos, F.A.R. Pollen in honey of Melipona scutellaris L. (Hymenoptera: Apidae) in an Atlantic rainforest area in Bahia, Brazil. Palynology 2017, 41, 144–156. [Google Scholar] [CrossRef]
  41. Espinoza-Toledo, C.; Vázquez-Ovando, A.; Santos, R.T.D.L.; López-García, A.; Albores-Flores, V.; Grajales-Conesa, J. Stingless bee honeys from Soconusco, Chiapas: A complementary approach. Rev. Biol. Trop. 2018, 66, 1536–1546. [Google Scholar] [CrossRef]
  42. de Novais, J.S.; Absy, M.L. Melissopalynological records of honeys from Tetragonisca angustula (Latreille, 1811) in the lower amazon, Brazil: Pollen spectra and concentration. J. Apic. Res. 2015, 54, 11–29. [Google Scholar] [CrossRef]
  43. Ahmad, F.; Anwar, F.; Hira, S. Review on medicinal importance of fabaceae family. Pharmacologyonline 2016, 3, 151–157. [Google Scholar]
  44. Villaseñor, J.L. Diversidad y distribución de las Magnoliophuya de Mexico. Interciencia 2003, 28, 160–167. [Google Scholar]
  45. Villanueva-Gutiérrez, R.; Moguel-Ordóñez, Y.B.; Echazarreta, G.C.M.; Arana, L.G. Monofloral honeys in the Yucatán Peninsula, Mexico. Grana 2009, 48, 214–223. [Google Scholar] [CrossRef]
  46. Báez, C.G.; Zamora-Crescencio, P.; Hernández-Mundo, S.C. Structure and floristic composition of deciduous forest of Mucuychacan, Campeche, Mexico. For. Veracruzana 2012, 14, 9–16. [Google Scholar]
  47. Zamora-Crescencio, P.; Domínguez-Carrasco, M.D.R.; Villegas, P.; Gutiérrez-Báez, C.; Manzanero-Acevedo, L.A.; Ortega-Haas, J.J.; Puc-Chávez, R. Floristic composition and structure of the secondary vegetation in northern Campeche, Mexico. Bol. Soc. Bot. Mex. 2011, 89, 27–35. [Google Scholar]
  48. Carreón-Santos, R.J.; Valdez-Hernández, J.I. Estructura y diversidad arbórea de vegetación secundaria derivada de una selva mediana subperennifolia en Quintana Roo. Rev. Chapingo Ser. Cienc. For. Ambiente 2014, 20, 119–130. [Google Scholar]
  49. Zamora, L.G.; Beukelman, K.; van den Berg, B.; Arias, M.L.; Umaña, E.; Aguilar, I.; Gross, N. The antimicrobial activity and microbiological safety of stingless bee honeys from Costa Rica. J. Apic. Res. 2014, 53, 503–513. [Google Scholar] [CrossRef]
  50. Bohn, J.L.; Diemont, S.A.; Gibbs, J.P.; Stehman, S.V.; Vega, J.M. Implications of mayan agroforestry for biodiversity conservation in the Calakmul biosphere reserve, Mexico. Agrofor. Syst. 2014, 88, 269–285. [Google Scholar] [CrossRef]
  51. Martínez-Vásquez, E.; Vázquez-Garcia, V. Impacto f the transgenic soy expansión on corn and honey production in Campeche, Mexico. Rev. Latinoam. Estud. Socioamb. 2019, 26, 173–190. [Google Scholar]
  52. Roubik, D.W.; Villanueva-Gutierrez, R. Invasive africanized honey bee impact on native solitary bees: A pollen resource and trap nest analysis. Biol. J. Linn. Soc. 2009, 98, 152–160. [Google Scholar] [CrossRef]
  53. Momose, K.; Yumoto, T.; Nagamitsu, T.; Kato, M.; Nagamasu, H.; Sakai, S.; Harrison, R.; Itioka, T.; Hamid, A.; Inoue, T. Pollination biology in a lowland dipterocarp forest in Sarawak, Malaysia. Characteristics of the plant-pollinator community in a lowland dipterocarp forest. Am. J. Bot. 1998, 85, 1477–1501. [Google Scholar] [CrossRef]
Diversity 15 01218 g001
Figure 1. State of Campeche, Melipona beecheii honey sample collection sites. MC1–MC3: 20 Noviembre, Calakmul; MC4; La Lucha 1, Calakmul; MC5: Xcalot Akal, Hopelchén; MC6: Ich ek, Hopelchén; MC7: San Antonio, Hopelchén; MC8 and MC9: Sihochac, Champotón; MC10: Pucnachén, Calkiní; MC11: Tankunché, Calkiní; MC12: Santa María, Calkiní; MC13: Sahcabchén, Calkiní; MC14: Tankunché, Calkiní; MC15: Pucnachén, Calkiní; MC16: Santa María, Calkiní.
