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Article

Wild Bee Diversity and Bee–Plant Interactions in Tropical and Temperate Forest Clearings in a Natural Protected Area in Central West Mexico

by
Alvaro Edwin Razo-León
1,
Alejandro Muñoz-Urias
1,*,
Claudia Aurora Uribe-Mú
1,
Francisco Martín Huerta-Martínez
1,
Hugo Eduardo Fierros-López
2,
Miguel Vásquez-Bolaños
2,
Gustavo Moya-Raygoza
2 and
Pablo Carrillo-Reyes
2
1
Departamento de Ecología Aplicada, Centro Universitario de Ciencias Biológicas y Agropecuarias (CUCBA), Universidad de Guadalajara, Zapopan 44600, Jalisco, Mexico
2
Departamento de Botánica y Zoología, Centro Universitario de Ciencias Biológicas y Agropecuarias (CUCBA), Universidad de Guadalajara, Zapopan 44600, Jalisco, Mexico
*
Author to whom correspondence should be addressed.
Insects 2024, 15(12), 1009; https://doi.org/10.3390/insects15121009
Submission received: 7 November 2024 / Revised: 30 November 2024 / Accepted: 18 December 2024 / Published: 20 December 2024
(This article belongs to the Section Social Insects and Apiculture)
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Simple Summary

Bees depend on plants for food and reproduction, making the preservation of natural areas crucial as refuges for pollinators. Seasonal tropical dry forests, particularly in forest clearings, are among the richest habitats for bees, yet these ecosystems are severely threatened, with only 27% of their original area remaining in Mexico. In contrast, temperate forests show lower bee diversity and face high deforestation rates, with 40% of their land converted to other uses. This research compared wild bee diversity and their interactions with plants in forest clearings of seasonal tropical dry and temperate forests in the Sierra de Quila, a protected area in central west Mexico. Over the course of one year, bee species and their plant interactions were studied at four sites. Seasonal tropical dry forest clearings were found to host a higher number of bee species compared to temperate forest. Nine bee species were present in both forest types, forming a link between interaction networks. This study also found that the overlap in bee–plant interactions was low, likely due to different flowering periods and bee behavior, which helps reduce competition and supports greater bee diversity. This highlights the need to conserve both forest types to protect bee diversity and their essential pollination roles.

Abstract

Background: Bees rely on plants for nutrition and reproduction, making the preservation of natural areas crucial as pollinator reservoirs. Seasonal tropical dry forests are among the richest habitats for bees, but only 27% of their original extent remains in Mexico. In contrast, temperate forests harbor fewer bee species and face high deforestation rates, with 40% of their area converted to other land uses. This study aimed to estimate the α and β diversities of wild bees and compare bee–plant interaction networks between these two vegetation types. Methods: Wild bees and their interactions with plants were monitored for one year in four sites within the Área de Protección de Flora y Fauna Sierra de Quila. Two sites corresponded to seasonal tropical dry forest and two to temperate forest. α and β diversity, connectance, nestedness, web asymmetry, and niche overlap were analyzed. Results: Sierra de Quila harbors high bee diversity, with 155 species in tropical dry forest and 103 in temperate forest. Species turnover between vegetation types was high, although nine species used floral resources in both forests, connecting the interaction networks. Conclusions: Sierra de Quila diverse habitats promote high bee diversity, with niche partitioning and low connectance facilitating coexistence across different vegetation types.

Graphical Abstract

1. Introduction

Bees depend on vegetation for nutrition and reproduction because their diet is based exclusively on floral resources [1]. To collect these resources, bees visit different flowers, which in turn leads to the pollination of many plant species [2]. This mutual relationship contributes greatly to the biodiversity and function of terrestrial communities [3]. Bees are considered the most important pollinator group, but are threatened by habitat loss and other human disturbances [4,5,6,7,8].
Bee communities are affected by the quality of physical and ecological characteristics of their habitat. Each habitat has different food resources, climatic conditions, nesting sites, competitors, and predators [9]. The structure, composition of vegetation, and, in particular, the richness and abundance of the herbaceous species [10,11] are the main factors that affect bee communities, because vegetation directly influences the availability of floral resources through space and time [12]. On the other hand, climate also affects bee communities. Several studies have recorded a negative correlation between altitude, species richness, and abundance of bees. This relationship is mainly attributed to temperature [13,14,15,16,17], accompanied by other abiotic variables such as wind speed, precipitation, and water vapor pressure [15]. In addition, the lower productivity of colder ecosystems has a negative influence on the bee community [18]; for example, at a lower temperature, the floral density decreases and affects biotic interactions such as competition for floral resources [16].
The main factors influencing bee community composition may change in an elevational gradient. Bees tend to be richer and the most dominant pollinator group at low elevations [19]. Therefore, the beta diversity between low-elevation habitats is determined to a greater extent by the turnover of bees due to species replacement than by the changes in composition due to the loss of species in a less rich assemblages; and sites with subequal altitudes present a greater similarity [20]. On the other hand, plant community compositions present strong changes in species in altitudinal gradients, so the interactions between plants and bees can be very specific for certain habitats [21]. As altitude increases, the number of pollinator and plant species typically declines, which has been demonstrated to have a significant impact on the structure of these interaction networks [22].
Nevertheless, there is a lack of research examining pollinator–plant interactions in tropical regions. Moreover, most existing studies have focused on individual plant species or primarily on vertebrate pollinators, with studies on insect pollinators being particularly scarce [23]. It is therefore imperative to safeguard natural habitats with high floral diversity, which serve as vital pollinator reservoirs [24], and to advance our understanding of bee communities and their ecological requirements.
Temperate and tropical forest differ in climatic conditions. These forests occur along elevational gradients in tropical and subtropical regions like Mexico; temperate forests (TF) develop in high elevations, and seasonally dry tropical forests develop in low elevations (SDTF). These ecosystems also differ in diversity and availability of floral resources throughout the year. Seasonally dry tropical forests have a high plant diversity; mellitophily is the most important pollination system. SDTF are the ecosystems with the greatest richness of bees after the arid zones in Mexico. In contrast, in TF a lower number of bee species has been recorded [25]. In Mexico, SDTF is one of the vegetation types most affected by the impact of human activities as only an estimated 27% of its original surface area persists [26]. TF also presents high rates of deforestation, and an estimated 40% of its surface area has changed to other land uses [27]. Natural protected areas contain native conserved vegetation with high floral diversity that act as pollinator reservoirs [28] and allow for the study of the ecology of bee communities under relatively unaltered environments. This knowledge will facilitate the development of conservation strategies for these pollinators under disturbance [11].
The Sierra de Quila Flora and Fauna Protection Area in western central Mexico offers a great opportunity to study bee richness, species with medium abundance and high abundance within communities (alpha diversity), and compare bee species compositions between contiguous SDTF and TF on an elevational gradient (beta diversity). The aims of this work were to compare bee diversity and bee–plant interaction networks in forest clearings of contiguous SDTF and TF in the altitudinal gradient of a protected area in western Mexico. Particularly, we aimed to (1) estimate the α and β diversities of native bees and the plant community they visit for feeding and (2) compare interaction network metrics and β diversity between the two types of vegetation. We expect that each type of vegetation has a specific community composition of native bees and that their relationships with plants will differ drastically between them.

