Bee communities were studied with three different conditions of land-use: 1) urban area; 2) crops and livestock; and, 3) preserved vegetation. All three conditions have elements of tropical dry forest and are in the "Sierra de Quila" Flora and Fauna Protection Area and its influence zone. Sampling was carried out throughout the year (three days per month) for each land-use condition. Bee species and their abundance were registered with the intention of knowing how changes in the vegetation are related to bee community structure (richness, abundance, and α and β diversity).

A total of 14,054 individuals from 160 species were registered. A rarefaction analysis, showed that the preserved areas had significantly greater richness and diversity. Beta diversity analysis revealed a species turnover of nearly 32% among each pair of conditions. It is concluded that the changes in land-use negatively affect richness and diversity and causes major changes in species composition of the bee community. For this reason, it is recommended that the protection of the tropical dry forest, both for this study area but also in general for Mexico, is essential to guarantee the conservation of this group of insects, which are required for the reproduction of a great number wild and cultivated plant specie.

Native bees, Mexico, tropical dry forest, bee abundance, bee diversity

Pollinators are a key component for global biodiversity, because they assist in the sexual reproduction of many plant species and play a crucial role in maintaining terrestrial ecosystems and food security for human beings (Potts et al. 2010, van der Sluijs and Vaage 2016). Approximately 80% of angiosperms depend on biotic pollination (Klein et al. 2007, Quesada et al. 2012). Bees (Hymenoptera: Apoidea) are some of the most important pollinators (Winfree et al. 2008). It is estimated that nearly 73% of cultivated plant species and more than 75% of global vegetation are pollinated by these insects (Coro 2009), which are considered the principal pollinators in tropical regions (O’Toole and Raw 1999, Nantes-Parra 2005).

Tropical dry forest present a great bee species richness in Mexico (Ayala 1988, Ayala et al. 1996), which is explained by the high diversity of entomophilous plants (Ayala 2004), and their differentiated phenology (generally, tree species flowering in dry season while herbaceous and shrub species flowering in wet season), which provides to this group of organisms, resources for most of the year (Reyes-Novelo et al. 2009). This vegetation type covered approximately 270,000 km² in 1990 but currently there are great pressures exerted on this type of forest. For example Trejo and Dirzo (2000), reported that 50% was either fragmented or existed as relicts. Furthermore, they found changes in land use on 23% of the surface and that only 27% of this type of vegetation remained intact (Trejo and Dirzo 2000).

Land use change, such as degradation or fragmentation of tropical dry forest, could have consequences on the richness and composition of bee communities. According to previous studies, bees are susceptible to the loss of their natural habitats by the fragmentation and transformation of the landscape for agricultural, livestock and urban purposes (Martins et al. 2013, Woodcock et al. 2013, Le Féon et al. 2016, Mogren et al. 2016). For this reason, it is important to compare local bee communities from disturbed environments with one from a preserved environment in the same region, as this should provide useful information for making conservation-based decisions on bee community management (Dalmazzo 2010).

Two of the most important factors for bee communities are food availability (nectar and pollen) and nesting sites (Reyes-Novelo et al. 2009). Changes in land use are expected to affect both and consequently alter the structure of these communities. Due to this, the aims of this study were: 1) to ascertain whether landscape transformations affect bee community structure (richness, abundance, and α and β diversity) and, 2) to identify which are the bee groups most susceptible to these changes, as well as those who benefit from them.

The highest bee richness was registered in P while the only significant differences were recorded between U and P. The results indicate a gradient in richness related to the habitat conservation. This finding is supported by different studies which show that the destruction of the habitat, for agriculture or urbanization, is principally responsible for bee species reduction, up to the point of local extinction for some species (Frankie et al. 1997, Martins et al. 2013). Furthermore, in a meta-analysis, Winfree et al. (2009) , report that bee richness decreases with increasing anthropogenic disturbance, while Ricketts et al. (2008), found that on average the richness of pollinators (principally bees) in crops decreased by half as the distance from preserved habitat increased to 1500 m.

The decrease in bee richness is related to their dependence on various resources to complete their lifecycle, such as food resources (pollen and nectar) and nesting substrates (either from the soil or vegetation), and materials for constructing their nests (Winfree 2010). The reason that a greater number of bee species is registered in the preserved area is possibly due to a greater availability of plant species for food, being that bee richness has been positively related to the richness of flowers (Carper et al. 2014) and to a great floral diversity, which provide food to a great variety of specialist and generalist bee species (Martins et al. 2013).

