A review of the melliferous flora of Yucatan peninsula, Mexico, on the basis for the honey production cycle

Melliferous flora of importance for honey production

A total of 23 species of MF play a very important role for beekeeping in the YP, within these species is G. floribundum “ts'iitsilche” (Mayan name), which is considered the main source of nectar production for bees in the central and northern portion of the YP [2, 29]. The honey produced with G. floribundum is of high value for beekeepers, since it is in demand in European markets for its quality and flavor [30]. However, Villanueva-Gutiérrez [11] mentions that in addition to G. floribundum, there are other highly important honey species for honey production such as V. dentata “tajonal” (Spanish name), Metopium brownei “chechem” (Mayan name), Bursera simaruba “chaká” (Mayan name) and Thouinia canescens “kaan-chunub” (Mayan name), which were found among the 16 most important species for honey production. It also agrees with what was reported by SIAP [31], CONABIO [32] and Alfaro-Bates et al. [33], which indicates that the preferred food sources for A. mellifera in the YP come from B. simaruba, G. floribundum, L. latisiliquum, P. piscipula, Turbina corymbosa “xtabentún” (Mayan name) and V. dentata.

The previous MF species considered as the main food sources were confirmed by Villanueva-Gutiérrez [34], through load samples (palynological analysis) in European and African bees in apiaries established in the Quintana Roo. Likewise, Villanueva-Gutiérrez et al. [35] using similar method confirmed that B. simaruba, P. piscipula and V. dentata are priorities for honey production in the YP, agreeing with the information obtained through surveys to producers by Porter-Bolland [36] and Zapata-Cauich [37].

Currently, various authors have continued to conduct interviews with producers in the YP, for example, Aguilar-Hernández et al. [38] found B. simaruba, P. piscipula and V. dentata as the most important nectar-pollinator plants during the harvest season in Quintana Roo. Coh-Martínez et al. [5] recorded 56 MF species using the same method; indicating that beekeepers only depend on 18 species (includes the aforementioned) to obtain their honey production in the Xmaben community in Campeche. This agrees when the MF studies of the region are analyzed together, with 15–40 species considered to be of greater importance for beekeeping.

However, MF species reported to be of high importance for honey production vary in the number of flowers available per year, seasonality, quality and quantity of nectar generated, and its abundance in different types of vegetation [39, 40]. Therefore, it is necessary to evaluate these aspects different scales of the landscape in the YP, as well as the pollen grains in honey from apiaries to identify their presence and abundance; flowering periods and distribution patterns to determine their local utility.

Growth habit

In the growth habits of MF at the regional level, a greater number of herbs were found, followed by shrubs and trees; however, the beekeepers in the interviews of the different local studies indicate that the trees are of greater importance for the production of honey, which is reflected in the different studies that are based on surveys. For example, Carnevali et al. [7] include 99 MF species, of these, 42 correspond to trees and 36 to herbs, followed by shrubs (11), lianas (6) and herbaceous climbers (4). While CONABIO & AECID [41] records 93 species, of these, 36 are trees, 17 shrubs, followed by herbs (13), herbaceous climbers (5), woody climbers (2) and palms (2). This same pattern is also observed in local studies of the predominance of tree species, Porter-Bolland [36] of 101 MF species recorded in the mountainous area of Campeche, a total of 83 are trees and 10 shrubs, followed by climbing species (5) and vines (3). Likewise, Coh-Martínez et al. [5] reported for this same area, a greater diversity of trees (39), followed by shrubs (6), herbs (5), climbers (4) and lianas (2).

The botanical families of MF best represented in this study are Fabaceae, Asteraceae and Euphorbiaceae; these families also stand out within the five families with the highest number of species at the national and regional level, Asteraceae (3,057, 147), Fabaceae (1,903, 230), Orchidaceae (1,213, 132), Poaceae (1,047, 216) and Euphorbiaceae with (714, 113) [7, 8].

Melliferous flora by seasons

The lowest number of flowering MF species was recorded from December to February (in the transition from nortes to dry season), although in general the three seasons recorded a similar number of MF species (Fig. 5). However, the most important species for beekeeping in the YP were recorded in the dry season, when trees in dry forests lose their leaves from 50 to 75% and in humid forests from 25% as a strategy to resist seasonal drought [7, 32, 42]. During the dry season from March to April (harvest period in beekeeping), the highest flowering peak of plants occurs (mainly legume species) for their subsequent fruiting throughout the rainy season [43]. The flowering pattern of increase or decrease in MF during the climatic seasons or for the beekeeping cycle cannot be easily observed at a regional scale, but when it is evaluated at a local scale, the flowering of MF increases in the dry seasons and decreases with the rain season [5]. This observed pattern is possibly due to the fact that the studies include only MF species of high importance for the beekeeping cycle derived from the knowledge of the interviewed producers. Considering that the honeys obtained during the dry season are of higher quality because they present a lower amount of moisture (greater than or equal to 20%) [12, 44], which contributes to reducing the presence of microorganisms that cause honey fermentation [45].

The rainy season in the YP is considered by beekeepers as a time of scarcity of food for bees due to the limited availability of floral resources [40]. A similar diversity of MF was recorded here with respect to other stations, but this flora is considered by beekeepers as of little nutritional importance for bees; hence they tend to incorporate food supplements to prevent the escape of bees from the hive [42]. In addition, beekeepers indicate that the honey produced in the rainy season is of poor quality due to the high humidity that allows easy fermentation of honey, reduction in storage time and changes in its organoleptic properties [32, 42]. At the beginning of this season (June), the most important species for beekeeping are still in bloom; but they decrease in July and August (Fig. 5), then the availability of herbaceous species increases, allowing the maintenance of bee hives.

Regarding the nortes season, a similar high number of MF flowering species were also found in October and November; but with a decrease in December. In beekeeping, this season is considered the recovery of bee colonies due to the increase in the availability of nectar food sources [2]. In this season, the most important species for bees are climbing herbaceous plants of the Convolvulaceae family that can grow in disturbed sites or with open spaces or roadsides where their establishment is favored by the availability of light in the different types of vegetation in the region [5, 42].

Species distribution

The distribution of the most important species for apiculture has been recorded in the northern and central portions of the YP in the low and medium deciduous and subdeciduous forests [7]. For example, V. dentata grows mainly in low deciduous forest, low forest with columnar cacti, low floodplain forest, semideciduous medium forest, and in secondary vegetation and coastal dunes. For their part, G. floribundum and L. latisiliquum also grow in these same types of predominant vegetation throughout the north and center of the region [23]. The collections in the southern zone of these species are scarce, due to the fact that they dominate more humid ecosystems such as MSFT and low flooded forests [46].

The state with the highest number of MF species at the regional level is Campeche, followed by Quintana Roo and Yucatán, influencing Campeche to be the largest honey-producing area, in addition to the fact that it has a tradition inherited from pre-Hispanic times of caring for bees and its existing MF [14, 47]. Hence, the rural communities of Campeche have been able to take advantage of this wide diversity of MF of the dry and humid regions for the production of honey [40, 48]. Furthermore, it is important to mention that organic honey is exported from the municipality of Calakmul in Campeche, with humid forests; since about half of its territory is located within the Calakmul Biosphere Reserve, an extensive protected area where one can take advantage of the beekeeping as an economic alternative that does not affect the ecosystem [42]. However, in terms of productivity, Yucatan is the main producer and exporter of honey at the national level [31]. In 2015, out of 15,058 tons of honey produced in Mexico; Yucatán contributed 45%, Campeche 37% and Quintana Roo 18% [31].

The honey obtained in the YP, according to its MF composition, is classified as monofloral (with a dominant type of pollen > 45%) and multifloral (with several types of pollen < 45%) [33]. Some authors indicate that 58% of the honey produced in Yucatan is monofloral (obtained from Viguiera dentata, Mimosa bahamensis and Bursera simaruba) and multifloral in Campeche (with 10 types of honey) and Quintana Roo (with five types of honey) [49]. Alfaro-Bates et al. [33] indicate that these differences in the types of honey are due to the diversity of MF that Campeche and Quintana Roo have with respect to Yucatan, since bees have more MF options available for their food. However, in the dry and humid forests of the YP (in a gradient from south to north) these floristic elements considered as monofloral or of the majority of the MF species of high importance for honey production, share the different types of vegetation and are distributed homogeneously throughout the region (Figs. 1 and 2). Even so, the populations of these species differ in their flowering periods and flowering peaks depending on where they grow, being probably monofloral according to this classification based on the type of vegetation, peak and favorable year of flowering when the honey is obtained (pre-harvest, harvest and postharvest) for melissopalynological analysis. In the YP, monofloral honeys possibly come from apiaries established in core or transition areas of mangroves in coastal areas with particular and dominant species such as Avicennia germinans (Additional file 2: Fig. S1); this is when their harvest is carried out in the rainy season and when the flowering of the plants decreases most important species for beekeeping (Laynes-Magaña et al., in prep.).

Apiculture challenges

The following challenges are directly related to the scarcity or lack of floral food (nectar and pollen) impacting the local bee colonies, making them more susceptible to attacks by various pathogens. Among the challenges facing apiculture in the region are diseases such as varroosis (Varroa destructor Anderson & Trueman), pest infestations by Aethina tumida Murray as well as rapid deforestation and habitat fragmentation of areas where the apiaries are located [5, 13]. Furthermore, the availability of bee food during the rainy season when the number of species in bloom decreases; causing a dip in the breeding percentages in the bee colony or the bees abandon their nests/hives in search of nectar and pollen. Hence, the beekeepers have to provide food supplements in the form of sugar syrup for the subsistence of the bees [2]. This decline in local bee populations for floral resources has been analyzed in European and Africanized bees during October in the Sian Ka'an Reserve in Quintana Roo, Mexico by Ceballos-Martínez [50] and Villanueva-Gutiérrez et al. [51].

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