2. Materials and Methods

2.1. Description of the Study Area

The Sierra de Quila Flora and Fauna Protection Area is in Jalisco 100 km southwest of the city of Guadalajara in the municipalities of Tecolotlán, Tenamaxtlán, San Martín Hidalgo and Cocula between the coordinates 20°14′ and 20°22′ N and 103°57′ and 104°07′ W. The Sierra spans 15,912 hectares with a mountainous relief with an altitudinal gradient ranging from 1300 at the foothills to 2560 m a.s.l. Six vegetation types are described for the Sierra de Quila, where TF covers 82% of the protected area, SDTF covers 15%, and the rest of the vegetation is composed of other reduced vegetation types [29].
Two study sites were selected in each vegetation type along its altitudinal gradient (Figure 1). The SDTF sites were placed at 1400 and 1700 m of altitude, and the TF sites at 1800 and 2150 m of altitude. All sites were forest clearings with the presence of herbs and shrubs embedded in the corresponding vegetation type because open areas with abundant floral resources favor the presence of bees [11,30]. A transect 70 m long by 5 m wide was established at each site, i.e., two in seasonally dry tropical forest (SDTF1 and SDTF2) and two in temperate forest (TF1 and TF2). The same transects were sampled each month. The shortest distance among transects was 1.12 km, between SDTF1 to SDTF2, and the longest distance was 4.75 km between TF2 and SDTF1 (Figure 1).

2.2. Data Collection

For one year, from October 2013 to October 2014, sampling was carried out to collect wild bees. Honeybees were omitted, as they are not native and because the presence of managed (hives) and feral colonies in the area makes it impossible to recognize feral bees. During the dry season (from December to June), the sites were visited two days per month due to the low availability of floral resources, while during the rainy season (from July to November), the sampling was carried out four days per month. In this season, there occurs the peak of the flowering period in the study area when the emergence of adult bees is higher.
Bees were captured with an aerial net on flowering plants, in flight, or in their nests. At each site, two people worked collecting bees on the established transects for three hours between 10:00 and 16:00 h, the period of maximum activity of bees. When collected on flowering plants, the information of the visited plant species by each bee was registered and used to construct plant–bee interaction networks. Once collected, the specimens were processed following the standard method for bee preservation [31] and then determined to the lowest taxonomic level possible by specialists in bees. The samples were deposited in the Entomological Collection of the Centro de Estudios en Zoología de la Universidad de Guadalajara, Jalisco, Mexico (CZUG). In addition, specimens were collected from the plants visited by the bees and determined by a specialist in flora of the study area. Specimens are in the Herbarium “Luz María Villarreal de Puga” at the Institute of Botany of the University of Guadalajara (IBUG).

2.3. Data Analyses

Rarefaction/extrapolation curves based on samples with equal completeness were used to determine differences in species richness (q0) and species number with median frequency (q1) and higher frequency (q2) for bee communities. Rarefaction and extrapolation curves and 95% confidence intervals were based on the bootstrap method [32] and calculated with 200 replicates using the software R package iNEXT (version 3.0.1) [33]. To analyze the diversity of bee communities collected when they were visiting flowers, as well as the plant community visited by the bees and their interactions, we additionally calculated the richness of these bees, plants, and their interactions (q0) using the same method. β diversity of bees and plants were analyzed across sites following [34], where the index of dissimilarity of Sorensen ꞵSor is decomposed in their turnover (ꞵSim) and nestedness (βSne) components using the software R package vegan (version 2.6—6) [35].
Qualitative bee–plant interaction networks were constructed for each site, with the adjacency matrix containing the information of bee visits to flowers, where rows represented plant species, columns bee species, ones were used to represent interactions between two species, and zeros were used to represent the absence of interactions. Network metrics were obtained using the bipartite package of R [36,37]. The metrics analyzed were as follows: (a) connectance (the proportion of links observed in relation to the total possible given the species recorded [38]; (b) mean number of links per species [39]; (c) nestedness and the temperature of the matrix (values close to zero mean high nestedness, and values close to 100 mean chaos), and also we analyzed statistically whether nestedness occurs randomly by comparing 999 random null models against the observed network using the vegan package [35]; (d) web asymmetry (balance between numbers in the bee and plant species [40]); and (e) niche overlap (mean similarity in interaction patterns between species of the same trophic level, where values near 0 indicate no niche overlap and 1 indicates complete niche overlap). Finally, we calculated the β diversity of interactions (BWN) and their components, diversity of interactions, the β diversity of interactions due to species turnover (βST), and the β diversity of interactions established between species common to both communities (βOS) using the index of dissimilarity of Sorensen [41,42].

3. Results

A total of 1574 individuals and 200 species were recorded; 155 were recorded in SDTF, and 92 species in TF (see Table S1). All recorded species are represented in the network, except for three that were collected flying or near their nests. Sample completeness was greater than 90% in all sites, except for TF1 with 84%. Bee richness (q0) showed significant differences between vegetation types, but not within them (Figure 2). SDTF1 and SDTF2 also showed a higher number of common species than TF1 and TF2, and SDTF1 showed a higher number of dominant species than the rest of the sites (Figure 2). Eleven species were common to all sites (ubiquitous), seven species were exclusive to TF sites, fifty-two species were exclusive to SDTF sites, and the rest of the species were present at sites of both vegetation sites but were not ubiquitous (see Table S1). All records are of polylectic bee species, i.e., bees that collect pollen of unrelated plant species, except for eleven oligolectic species, i.e., bees that collect pollen of a 177 reduced group of related plant species, usually from one family [43].
Species richness per family was consistently higher in SDTF sites than in TF sites (Figure 3 and Figure 4). The family with the highest richness was Apidae for both vegetation types. In SDTF, Megachilidae and Halictidae had an intermediate and similar richness, while in TF, Halictidae was richer than Megachilidae (Figure 3 and Figure 4). The families with the lowest richness were Andrenidae and Colletidae.
Beta diversity of bees and plants was high among sites (with βsor values between 0.43 and 0.84) and was attributed to a much greater extent to the species replacement (βsim) than to loss of species due to nestedness of species assemblages from more diverse to less diverse sites (βsne); β diversity values (βsor) of bees and plants were higher between TF than between SDTF sites. The nestedness component (βsne) was considerably higher among sites with different vegetation types than between sites within the same vegetation type, particularly for bees, reflecting the loss of species richness from SDTF to TF sites (Table 1). The lowest beta diversity values (βsor and βsim) for plants (i.e., the most similar plant communities) were between SDTF2 and TF1, the sites with the least difference in elevation. For bees, these sites had the second lowest value after the value between SDTF1 and SDTF2.
The networks of SDTF had higher plant richness, bee richness and number of interactions than the networks of TF. The number of plants in SDTF1 was significantly higher than in the other sites. Niche overlap in plants and bees was lower in SDTF than TF. On the other hand, the links per species in SDTF were higher than in TF. Connectance, nestedness and web asymmetry showed no trend in relation to vegetation type. All networks were significantly nested, and web asymmetry showed that there were more bees than plants (Table 2), as it is generally true for plant–pollinator networks Beta diversity of interactions (βWN) is high at all sites, showing an almost complete change in the identity of interactions, and is mostly explained by the turnover of species (βST) rather than by the rewiring of interactions among species shared by the compared networks (Table 1). Rewiring of interactions (βOS) was highest between SDTF sites and between the sites with the least difference in elevation (SDTF2 and TF1), which are the pairs of sites with the lowest turnover of bee species (βsim).
Salvia xalapensis, Lamiaceae was one of the plant species with the highest number of visiting species in the four sites, whereas Marina scopa was found in both SDTF sites and in TF1; in SDTF1, it was visited mainly by bees of the Apidae family, while in SDTF2 and TF1, it was visited mainly by Megachilids. Dyssodia tagetiflora, Asteraceae in SDTF1 was an important resource for all five bee families, but the number of species visiting this plant decreased in SDTF2 and TF1, Condea albida, Lamiaceae, found in all four sites, was visited by a high number of species in SDTF, while in TF, only one record was observed for each site due to its limited abundance (Figure 3 and Figure 4).