The abundance of bees did not differ significantly between the three land-use conditions. This agrees with various studies that report a similar or greater abundance in human modified areas (Carper et al. 2014, Mallinger et al. 2016, Nantes-Parra et al. 2008, Olalde-Estrada et al. 2015, Otero and Sandino 2003, Tonhasca et al. 2002); this occurs in sites with moderate disturbance with gaps on forest canopy, which facilitate grow of herbaceous layer (Carper et al. 2014). This also shows that urban areas could be important for bee communities, despite the modification of vegetation, because they offer ornamental and wild flowers, particularly because they are watering them in times when native vegetation is diminished, as well as nesting resources associated to human constructions (Dalmazzo 2010). The differences in abundance between the P and CL when Apis mellifera is excluded from analysis could be due to the same reasons that affect bee richness in addition to the use of pesticides in the crops which affect wild bees (Winfree 2010).

The number of individuals per family varied, Andrenidae, Megachilidae and Colletidae being far less abundant than the Apidae and Halictidae. Potts et al. (2003) found the Andrenidae positively associated with annual plant diversity, and Megachile with plant richness, pollen and available nectar. Vergara (2005) suggests that, in areas with agricultural activity, bee genera that nest in the soil, including andrenids and colletids, are under-represented due to plowing for agricultural activities and the presence of livestock, which affect nesting. While Halictidae presented greater abundance in the urban area, this is possibly because most of the registered bees of this family are small (<1 cm) and most of them are polilectic (Michener 2000).

Banaszak-Cibicka and Zmihorski (2012), reported that urban areas contain small green isolated island (parks and gardens), that promote the abundances of small bees, which require only a small amount of food. Winfree et al. (2009), indicate that they do not have problems in finding nesting sites in disturbed areas.

Total bee abundance tends to decline at disturbed sites, while individual species present different responses, some of them show drastic reduction in their populations, while others remain stable or even increase with land-use change (Winfree et al. 2008). For this reason, the use of the habitat according to bee species plays an important role. Bees that require specific conditions for their development, become the most vulnerable to the disappearance of their habitat. On the other hand, if the resources generated by the modification of the habitat is exploited by the bees, they could survive in disturbed areas (Winfree 2010). That is the reason why bees that can use a wide variety of resources are often able to compensate when circumstances change, although some species disappear due to land use changes. The higher richness and evenness patterns in preserved areas is supported by Reyes-Novelo et al. (2009), who explain that in disturbed areas some species disappear locally and the abundance of others decreases, which modifies dominance.

Finally, β diversity showed a medium level of species turnover rate among conditions, despite the maximum distance between sampling sites was 6 km. The structure of bee community contrasts with P and U, in which tribes such as Halictini and Anthophorini (due to the high abundance of Anthophora squammulosa) are associated with the urban area. The tribes of the Andrenidae, Colletidae, Megachilidae and Apidae, such as bumblebees (Bombini), are strongly associated with P, while the CL area is found at the mid-point of the gradient. This suggests that disturbance, with its variations in micro-environments and food and nesting resource has a significant effect on bee community species composition.

The bee fauna of the TDF in Mexico is one of the richest and most diverse in the country (Ayala 2004), so, the protection of this type of vegetation is crucial for the conservation of this group of insects, given that the reduction of these native pollinators could have a negative economic impact on crops (Maass et al. 2005). As the expansion of human settlement and the population growth or production activities have led to the process of deforestation, fragmentation and degradation of this forest (Maass et al. 2010), Trejo and Dirzo (2000) report that approximately 3.7% of the TDF of the total area of Mexico (72,850 km²) remains relatively intact and with a high annual deforestation rate of 2.02% of the total coverage.

The APFFSQ is an important site for maintaining wild bee diversity, given that 200 species of bees were registered in the area, of which 160 are present in the TDF (Razo-León 2015). According to Ortega, (2007), the TDF covered 19.84% of APFFSQ (2,797 ha) in 1993, by the year 2000, it only covered 15.25% (2,149 ha), this means that the TDF lost 23.2% of its area in seven years, because it is rounded by agricultural or livestock production areas which make it more vulnerable to transformation. This leads to the conclusion that change in land-use negatively affects the richness, abundance, and diversity of species of bee community, for this reason it is recommended that the TDF in Mexico should be protected in order to guarantee the conservation of this group of insects.

We thank anonymous reviewers for suggesting improvements to the manuscript. A doctoral scholarship from CONACYT, Hugo Eduardo Fierros-López (CUCBA, University of Guadalajara) for the identification of bees, Regional Committee for the Protection and Promotion of the Natural Resources of the Sierra de Quila A.C. for all its institutional and logistical support, Raymundo Villavicencio and Victoria Belen Muñoz for the preparation of the map.