Figure 1. State of Campeche, Melipona beecheii honey sample collection sites. MC1–MC3: 20 Noviembre, Calakmul; MC4; La Lucha 1, Calakmul; MC5: Xcalot Akal, Hopelchén; MC6: Ich ek, Hopelchén; MC7: San Antonio, Hopelchén; MC8 and MC9: Sihochac, Champotón; MC10: Pucnachén, Calkiní; MC11: Tankunché, Calkiní; MC12: Santa María, Calkiní; MC13: Sahcabchén, Calkiní; MC14: Tankunché, Calkiní; MC15: Pucnachén, Calkiní; MC16: Santa María, Calkiní.
Diversity 15 01218 g001
Diversity 15 01218 g002
Figure 2. Pollen types identified in Melipona beecheii honey samples from Campeche, Mexico. (a) Senna racemosa; (b) Lonchocarpus longistylus; (c) Piscidia piscipula; (d) Senna villosa; (e) Bursera simaruba; (f) Pimienta dioica; (g) Mimosa bahamensis; (h) Waltheria communis; (i) Croton sp. Scale: 10 μm.
Figure 2. Pollen types identified in Melipona beecheii honey samples from Campeche, Mexico. (a) Senna racemosa; (b) Lonchocarpus longistylus; (c) Piscidia piscipula; (d) Senna villosa; (e) Bursera simaruba; (f) Pimienta dioica; (g) Mimosa bahamensis; (h) Waltheria communis; (i) Croton sp. Scale: 10 μm.
Diversity 15 01218 g002
Diversity 15 01218 g003
Figure 3. Characterization of the honey samples collected in different regions of Campeche, Mexico, as monofloral or multifloral. Numbers in the bars correspond to the percentages of pollen frequency per sample. Pollen taxa were included only as predominant (>45%) and secondary (15–45%).
Figure 3. Characterization of the honey samples collected in different regions of Campeche, Mexico, as monofloral or multifloral. Numbers in the bars correspond to the percentages of pollen frequency per sample. Pollen taxa were included only as predominant (>45%) and secondary (15–45%).
Diversity 15 01218 g003
Diversity 15 01218 g004
Figure 4. Principal components analysis (PCA) of the floral origin of Melipona beecheii honey from the state of Campeche. (Ar) Alternanthera ramosissima; (B) Boraginaceae sp.; (Bs) Bursera simaruba; (C) Croton sp.; (Ea) Eugenia axillaris; (Lel) Leucaena leucocephala; (Ll) Lonchocarpus longistylus; (Mb) Mimosa bahamensis; (Mp) Mimosa pudica; (Ne) Neomillspaughia emarginata; (P) Poligonaceae sp.; (Pc) Protium copal; (Pd) Pimienta dioica; (Pp) Piscidia piscipula; (S) Sapindaceae sp.; (Sep) Senna pallida; (Sn) Solanum nudum; (Sr) Senna racemosa; (Sv) Senna villosa; (Vd) Viguiera dentata; (Wc) Waltheria communis.
Figure 4. Principal components analysis (PCA) of the floral origin of Melipona beecheii honey from the state of Campeche. (Ar) Alternanthera ramosissima; (B) Boraginaceae sp.; (Bs) Bursera simaruba; (C) Croton sp.; (Ea) Eugenia axillaris; (Lel) Leucaena leucocephala; (Ll) Lonchocarpus longistylus; (Mb) Mimosa bahamensis; (Mp) Mimosa pudica; (Ne) Neomillspaughia emarginata; (P) Poligonaceae sp.; (Pc) Protium copal; (Pd) Pimienta dioica; (Pp) Piscidia piscipula; (S) Sapindaceae sp.; (Sep) Senna pallida; (Sn) Solanum nudum; (Sr) Senna racemosa; (Sv) Senna villosa; (Vd) Viguiera dentata; (Wc) Waltheria communis.
Diversity 15 01218 g004
Diversity 15 01218 g005
Figure 5. Dendrogram representation of Euclidean distance, based on frequent pollen types in each geographical region.
Figure 5. Dendrogram representation of Euclidean distance, based on frequent pollen types in each geographical region.
Diversity 15 01218 g005
Table 1. Collection sites of Melipona beecheii honey samples and vegetation type.
Table 1. Collection sites of Melipona beecheii honey samples and vegetation type.
RegionsLocalitySampleVegetation Type
Southeast
20 de Noviembre, CalakmulMC1Medium sub-evergreen forest
20 de Noviembre, CalakmulMC2Medium sub-evergreen forest
20 de Noviembre, CalakmulMC3Medium sub-evergreen forest
La lucha I, CalakmulMC4Medium sub-evergreen forest
Northeast
Xcalot Akal, HopelchénMC5Medium sub-deciduous forest
Ich ek, HopelchénMC6Medium sub-deciduous forest