4. Discussion

Our investigation focuses on examining the patterns of alpha and beta diversity in bees, visited plants, and bee–plant interactions among forest clearing sites within contiguous SDTF and TF. Our findings reveal that plant and bee richness were higher in the clearings of SDTF compared to clearings of TF in the Sierra de Quila Flora and Fauna Protection Natural Area. Beta diversity was greater among sites of different types of vegetation than between sites of same type of vegetation. TF sites showed higher beta diversity than SDTF sites. Moreover, beta diversity was higher in plants than in bees and was primarily driven by species turnover rather than species loss. Bee–plant interaction networks from SDTF exhibited higher richness of species than those from TF and were characterized by large network sizes, more links per species, and greater niche overlap, and interaction turnover was almost total among sites.
Our sampling conducted in forest clearings was biased towards bees visiting herbs and shrubs. Bee richness at the sampling sites is likely due to the high annual plant richness in vegetation clearings. This provides ample food resources and potential nesting sites for solitary bee species [30,44]. Due to these sampling sites, it is possible that bee species with a preference for tree flower resources may be underrepresented. However, this may not be the case for bee species that utilize both pollen and nectar from tree flowers as well as herbaceous resources.
Apidae, Halictidae, and Megachilidae were the richest families of bees in the study area, as reported in previous studies on the melitofauna of Mexico [45,46,47,48,49,50]. These families are known for their high diversity in the tropics, with numerous generalist species, including seasonal species, and a great range of social levels [51].
Bee richness in Mexico is intermediate between that of the United States of America and Central America. The xeric regions of North America have the highest number of species [21], followed by SDTF, and finally TF. This relationship is confirmed in Mexico [45,49,52]. The estimated α diversity of bees and plants was found to be higher in SDTF; in this vegetation type, the most plants are pollinated by animals [53]. Bee richness is related to the diversity of plants that require melitophilic pollination [25]. It has been demonstrated that bee diversity is strongly related with plant species diversity, and a positive relationship has been observed between bee abundance and floral abundance [30]. The increased availability of food resources may enable a greater partitioning of the food niche, which could potentially support a larger number of bee species.
The study shows that the richness of bee species is reflected in oligolectic bees. Specifically, ten out of the eleven species recorded are present in the SDTF, while only one is found in the TF. It is worth noting that the number of specialist bee species tends to increase in areas with higher plant richness, [24]. Kleptoparasitic species (bees that do not collect pollen and lay eggs in another bee’s nest) depend on the richness and abundance of their hosts. Nine out of the ten species recorded in the area are found in the SDTF, while only two are found in the TF. These results have potential implications for the conservation of bee species and their habitats, possibly due to greater host richness in the SDTF.
Several authors reported a decrease in bee species as altitude increases [14,15,46,54]. Higher elevation sites (q0, q1, q2) exhibit lower diversity, likely due to colder temperatures that restricts small bees by their poor ability to thermoregulate [55]. In contrast, lower elevation SDTF sites show higher diversity, influenced by climatic factors such as higher temperature and relative humidity, which affects life cycles and reduces dehydration risk [15,56]. This is reflected in sites with minimal elevation differences, such as SDTF2 and TF1, which have comparable diversities.
Elevated values of β diversity were reported among both bee and plant species. There was a general trend of reduced β diversity observed in plants and bees across SDTF sites. High values of β diversity were mainly due to species turnover (ꞵSim) rather than species loss (ꞵSne). The high species turnover may be attributed to environmental gradients associated with the elevation of the sampled sites ranging from 1400 to 2150 m of altitude [34], because pollinating insects tend to occur at particular elevations rather than across the entire altitudinal gradient [57,58].
Additionally, it has been shown that sites with more homogeneous environmental conditions tend to reduce species turnover [59]. This could explain the lower species turnover observed in SDTF sites compared to TF sites, particularly due to the pronounced temperature differences between the cold and warm months of the TF resulting from altitude gradient.
β diversity bees exhibited the lowest rate of species turnover compared to the plants among all sampled sites, which is consistent with previous research [30]. This can be attributed to the large number of generalist bee species and their ability to fly. In contrast, plants showed high values of species turnover, perhaps due to their lack of mobility, as noted by [34]. This pattern was also observed in other taxonomic groups and is related to their ability to disperse. Groups with higher mobility tend to have a lower rate of replacement between sites [59].
Altitudinal difference in the sites SDTF2 and TF1 separated by 100 m in elevation share some plant species, and could be considered as ecotone; in the case of plant species, we observed the lowest diversity βSor of all sites studied, while bees showed the second lowest value. However, βSne for bees is the highest value, so there is a marked trend in the loss or gain of species between these sites; it is possible that this loss of bee species is caused by the effects of temperature decrease related to altitude increase [13,14,15,16,17,18].
The βWN > 0.9 indicates high interaction diversity among the sites and vegetation types; there have been reported similarly high values of βWN (0.70–0.86) between different successional stage or season of year in SDTF or altitudinal gradient [60]. βWN and βST among vegetation types was high, and differences in interactions along the gradient are mainly explained by species turnover with high βST values, coupled with decreasing plant and pollinator richness at higher altitudes, with only a few generalist species persisting at all sites [61].
However, generalist bees exhibit remarkable flexibility in utilizing different floral resources, as suggested by the varying foraging patterns observed among bees depending on the site [62]. For example, social species bees that exhibit higher abundance, better foraging strategies, and provide the greatest number of interactions in plant–bee relationships [63]. This is consistent with the with other results that report losses of up to 80% in unique interactions; they also observed that these changes mostly affect species with low abundance and specialists, as these are the ones that tend to be replaced when habitat conditions change [64,65]. This high βWN diversity aligns with the principles of functional redundancy, ensuring that ecosystem functioning remains unaffected even with the loss of certain species such as bees [66], as well as niche complementarity, where different species utilize the same resource but in different temporal and spatial contexts [67].
The interaction networks are dynamic and change over time, likely to reduce competition between species, especially if they are generalists. Changes in interaction identities have been observed at different scales, including throughout the day, year, or during different early stages of succession, or due to the introduction of new species into the system [60,68,69]. These seasonal or habitat changes may be due to the replacement of species from the networks or to the turnover of interactions in common species.
The network structure appears to be homogeneous across the different vegetation types, except for those affected by richness. The different sites have similar values of connectance and niche overlap. It has been observed in mutualistic networks that forbidden interactions due to morphological and phenological constraints are common in bee–plant interactions [70,71].
Some of the forbidden interactions are due to annual sampling because there is no overlap between the flight period of bees and the flowering period of many plants. This is known to reduce connectance in very large networks because it lowers the probability that a bee will visit all plant species. However, sites with a high richness of bee species may experience increased competition for food and a subsequent decrease in connectance. Furthermore, sites with low c are highly vulnerable to the loss of their most connected species [72]. It is therefore recommended to protect social species such as meliponines and bumblebees, which are highly connected and sensitive to habitat disturbance [73].
Nestedness is a common feature of animal–plant interaction networks [70,71,74,75], Sierra de Quila is no exception; we found this pattern in all networks, which supports the idea that pollination systems tend to nestedness because of the coevolutionary process. Additionally, the high degree of nestedness observed is characterized by a group of polylectic bees that feed on generalist plants, and these connect the specialist species [76,77].
The low niche overlap observed serves as a mechanism to avoid competition between species and foster beneficial bee–plant relationships, which facilitate the partitioning of the food niche and support a high diversity of bees. To coexist in these sites, a reduction, partial, or total change in the feeding niche can take place, so that different bee species would visit different plant species, depending on the habitat. Bees can change their feeding even to plants with less preference and to reduce the resources used, increasing their specialization in some plants due to competition with other bee species.
Consequently, they may be displaced to use other resources or even excluded from these habitats. The SDTF sites exhibited reduced levels of niche overlap compared to the TF sites, observed across both plants and bees. This result suggests that as altitude rises, niche partitioning becomes less pronounced, likely attributable to the decreased productivity and richness species associated with higher altitudes, which are colder [18]. Moreover, there exists a positive correlation between floral abundance and temperature [16], implying that in higher altitude regions, competition for floral resources intensifies, leading to more specialized interactions among species affecting the pollinator network [22]. This observation is further supported by the higher average number of links per species observed in SDTF sites compared to temperate forests.
The foraging patterns of bees vary depending on the site; they can use completely different resources in most cases, suggesting that the most dominant bee species show great flexibility in their food resources [62]. We observed low values of niche overlap of the network in general, potentially attributed to interactions among different bee species and even with other pollinators, which may modify the fundamental niche or feeding preferences of individual species when others are absent [78]. To sustain bee richness across diverse vegetation types, it is necessary to reduce the overlap in food resources.
Our results show that some interaction network indices between sites remained similar, and that the change in networks are due to the composition of species and the turnover interactions between sites and is greater among types of vegetation. Consequently, safeguarding the diverse array of native vegetation is essential for preserving wild bee communities. Alterations to these habitats could accelerate the loss of bees or plants that thrive under specific environmental conditions [79].
The Sierra de Quila can be an important site for the conservation of wild bees, the melitophilic flora, and the interaction of pollinating plants due to the great richness of species favored by the altitudinal gradient and also due to having different types of vegetation, which represents an essential ecosystem service; this is evident in bee communities, at least in relatively well-conserved environments in Jalisco.
The importance of the study area is related to high diversity due to their high specific richness; the species with greater dominance are formed by several species, at least 12 eusocial species, which form colonies, and some solitary bees that contribute to this diversity; also, bee–plant interaction networks with different vegetation types are interconnected by these species.
The Sierra de Quila Flora and Fauna Protected Area is a priority reservoir of wild bee diversity, particularly in the clearings of seasonally dry tropical forests, which exhibit greater species richness and diversity compared to temperate forests. Differences in bee–plant interactions between these forest types reveal a high turnover in interactions, underscoring the importance of conserving both habitats to maintain bee diversity and ensure the essential pollination services they provide to ecosystems.
For future research, long-term monitoring of bee–plant interactions is recommended to better understand interannual climate variability and its effects on these interactions. In addition, studies focusing on the pollination efficiency of the most abundant bee species are strongly encouraged. Finally, the integration of other groups of insect pollinators is suggested to build more comprehensive pollinator–plant networks and to better understand their role in plant reproduction.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/insects15121009/s1, Table S1: List of acronyms of bees and plants. Habits of recollection pollen (HRP): Polilectic (P), oligolectic (O), kleptoparasitic (K) do not collect pollen. Eusocial bees in bold letters.

Author Contributions

Conceptualization, methodology, fieldwork, writing—original draft preparation A.M.-U., A.E.R.-L., M.V.-B., and G.M.-R.; data curation, A.E.R.-L., P.C.-R., H.E.F.-L., and C.A.U.-M.; writing—review and editing, F.M.H.-M., C.A.U.-M., M.V.-B., and G.M.-R.; statistical analysis A.M.-U., A.E.R.-L., and F.M.H.-M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by Universidad de Guadalajara.

Data Availability Statement

The data from this study are available in the article.

Acknowledgments

The authors are grateful for the comments of reviewers who improved previous versions of the manuscript, Regional Committee for the Protection of the Natural Resources of the Sierra de Quila A. C. for all its institutional and logistic support. Thank you to Saúl Alejandro Huerta Sánchez for the map elaboration. We would also like to thank Martha Lopezaraiza Mikel for her valuable feedback on how to improve the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Reyes-Novelo, E.; Méléndez, V.R.; Ayala, R.; Delfín, H.G. Bee faunas (Hymenoptera: Apoidea) of six natural protected areas in Yucatan, Mexico. Entomol. News 2009, 120, 530–544. [Google Scholar] [CrossRef]
  2. Nantes-Parra, G. Abejas silvestres y polinización. Manejo Integr. Plagas Agroecol. 2005, 75, 7–20. [Google Scholar]
  3. Jordano, P.; Vázquez, D.; Bascompte, J. Networks of Mutualistic Plant-Animal Interactions. In Ecology and Evolution of Plant-Animal Interactions: Concepts and Applications; Medel, R., Aizen, M.A., Zamora, R., Eds.; Editorial Universitaria: Santiago de Chile, Chile, 2009; pp. 17–42. [Google Scholar]
  4. Biesmeijer, J.C.; Roberts, S.P.; Reemer, M.; Ohlemüller, R.; Edwards, M.; Peeters, T.; Schaffers, A.P.; Potts, S.G.; Kleukers, R.; Thomas, C.D.; et al. Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 2006, 313, 351–354. [Google Scholar] [CrossRef]
  5. Winfree, R.; Aguilar, R.; Vázquez, D.P.; LeBuhn, G.; Aizen, M.A. A meta-analysis of bees’ responses to anthropogenic disturbance. Ecology 2009, 90, 2068–2076. [Google Scholar] [CrossRef] [PubMed]
  6. Potts, S.G.; Biesmeijer, J.C.; Kremen, C.; Neumann, P.; Schweiger, O.; Kunin, W.E. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 2010, 25, 345–353. [Google Scholar] [CrossRef]
  7. Martins, A.C.; Gonçalves, R.B.; Melo, G.A. Changes in wild bee fauna of a grassland in Brazil reveal negative effects associated with growing urbanization during the last 40 years. Zoologia 2013, 30, 157–176. [Google Scholar] [CrossRef]
  8. van der Sluijs, J.P.; Vaage, N.S. Pollinators and global food security: The need for holistic global stewardship. Food Ethics 2016, 1, 75–91. [Google Scholar] [CrossRef]
  9. Nantes-Parra, G.; Palacios, E.; Parra, A. Efecto del cambio del paisaje en la estructura de la comunidad de abejas sin aguijón (Hymenoptera: Apidae) en Meta, Colombia. Rev. Biol. Trop. 2008, 56, 1295–1308. [Google Scholar]
  10. Widhiono, I.; Sudiana, E.; Sucianto, E.T. Insect pollinator diversity along a habitat quality gradient on Mount Slamet, Central Java, Indonesia. Biodiversitas 2016, 17, 746–752. [Google Scholar] [CrossRef]
  11. Alvarenga, A.S.; Silveira, F.A.; dos Santos Júnior, J.E.; de Novais, S.M.A.; Quesada, M.; Neves, F.D.S. Vegetation composition and structure determine wild bee communities in a tropical dry forest. J. Insect Conserv. 2020, 24, 487–498. [Google Scholar] [CrossRef]
  12. Winfree, R.; Kremen, C. Are ecosystem services stabilized by differences among species? A test using crop pollination. Proc. R. Soc. B 2009, 276, 229–237. [Google Scholar] [CrossRef] [PubMed]
  13. Conrad, K.M.; Peters, V.E.; Rehan, S.M. Tropical bee species abundance differs within a narrow elevational gradient. Sci. Rep. 2021, 11, 23368. [Google Scholar] [CrossRef]
  14. Hoiss, B.; Krauss, J.; Potts, S.G.; Roberts, S.; Steffan-Dewenter, I. Altitude Acts as an Environmental Filter on Phylogenetic Composition, Traits and Diversity in Bee Communities. Proc. R. Soc. B 2012, 279, 4447–4456. [Google Scholar] [CrossRef] [PubMed]
  15. Perillo, L.N.; Neves, F.D.S.; Antonini, Y.; Martins, R.P. Compositional changes in bee and wasp communities along Neotropical mountain altitudinal gradient. PLoS ONE 2017, 12, e0182054. [Google Scholar] [CrossRef] [PubMed]
  16. Osorio-Canadas, S.; Flores-Hernández, N.; Sánchez-Ortiz, T.; Valiente-Banuet, A. Changes in the structure and composition of the ‘Mexical’ scrubland bee community along an elevational gradient. PLoS ONE 2021, 16, e0254072. [Google Scholar] [CrossRef] [PubMed]
  17. Perillo, L.N.; Castro, F.S.D.; Solar, R.; Neves, F.D.S. Disentangling the effects of latitudinal and elevational gradients on bee, wasp, and ant diversity in an ancient neotropical mountain range. J. Biogeogr. 2021, 48, 1564–1578. [Google Scholar] [CrossRef]
  18. Classen, A.; Steffan-Dewenter, I.; Kindeketa, W.J.; Peters, M.K. Integrating intraspecific variation in community ecology unifies theories on body size shifts along climatic gradients. Funct. Ecol. 2017, 31, 768–777. [Google Scholar] [CrossRef]
  19. Arnold, S.E.; Savolainen, V.; Chittka, L. Flower colours along an alpine altitude gradient, seen through the eyes of fly and bee pollinators. Arthropod-Plant Interact. 2009, 3, 27–43. [Google Scholar] [CrossRef]
  20. Sponsler, D.B.; Requier, F.; Kallnik, K.; Classen, A.; Maihoff, F.; Sieger, J.; Steffan-Dewenter, I. Contrasting patterns of richness, abundance, and turnover in mountain bumble bees and their floral hosts. Ecology 2022, 103, e3712. [Google Scholar] [CrossRef] [PubMed]
  21. Ayala, R.; Griswold, T.L.; Yanega, D. Apoidea (Hymenoptera). In Biodiversidad, Taxonomía, y Biogeografía de Artrópodos de México: Hacia una Síntesis de su Conocimiento; Llorente, J., García, A., González, E., Eds.; UNAM-CONABIO: Ciudad de México, Mexico, 1996; pp. 423–464. [Google Scholar]
  22. Escobedo Escobedo-Kenefic, N.; Landaverde-González, P.; Theodorou, P.; Cardona, E.; Dardón, M.J.; Martínez, O.; Domínguez, C.A. Disentangling the effects of local resources, landscape heterogeneity and climatic seasonality on bee diversity and plant-pollinator networks in tropical highlands. Oecologia 2020, 194, 333–344. [Google Scholar] [CrossRef]
  23. Vizentin Vizentin-Bugoni, J.; Maruyama, P.K.; de Souza, C.S.; Ollerton, J.; Rech, A.R.; Sazima, M. Plant-pollinator networks in the tropics: A review. In Ecological Networks in the Tropics: An Integrative Overview of Species Interactions from Some of the Most Species-Rich Habitats on Earth; Dáttilo, W., Rico-Gray, V., Eds.; Springer: Cham, Switzerland, 2018; pp. 73–91. [Google Scholar] [CrossRef]
  24. Dalmazzo, M. Diversidad y aspectos biológicos de abejas silvestres de un ambiente urbano y otro natural de la región central de Santa Fe, Argentina. Rev. Soc. Entomol. Argent. 2010, 69, 33–44. [Google Scholar]
  25. Ayala, R. Fauna de abejas silvestres (Hymenoptera: Apoidea). In Artrópodos de Chamela; García, A.N., Ayala, R., Eds.; UNAM: Ciudad de México, Mexico, 2004; pp. 193–219. [Google Scholar]
  26. Trejo, I.; Dirzo, R. Deforestation of seasonally dry tropical forest: A national and local analysis in Mexico. Biol. Conserv. 2000, 94, 133–142. [Google Scholar] [CrossRef]
  27. Galicia, L.; Zarco-Arista, A.E. Multiple ecosystem services, possible trade-offs and synergies in a temperate forest ecosystem in Mexico: A review. Int. J. Biodivers. Sci. Ecosyst. Serv. Manag. 2014, 5, 275–288. [Google Scholar] [CrossRef]
  28. Hill, R.; Nates-Parra, G.; Quezada-Euán, J.J.G.; Buchori, D.; LeBuhn, G.; Maués, M.M.; Roué, M. Biocultural approaches to pollinator conservation. Nat. Sustain. 2019, 2, 214–222. [Google Scholar] [CrossRef]
  29. Villavicencio, R.; Ávila, C.R. Mapa de uso de Suelo y Vegetación y Zona de Influencia del Área Natural Protegida Sierra de Quila; Final Technical Report; Universidad de Guadalajara: Guadalajara, Mexico, 2015. [Google Scholar]
  30. Potts, S.G.; Vulliamy, B.; Dafni, A.; Ne’eman, G.; Willmer, P. Linking bees and flowers: How do floral communities structure pollinator communities? Ecology 2003, 84, 2628–2642. [Google Scholar] [CrossRef]
  31. Michener, C.D.; McGinley, R.J.; Danforth, B.N. The Bee Genera of North and Central America (Hymenoptera: Apoidea); Smithsonian Institution Press: Washington, DC, USA, 1994; pp. 1–208. [Google Scholar]
  32. Chao, A.; Jost, L. Coverage-based rarefaction and extrapolation: Standardizing samples by completeness rather than size. Ecology 2012, 93, 2533–2547. [Google Scholar] [CrossRef] [PubMed]
  33. Hsieh, T.C.; Ma, K.H.; Chao, A. iNEXT: Interpolation and Extrapolation for Species Diversity. R package, Version 2.0.5. Available online: https://github.com/JohnsonHsieh (accessed on 14 July 2023).
  34. Baselga, A. Partitioning the turnover and nestedness components of beta diversity. Glob. Ecol. Biogeogr. 2010, 19, 134–143. [Google Scholar] [CrossRef]
  35. Oksanen, J.; Blanchet, F.G.; Friendly, M.; Kindt, R.; Legendre, P.; McGlinn, D.; Minchin, P.R.; O’Hara, R.B.; Simpson, G.L.; Solymos, P.; et al. Vegan: Community Ecology Package. R Package Version 2.5-7. 2020. Available online: https://CRAN.R-project.org/package=vegan (accessed on 14 July 2023).
  36. Dormann, C.F.; Gruber, B.; Freund, J. Introducing the bipartite Package: Analyzing Ecological Networks. Interaction 2008, 8, 8–11. [Google Scholar]
  37. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2021; Available online: https://www.R-project.org/ (accessed on 14 July 2024).
  38. Jordano, P. Patterns of mutualistic interactions in pollination and seed dispersal: Connectance, dependence asymmetries, and coevolution. Am. Nat. 1987, 129, 657–677. [Google Scholar] [CrossRef]
  39. Rodríguez-Gironés, M.A.; Santamaría, L. A new algorithm to calculate the nestedness temperature of presence-absence matrices. J. Biogeogr. 2006, 33, 924–935. [Google Scholar] [CrossRef]
  40. Blüthgen, N.; Menzel, F.; Hovestadt, T.; Fiala, B.; Blüthgen, N. Specialization, constraints, and conflicting interests in mutualistic networks. Curr. Biol. 2007, 17, 1–6. [Google Scholar] [CrossRef] [PubMed]
  41. Novotny, V. Beta diversity of plant-insect food webs in tropical forests: A conceptual framework. Insect Conserv. Divers. 2009, 2, 5–9. [Google Scholar] [CrossRef]
  42. Poisot, T.; Canard, E.; Mouillot, D.; Mouquet, N.; Gravel, D.; Jordan, F. The dissimilarity of species interaction networks. Ecol. Lett. 2012, 15, 1353–1361. [Google Scholar] [CrossRef] [PubMed]
  43. Michener, C.D. The Bees of the World, 1st ed.; Johns Hopkins University Press: Baltimore, MD, USA, 2000; pp. 1–830. [Google Scholar]
  44. Potts, S.G.; Vulliamy, B.; Dafni, A.; Ne’eman, G.; O’Toole, C.; Roberts, S.; Willmer, P. Response of plant-pollinator communities to fire: Changes in diversity, abundance and floral reward structure. Oikos 2003, 101, 103–112. [Google Scholar] [CrossRef]
  45. Ayala, R. Abejas silvestres (Hymenoptera: Apoidea) de Chamela, Jalisco, México. Folia Entomol. Mex. 1988, 73, 395–493. [Google Scholar]
  46. Hinojosa, I.A.D. Distribución Altitudinal de las Abejas Silvestres (Hymenoptera: Apoidea) en el Declive sur de la Sierra de Chichinautzin. Morelos. Master’s Thesis, Universidad Nacional Autónoma de México, Ciudad de México, Mexico, 2021. [Google Scholar]
  47. Novelo-Rincón, L.F.; Delfín-González, H.; Ayala, B.R.; Contreras-Acosta, H. Estructura de las comunidades de abejas nativas de cuatro tipos de vegetación en el estado de Yucatán, México. Folia Entomol. Mex. 2003, 42, 177–190. [Google Scholar]
  48. Ramírez, F.L. Abejas Nativas (Hymenoptera: Apoidea: Anthophila) Asociadas a la Vegetación de Nuevo León, México. Bachelor’s Thesis, Universidad Autónoma de Nuevo León, Monterrey, Mexico, 2012. [Google Scholar]
  49. Vandame, R. Diversidad de Abejas (Hymenoptera: Apoidea) de la Reserva de la Biosfera El Triunfo, Chiapas; Final Technical Report. SNIB-CONABIO; El Colegio de la Frontera del Sur, Unidad Tapachula: Tapachula, Mexico, 2012; pp. 1–80. [Google Scholar]
  50. Vergara, H.C.; Ayala, R. Diversity, phenology and biogeography of the bees (Hymenoptera: Apoidea) of Zapotitlán de Salinas, Puebla, México. J. Kansas Entomol. Soc. 2002, 75, 16–30. [Google Scholar]
  51. Smith-Pardo, A.; González, V.H. Diversidad de abejas (Hymenoptera: Apoidea) en estados sucesionales del bosque húmedo tropical. Acta Biol. Col. 2007, 12, 43–56. [Google Scholar]
  52. Fierros-López, H.E. Abejas silvestres (Hymenoptera: Apoidea) del Volcán de Tequila, Jalisco, México. Folia Entomol. Mex. 1998, 4, 21–70. [Google Scholar]
  53. Chang-Martínez, L.; Domínguez-Vázquez, G. Distribución altitudinal del polen en un gradiente altitudinal en Michoacán, México. Rev. Mex. Biodivers. 2013, 84, 876–883. [Google Scholar] [CrossRef]
  54. Baumann, K.; Keune, J.; Wolters, V.; Jauker, F. Distribution and pollination services of wild bees and hoverflies along an altitudinal gradient in mountain hay meadows. Ecol. Evol. 2021, 11, 11345–11351. [Google Scholar] [CrossRef]
  55. Roubik, D.W. Ecology and Natural History of Tropical Bees; Cambridge University Press: Cambridge, UK, 1989; pp. 1–514. [Google Scholar]
  56. Domínguez-Álvarez, A.; Cano-Santana, Z.; Ayala-Barajas, R. Estructura y fenología de la comunidad de abejas nativas (Hymenoptera: Apoidea). Div. Hábitats Ecol. Comunidades 2009, 2, 421–432. [Google Scholar]
  57. Lara-Romero, C.; Seguí, J.; Pérez-Delgado, A.; Nogales, M.; Traveset, A. Beta diversity and specialization in plant–pollinator networks along an elevational gradient. J. Biogeogr. 2019, 46, 1598–1610. [Google Scholar] [CrossRef]
  58. Minachilis, K.; Kantsa, A.; Devalez, J.; Vujic, A.; Pauly, A.; Petanidou, T. High species turnover and unique plant–pollinator interactions make a hyperdiverse mountain. J. Anim. Ecol. 2023, 92, 1001–1015. [Google Scholar] [CrossRef] [PubMed]
  59. Tonial, M.L.S.; Silva, H.L.R.; Tonial, I.J.; Costa, M.C.D.; Silva Júnior, N.J.D.; Diniz-Filho, J.A.F. Geographical patterns and partition of turnover and richness components of beta-diversity in faunas from Tocantins river valley. Braz. J. Biol. 2012, 72, 497–504. [Google Scholar] [CrossRef]
  60. Cristóbal-Perez, E.J.; Barrantes, G.; Cascante-Marín, A.; Hanson, P.; Picado, B.; Gamboa-Barrantes, N.; Rojas-Malavasi, G.; Zumbado, M.A.; Madrigal-Brenes, R.; Martén-Rodríguez, S.; et al. Elevational and seasonal patterns of plant-pollinator networks in two highland tropical ecosystems in Costa Rica. PLoS ONE 2024, 19, e0295258. [Google Scholar] [CrossRef]
  61. Cortés-Flores, J.; Lopezaraiza-Mikel, M.; de Santiago-Hernández, M.H.; Martén-Rodríguez, S.; Cristóbal-Pérez, E.J.; Aguilar-Aguilar, M.J.; Quesada, M. Successional and phenological effects on plant-floral visitor interaction networks of a tropical dry forest. J. Ecol. 2023, 111, 927–942. [Google Scholar] [CrossRef]
  62. Williams, N.; Crone, E.; Roulston, T.; Minckley, R.; Packer, L.; Potts, S. Ecological and life-history traits predict bee species responses to environmental disturbances. Biol. Conserv. 2010, 143, 2280–2291. [Google Scholar] [CrossRef]
  63. Adedoja, O.; Kehinde, T. Changes in interaction network topology and species composition of flower-visiting insects across three land use types. Afr. J. Ecol. 2018, 56, 964–971. [Google Scholar] [CrossRef]
  64. Beltrán, R.; Traveset, A. Redes de interacción entre flores e himenópteros en dos comunidades costeras: Efectos de la pérdida de hábitat. Rev. Ecosistemas 2017, 27, 102–114. [Google Scholar] [CrossRef]
  65. Jauker, F.; Jauker, B.; Grass, I.; Steffan-Dewenter, I.; Wolters, V. Partitioning wild bee and hoverfly contributions to plant–pollinator network structure in fragmented habitats. Ecology 2018, 100, e02569. [Google Scholar] [CrossRef]
  66. Walker, B.H. Biodiversity and ecological redundancy. Conserv. Biol. 1992, 6, 18–23. [Google Scholar] [CrossRef]
  67. Hooper, D.U.; Chapin III, F.S.; Ewel, J.J.; Hector, A.; Inchausti, P.; Lavorel, S.; Lawton, J.H.; Lodge, D.M.; Loreau, M.; Naeem, S.; et al. Effects of Biodiversity on Ecosystem Functioning: A Consensus of Current Knowledge. Ecol. Monogr. 2005, 75, 3–35. [Google Scholar] [CrossRef]
  68. Baldock, K.C.; Memmott, J.; Ruiz-Guajardo, J.C.; Roze, D.; Stone, G.N. Daily temporal structure in African savanna flower visitation networks and consequences for network sampling. Ecology 2011, 92, 687–698. [Google Scholar] [CrossRef]
  69. Valido, A.; Rodríguez-Rodríguez, M.C.; Jordano, P. Impacto de la introducción de la abeja doméstica (Apis mellifera, Apidae) en el Parque Nacional del Teide (Tenerife, Islas Canarias). Ecosistemas 2014, 23, 58–66. [Google Scholar] [CrossRef]
  70. Quesada, M.; Rosas, F.; Lópezaraiza, M.; Aguilar, R.; Ashworth, L.; Rosas, G.V.; Sánchez, M.G.; Martén, R.S. Ecología y Conservación Biológica de Sistemas de Polinización de Plantas Tropicales. In Ecología y Evolución de las Interacciones Bióticas; del Val, E., Bouge, K., Eds.; Fondo de Cultura Económica; CIECO y UNAM: Ciudad de México, Mexico, 2012; pp. 75–100. [Google Scholar]
  71. Tylianakis, J.M.; Laliberté, E.; Nielsen, A.; Bascompte, J. Conservation of species interaction networks. Biol. Conserv. 2010, 143, 2270–2279. [Google Scholar] [CrossRef]
  72. Calizza, E.; Costantini, M.L.; Rossi, L. Effect of multiple disturbances on food web vulnerability to biodiversity loss in detritus-based systems. Ecosphere 2015, 6, 1–20. [Google Scholar] [CrossRef]
  73. Dune, J.A.; Williams, R.J.; Martínez, N.D. Network Topology and Species Loss in Food Webs: Robustness Increases with Connectance. Ecol. Lett. 2002, 5, 558–567. [Google Scholar] [CrossRef]
  74. Bascompte, J.; Jordano, P. Redes mutualistas de especies. Investig. Cienc. 2008, 384, 50–59. [Google Scholar]
  75. Kratochwil, A.; Beil, M.; Schwabe, A. Complex structure of pollinator–plant interaction webs: Random, nested, with gradients or modules? Apidologie 2009, 40, 634–650. [Google Scholar] [CrossRef]
  76. Bascompte, J.; Jordano, P. The structure of plant-animal mutualistic networks. In Ecological Networks; Pascual, M., Dunne, J.A., Eds.; Oxford University Press: New York, NY, USA, 2006; pp. 143–162. [Google Scholar]
  77. Lara-Rodríguez, N.Z.; Díaz-Valenzuela, R.; Martínez-García, V.; Mauricio-Lopéz, E.; Anaid-Díaz, S.; Valle, O.I.; Fisher-de León, A.; Lara, C.; Ortiz-Pulido, R. Redes de interacción colibrí-planta del centro-este de México. Rev. Mex. Biodivers. 2012, 83, 569–577. [Google Scholar] [CrossRef]
  78. Ashton, I.W.; Miller, A.E.; Bowman, W.D.; Suding, K.N. Niche complementarity due to plasticity in resource use: Plant partitioning of chemical N forms. Ecology 2010, 91, 3252–3260. [Google Scholar] [CrossRef] [PubMed]
  79. Carvalho, D.M.; Presley, S.J.; Santos, G.M.M. Niche overlap and network specialization of flower-visiting bees in an agricultural system. Neotrop. Entomol. 2014, 43, 489–499. [Google Scholar] [CrossRef] [PubMed]
Insects 15 01009 g001
Figure 1. Location of the APFFSQ (Sierra de Quila Flora and Fauna Protection Area) and sampling sites (SDTF—seasonally dry tropical forest, TF—temperate forest).
Figure 1. Location of the APFFSQ (Sierra de Quila Flora and Fauna Protection Area) and sampling sites (SDTF—seasonally dry tropical forest, TF—temperate forest).
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Figure 2. Coverage—based rarefaction (solid line) and extrapolation (dashed line) plots with 95% confidence intervals (shaded areas) comparing (richness, q0), common species (q1), and dominant species (q2) on community bees between vegetation types (SDTF—seasonally dry tropical forest, TF—temperate forest).
Figure 2. Coverage—based rarefaction (solid line) and extrapolation (dashed line) plots with 95% confidence intervals (shaded areas) comparing (richness, q0), common species (q1), and dominant species (q2) on community bees between vegetation types (SDTF—seasonally dry tropical forest, TF—temperate forest).
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Figure 3. Bee plant interactions network (a) in SDTF1 and (b) SDTF2 of Sierra de Quila. Blue lines correspond to Apidae family, red lines to Megachilidae family, yellow lines to Halictidae, green lines to Colletidae, and orange lines to Andrenidae. (SDTF—seasonally dry tropical forest).
Figure 3. Bee plant interactions network (a) in SDTF1 and (b) SDTF2 of Sierra de Quila. Blue lines correspond to Apidae family, red lines to Megachilidae family, yellow lines to Halictidae, green lines to Colletidae, and orange lines to Andrenidae. (SDTF—seasonally dry tropical forest).
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Figure 4. Bee–plant interactions network (a) in TF1 and (b) TF2 of Sierra de Quila. Blue lines correspond to Apidae family, red lines to Megachilidae family, yellow lines to Halictidae, green lines to Colletidae, and orange lines to Andrenidae (TF—temperate forest).
Figure 4. Bee–plant interactions network (a) in TF1 and (b) TF2 of Sierra de Quila. Blue lines correspond to Apidae family, red lines to Megachilidae family, yellow lines to Halictidae, green lines to Colletidae, and orange lines to Andrenidae (TF—temperate forest).
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Table 1. β diversity of bees, plants, and interactions of networks in two types of vegetation.
Table 1. β diversity of bees, plants, and interactions of networks in two types of vegetation.
Bees βSor βSim βSne
SDTF1SDTF2TF1SDTF1SDTF2TF1SDTF1SDTF2TF1
SDTF20.4285 0.398 0.030
TF10.7310.634 0.560.44 0.1720.194
TF20.7240.6560.6720.600.5330.640.1240.1230.032
Plants
SDTF20.72 0.641 0.079
TF10.7660.583 0.5510.428 0.2150.155
TF20.8440.7940.7740.5690.5170.6120.2750.2770.162
βWN βST βOS
SDTF1SDTF2TF1SDTF1SDTF2TF1SDTF1SDTF2TF1
SDTF20.914 0.705 0.209
TF10.9640.943 0.8450.778 0.1190.165
TF20.9480.9390.9570.8810.8480.8710.0660.0910.08
(SDTF—seasonally dry tropical forest, TF—temperate forest). βSor—diversity that describes the changes in species composition between communities. βSim—diversity that quantifies the replacement of species between communities. βSne—diversity that quantifies species loss between communities. βWN—diversity of interactions. βST—diversity of interactions due to species turnover. βOS—diversity of interactions established between species common to both realizations.
Table 2. Comparison of network descriptors among different vegetation types in APFFSQ. (Comparison with confidence interval on same number of sampling units, * statistically significative < 0.05, ** statistically significative < 0.01).
Table 2. Comparison of network descriptors among different vegetation types in APFFSQ. (Comparison with confidence interval on same number of sampling units, * statistically significative < 0.05, ** statistically significative < 0.01).
Network DescriptorSDTF1SDTF2TF1TF2
Observed plant richness
Estimated plant richness (CI 0.95)		61
62 (51–73)		39
39 (31–49)		34
39 (30–45)		29
29 (21–39)
Observed bee richness
Estimated bee richness (CI 0.95)		113
108 (98–120)		101
101 (88–109)		49
53 (45–61)		58
50 (51–64)
Observed interactions richness
Estimated interactions richness (CI 0.95)		248
233 (211–255)		201
201 (172–224)		88
101 (83–120)		108
108 (91–122)
Connectance0.0350.050.050.06
Links per species1.41.41.061.13
Nestedness3.36 **5.41 **4.6 *4.58 **
Web asymmetry0.310.440.180.33
Niche overlap bees0.0740.0830.0910.145
Niche overlap plants0.030.040.0610.057
APFFSQ—Sierra de Quila Flora and Fauna Protection Area, SDTF—seasonally dry tropical forest, TF—temperate forest.
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Razo-León, A.E.; Muñoz-Urias, A.; Uribe-Mú, C.A.; Huerta-Martínez, F.M.; Fierros-López, H.E.; Vásquez-Bolaños, M.; Moya-Raygoza, G.; Carrillo-Reyes, P. Wild Bee Diversity and Bee–Plant Interactions in Tropical and Temperate Forest Clearings in a Natural Protected Area in Central West Mexico. Insects 2024, 15, 1009. https://doi.org/10.3390/insects15121009