San Antonio, HopelchénMC7Medium sub-deciduous forest
West
Sihochac, ChampotónMC8Medium sub-deciduous forest
Sihochac, ChampotónMC9Medium sub-deciduous forest
North
Pucnachén, CalkiníMC10Medium deciduous forest
Tankuché, CalkiníMC11Medium deciduous forest
Santa María, CalkiníMC12Medium deciduous forest
Sahcabchén, CalkiníMC13Medium deciduous forest
Tankunché, CalkiníMC14Medium deciduous forest
Pucnachén, CalkiníMC15Medium deciduous forest
Santa María, CalkiníMC16Medium deciduous forest
Table 2. Pollen types identified in Melipona beecheii honey samples from Campeche, Mexico.
Table 2. Pollen types identified in Melipona beecheii honey samples from Campeche, Mexico.
TaxaMayan NameStratumMC1MC2MC3MC4MC5MC6MC7MC8MC9MC10MC11MC12MC13MC14MC15MC16PR (%)
Acanthaceae
Avicennia germinansTa’abchéA 1 0.2 13
Amaranthaceae
Alternanthera ramosissimaZakmuulH 11.2 0.813
Asteraceae
Asteraceae sp. H 2.3 6
Chaptalia nutans H 0.6 6
Viguiera dentataTaj (tajonal)H7.218.5 0.818.71.8 0.2 38
Boraginaceae
Boraginaceae 24 6
Brassicaceae
Arabideae sp. H 40.2 13
Burseraceae
Bursera simarubaChakajA 3.450 0.22.44.95.15.50.935.420.90.218.62.67.488
Protium copalSak chakajA 90.2 2 19
Cactaceae
Cactaceae sp. H 0.2 6
Combretaceae
Bucida bucerasPuctéA 0.8 6
Convulvulaceae
Ipomea sp. H 0.2 6
Cyclanthaceae
Carludovica palmataGuanoH 0.4 6
Euphorbiaceae
Croton sp. S 2.118.4 13
Euphorbiaceae 1.9 6
Fabaceae
Acacia sp. S 0.2 6
Acacia collinsiiSubinS 0.7 6
Caesalpinia gaumeriKitim che’A 2.20.6 13
Gliricidia sepium A -- 6.6 3.413
Leucaena leucocephalaWaaximA 3.71.52.62.94.29 2-44
Lonchocarpus longistylusBaal che’A3.62.33.91.26.4222.9-0.919.647.231.31.20.216.824.994
Lonchocarpus xuulK’an xu’ulA 1.20.613
Mimosa bahamensisKáatsim blancoA 1.94.51.21.316.827.50.90.4 0.95.7 3.226.681
Mimosa pigraJe’ beech’S 25.6 6
Mimosa pudicaMúuts’il xiiwH 0.4 4.20.4 0.41.41.30.67.850
Piscidia piscipulaJa’abinS20.6 78.124.72610.2 2.20.94.24.947.33.210.181
Senna atomaria A 4.9 6
Senna pallidaCh’iilib michS 6.427.958.815.43 31
Senna racemosaK’an loolA1027.96.9 13.627.666.726.84012.10.21.715.81.719.4 88
Senna villosaSaal che’S 5.962.1 6.3 19
Gesneriaceae
Achimenes palmata H 0.2 6
Malvaceae
Luehea speciosaK’an kaatA 0.4 6
Waltheria communis H 5.32.234.57.425
Waltheria rotundifolia H 1.6 1.8119
Meliaceae
Meliaceae sp. 0.8 6
Myrtaceae
Eugenia axillaris S6.56.67.36.30.9 2.20.71.70.4-0.80.6 0.6 75
Eugenia foetidaSak loobA 1.5 6
Pimienta dioicaBoox poolA44.7 3.10.4 19
Psidium guajavaPichiS 0.2 6
Nictaginaceae
Pisonia aculeataBéebH 3.9 6
Onagraceae
Ludwigia octovalvisMáaskab che’H2.2 1.62.619
Poligoncaceae
Coccoloba manzanillensis A 4.7 0.6 13
Neomillspaughia emarginataSak iitsa’S 0.4 3.7 1.5 11.231
Poligonaceae sp. A0.3 17.6 1.7 19
Primulaceae
Jacquinia aurantiaca S 0.4 6
Rubiaceae
Psychotria nervosaK’aananS 3.9 6
Sapindaceae
Sapindacea sp. H 13.91 13
Serjania goniocarpaChak sik’iix le’H 2.4 0.8 13
Serjania lundelliibuy aak’H 0.8 2.2 13
Thouinia paucidentatak’an chuunupA 2.3 4.4 13
Sapotaceae
Sideroxylon foetidissimumSibulA 1.4 6
SOLANACEAE
Cestrum nocturnumk’an chuunukS 4.2 6
Solanacea sp. S 12.7 65
Solanum lanceifolium H 1.1 6.413
Solanum lanceolatumSikil múuchS 4.6 6
Solanum nudumBoox kúutsS -3.3 5.5 1.3 9
Solanum tridynamunKóon ya’ax iikH 4.6 6
Unidentified sp.s
sp. 1 1.2 6
sp. 2 0.2 6
sp. 3 0.9 6
sp. 4 2.6 6
sp. 5 3.3 6
sp. 6 1.2 6
sp. 7 0.6 6
sp. 8 6.6 6
sp. 9 0.2 6
sp. 10 3.7 6
sp. 11 0.6 6
sp. 12 1.1 6
Total 100100100100100100100100100100100100100100100100
The numbers correspond to the relative frequency and white space is equal to zero, which is the equivalent of not finding grain. Abbreviations: A, arboreal; S, shrubs; H, herbaceous; PR, percentage of recurrence.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