AMA Style

Razo-León AE, Muñoz-Urias A, Uribe-Mú CA, Huerta-Martínez FM, Fierros-López HE, Vásquez-Bolaños M, Moya-Raygoza G, Carrillo-Reyes P. Wild Bee Diversity and Bee–Plant Interactions in Tropical and Temperate Forest Clearings in a Natural Protected Area in Central West Mexico. Insects. 2024; 15(12):1009. https://doi.org/10.3390/insects15121009

Chicago/Turabian Style

Razo-León, Alvaro Edwin, Alejandro Muñoz-Urias, Claudia Aurora Uribe-Mú, Francisco Martín Huerta-Martínez, Hugo Eduardo Fierros-López, Miguel Vásquez-Bolaños, Gustavo Moya-Raygoza, and Pablo Carrillo-Reyes. 2024. "Wild Bee Diversity and Bee–Plant Interactions in Tropical and Temperate Forest Clearings in a Natural Protected Area in Central West Mexico" Insects 15, no. 12: 1009. https://doi.org/10.3390/insects15121009

APA Style

Razo-León, A. E., Muñoz-Urias, A., Uribe-Mú, C. A., Huerta-Martínez, F. M., Fierros-López, H. E., Vásquez-Bolaños, M., Moya-Raygoza, G., & Carrillo-Reyes, P. (2024). Wild Bee Diversity and Bee–Plant Interactions in Tropical and Temperate Forest Clearings in a Natural Protected Area in Central West Mexico. Insects, 15(12), 1009. https://doi.org/10.3390/insects15121009

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