León-Canul, R.A.; Chalé-Dzul, J.B.; Vargas-Díaz, A.A.; Ortiz-Díaz, J.J.; Durán-Escalante, K.C.; Carrillo-Ávila, E.; Santillán-Fernández, A. Identification of Floral Resources Used by the Stingless Bee Melipona beecheii for Honey Production in Different Regions of the State of Campeche, Mexico. Diversity 2023, 15, 1218. https://doi.org/10.3390/d15121218

AMA Style

León-Canul RA, Chalé-Dzul JB, Vargas-Díaz AA, Ortiz-Díaz JJ, Durán-Escalante KC, Carrillo-Ávila E, Santillán-Fernández A. Identification of Floral Resources Used by the Stingless Bee Melipona beecheii for Honey Production in Different Regions of the State of Campeche, Mexico. Diversity. 2023; 15(12):1218. https://doi.org/10.3390/d15121218

Chicago/Turabian Style

León-Canul, Román Alberto, Juan Bautista Chalé-Dzul, Arely Anayansi Vargas-Díaz, Juan Javier Ortiz-Díaz, Kelly Cristina Durán-Escalante, Eugenio Carrillo-Ávila, and Alberto Santillán-Fernández. 2023. "Identification of Floral Resources Used by the Stingless Bee Melipona beecheii for Honey Production in Different Regions of the State of Campeche, Mexico" Diversity 15, no. 12: 1218. https://doi.org/10.3390/d15121218

APA Style

León-Canul, R. A., Chalé-Dzul, J. B., Vargas-Díaz, A. A., Ortiz-Díaz, J. J., Durán-Escalante, K. C., Carrillo-Ávila, E., & Santillán-Fernández, A. (2023). Identification of Floral Resources Used by the Stingless Bee Melipona beecheii for Honey Production in Different Regions of the State of Campeche, Mexico. Diversity, 15(12), 1218. https://doi.org/10.3390/d15121218

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop