Seasonal abundance and diversity of native bees in a patchy agricultural landscape in Southern Mexico

Agriculture, Ecosystems and Environment 292 (2020) 106807

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Seasonal abundance and diversity of native bees in a patchy agricultural landscape in Southern Mexico

T

Ruiz-Toledo Jovania, Vandame Rémyb, Penilla-Navarro Patriciac, Gómez Jaimea, Sánchez Daniela,* a

El Colegiodela Frontera Sur Unidad Tapachula, Carretera Antiguo Aeropuerto Km 2.5, CP 30700, Tapachula, Chiapas, Mexico El Colegiodela Frontera Sur Unidad San Cristóbal, Periférico Sur s/n, María Auxiliadora, CP 29290, San CristóbaldeLas Casas, Chiapas, Mexico c Centro RegionaldeInvestigación En Salud Pública, Instituto NacionaldeSalud Pública, LaboratoriodeResistencia a Insecticidas, 4a. Norte y 19 Calle Poniente S/N, CP, 30700, Tapachula, Chiapas, Mexico b

A R T I C LE I N FO

A B S T R A C T

Keywords: Agroecosystem Richness Agriculture Native bees

Diversity and abundance of native bees was measured in four sites of an agricultural landscape dominated by soybean crops in Southern Mexico. Bees were sampled from June 2014 to May 2015 using entomological nets along five 500 m long transects in each site. Two sites (S1 and S2) were fully anthropized (100% of urban and agricultural land use) and the two other sites (R1 and R2) were on average less anthropized with 27.5% of forest relicts. Overall, we collected 2115 specimens; the most abundant species were Augochlora (Oxystoglossella) aurifera (12.8%), Trigona fuscipennis (9.2%), and T. fulviventris (8.6%). The highest diversity was observed in June and July (rainy season), in sites S2 and S1. Site S2 had the greatest diversity and abundance (56 species, 885 individuals), followed by S1 (41 species, 577 individuals), R2 (38 species, 289 individuals) and R1 (25 species, 117 individuals). However, rarefaction analysis showed no significant difference among four sites. Compared to studies carried out in protected natural areas with similar climatic conditions, our results suggest that small-scale agriculture in southern Mexico apparently does not affect detrimentally pollinator populations as expected. Thus, this study suggest that the presence of preserved patches contributes to the richness and abundance of bees, due to the maintenance of wild flowers and ruderal plants in patches next to the crop fields, providing a continuous source of pollen, nectar and shelters. Nonetheless, further studies are necessary to examine the connections between the different elements in the agricultural landscape and to understand in depth the response of the pollinator communities.

1. Introduction Bees (Hymenoptera, Apoidea) are insects that contribute to the preservation of wild plant populations and crop productivity through pollination (Costanza et al., 1997; Klein et al., 2003; Potts et al., 2010). It has been estimated that more than 66% of the approximately 1500 species of crops in the world are pollinated by bees, and that 5–8 percent of current global crop production, with an annual market value of $235 billion-$577 billion, is directly attributable to animal pollination (Ferrier et al., 2016). Paradoxically, agriculture represents one of the main threats to these organisms as it causes changes in land use, habitat loss and fragmentation, introduction of exotic organisms and pesticide use (Garibaldi et al., 2011; Richards, 2001; Steffan-Dewenter et al., 2005), which not only affect bee richness but also the structure and

functioning of entire ecological communities (Saunders et al., 1991; Steffan-Dewenter, 2002). Thus bees are restricted to search for food, but mainly refuge, in habitats around croplands, which function as dispersion corridors, providing the necessary resources for their survival (Ockinger and Smith, 2007; Stoate et al., 2001; Tilman et al., 2001). However, such natural and semi-natural habitats seemingly do not provide sufficient resources to maintain bee populations, which is evidenced by a reduction in the pollination of agroecosystems due to a lowered capacity to allow wild vegetation to flourish (Williams et al., 1991). Therefore, the role that distinct elements in the agricultural landscape (like proportion of conserved, agricultural and urbanized lands, beekeeping, presence of rivers and industry) play in maintaining the abundance and diversity of pollinators might be very important. For example, it is known that natural and semi-natural habitats and organic

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Corresponding author. E-mail addresses: [email protected] (J. Ruiz-Toledo), [email protected] (R. Vandame), [email protected] (P. Penilla-Navarro), [email protected] (J. Gómez), [email protected] (D. Sánchez). https://doi.org/10.1016/j.agee.2019.106807 Received 21 June 2019; Received in revised form 17 December 2019; Accepted 20 December 2019 0167-8809/ © 2019 Published by Elsevier B.V.

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associated with flower diversity (Roulston and Goodell, 2011), habitats with high floristic diversity are expected to provide better pollination services to adjacent croplands (Garibaldi et al., 2011, 2016, 2013). Intensively managed agricultural landscapes, well-connected remnant patches of natural and semi-natural habitat may act as reservoirs of biodiversity (Geslin et al., 2016; Hendrickx et al., 2007; Hevia et al., 2013), and as important providers of several ecosystem services (Carvalheiro et al., 2011; Tscharntke et al., 2005). As central place foragers, wild social bees that build their colonies in these habitats may pollinate crops within their foraging range (Ricketts, 2004). Therefore, the spatial scale that affects agricultural production is determined by foraging distance (Greenleaf et al., 2007). In this study, we measured the diversity and abundance of native bees in an agricultural patchy landscape in which reduced spaces of conserved habitats, which might function as buffer zones for the bees, are found adjacent to croplands. We expected to find a higher diversity and abundance in those sites with higher proportion of conserved areas within the agricultural landscape.

cultivation of crops buffer the negative effects of intensive farming (Holzschuh et al., 2006; Kennedy et al., 2013). It has been shown that the diversification of agricultural practices can contribute to the ecological intensification of agriculture by providing multiple ecosystem services, promoting biological control of pests (Redlich et al., 2018; Wan et al., 2018a, 2018b), reducing the use of pesticides (Gurr et al., 2016; Tscharntke et al., 2005; Zhao et al., 2016), improving soil quality (Cassman, 1999) and improving crop yields (Gurr et al., 2016; Tittonell and Giller, 2013). The presence of refuges is thus important to maintain bee populations at acceptable levels that do not compromise crop productivity, wild plant and animal communities and ultimately the integrity of entire ecosystems. Studies at the agricultural landscape scale have reported that the improvement of the vegetation on the ground cover regulates insect populations. Green plants constitute the base of the food chain as primary producers since they are food for herbivores and provide shelter, overwintering sites and reproduction (e.g. oviposition) opportunities for many animal species. This implies that vegetation hosts the prey of secondary consumers (carnivores). Therefore, structure, composition and management of the vegetation in and around cropfields can be considered as important drivers of biodiversity in agricultural areas (Southwood and Way, 1970). Many authors have reviewed the importance of vegetation diversity for enhancing populations of beneficial arthropods in cropland (Delucchi, 1997; Landis and Marino, 1999). Roschewitz et al. (Roschewitz et al., 2005), Gardiner et al. (2009) and Wan et al. (2018a, 2018b) reported that vegetation diversity can provide support for insect biological control at the local and landscape levels. Weeds play an important role in enhancing the abundance and diversity of arthropod predators and serve as a source of increased diversity in agroecosystems. In most agroecosystems, weeds are ever-present biological components within and around fields, adding to the complexity of interacting trophic levels which mediate a number of crop insect interactions with major effects on final yields (Nicholls and Altieri, 2012). However, weeds are traditionally viewed as plants that reduce yields by competing with crops or by harboring pests and plant pathogens (Penagos et al., 2003). Increased diversity has been the rationale for enhancing biological control of arthropod pests through habitat management (Norris and Kogan, 2005). The same authors (Norris and Kogan, 2000) indicated that weed cover enhances the number and activity of spiders and ground beetles. In their research on dicotyledonous weeds, Wilson and Aebischer, 1995 reported that the density of most arthropod species decreased significantly as distance from crop edge increased from 0 to 128 m. Bárberi et al. (2010) have reviewed the importance of vegetation diversity for enhancing populations of beneficial arthropods in cropland. Wyss (1996); Simon et al. (2010) and Song et al. (2010) reported a positive effect of plant community diversification on beneficial arthropods in orchards. Non-crop habitats bordering agricultural fields in Europe have been found to have a favorable effect on a number of beneficial animals as spiders, ladybugs, and syrphids (Ernoult et al., 2013; Hillocks, 1998). Woodcock et al. (Woodcock et al., 2008) showed the positive effects of composition and diversity of plants around the field margins on ground beetle diversity. Fields with a dense weed cover and high diversity usually have more predaceous and parasitic arthropods than weed-free fields (Speight and Lawton, 1976). Croplands in the Soconusco region in Chiapas, Mexico, are mainly used to grow soybean, mango, bean, pumpkin, maize and sesame (authors’ observation) at small scale. Such areas are commonly found next to patches of conserved habitat and houses with back and front gardens, which also provide food and shelter to bees. Such a patchy landscape may be beneficial to the populations of these insects within the agroecosystem, and somehow buffer the negative effects of agricultural practices as proposed by some studies (Winfree et al., 2009). For example, Ricketts et al. (2008) mention that, in order to enhance and maintain the pollination service provided by arthropods, sufficient floral and nesting resources, as well as low pesticide input, are needed within agricultural landscapes. Because pollinator diversity is often

2. Materials and methods 2.1. Study area The study site is a quite homogeneous agricultural landscape out of the city of Tapachula, located in the Soconusco region in Chiapas, Mexico. The area is characterized by a humid and hot climate with heavy rain during the rainy season (mean annual precipitation: 2,653 mm; mean annual temperature: 26.5 °C (Centro Meteorológico Nacional, 2017). It is mainly composed by non-irrigated crops [maize (Zea mays), sorghum (Sorghum spp.), sesame (Sesamum indicum) and soybean (Glycine max)] cultivated under a rotation regime. Most of these are monocultures that occupy relatively large areas, and regarding to soybeans, an unknown proportion is resistant to herbicides, so it is common to use formulations based on glyphosate and various pesticides (organochlorine, organophosphorus and carbamate insecticides, fungicides chlorothalonil and mancozeb (Ruiz-Toledo et al., 2018, 2014)) and fertilizers. Applications are carried out twice per cultivation period (June-July or November-December). The dominant type of vegetation was perennial tropical forest composed of species such as Guadua angustifolia, Ipomoea purpurea, I. triloba, Solanum mayanum, Mimosa pudica, Melampodium divaricatum, Malvastrum coromandelianum, Acacia collinsii, Jatropha curcas, Tithonia rotundifolia¸ Castilla elastica, Guazuma ulmifolia, Gliricidia sepium and other species of tropical plants. However, maize, sorghum, sesame, soybean and mango crop and native and ruderal grasslands are currently the most abundant plant species in the study area. 2.2. Sampling design and data collection We selected four sampling sites (Fig. 1), two of them with less area devoted to agriculture [Sites R1 (14°45′19.20″N, 92°17′30.60″W) and R2 (14°45′5.08″N, 92°15′46.87″W)], and two with more area cultivated with soybean [Sites S1 (14°46′15.01″N, 92°17′57.50″W) and S2 (14°44′39.83″N, 92°18′35.43″W)] as shown in Table 1. Sampling sites were selected so that (a) they were separated from each other by at least 3 km, and (b) they were at least 1 km away from the soybean fields. The 1 km distance was chosen because most solitary bees appear to forage within a range of 500 m (Gathmann and Tscharntke, 2002; Zurbuchen et al., 2010). Anthropization percentages were calculated by analyzing satellite imagery from 2015 using ArcView GIS software v10.5. The image of each site was cropped in the shape of a circle with a radius of 500 m. Next, the digitization of the different land uses was carried out in each image, considering three categories: urban use (U), agricultural use (A) and conserved area (C). Finally, the agricultural and urban uses were added into a single value, the degree of anthropization (% U +% A, 2

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Fig. 1. Sampling sites.

area, and A. mellifera abundance responds more to management by beekeepers than to natural community processes. All specimens were identified to the highest taxonomic level possible and pin-mounted for storage in the Bee Collection of ECOSUR.

Table 1 Diversity/abundance parameters and land use proportion in the four sampling sites.

Number of species Estimated diversity Sampling completeness (%) Number of specimens Shannon Simpson %U %A %C %Anthropization (%U + %A)

R1

R2

S1

S2

25 48 52 117 2.60 0.88 2.05 80.86 16.97 82.92

38 64 59 289 2.76 0.91 0 62.07 36.49 62.07

56 70 80 885 2.44 0.85 10.54 89.45 0 100

41 57 72 577 2.35 0.81 0 100 0 100

2.4. Data analysis To avoid spatial and temporal autocorrelation, we summed the number of bees collected in the five transects in each site. Any difference in diversity (Simpson and Shannon indexes following Magurran (2004)) among sites was determined by comparing 95% confidence intervals using a bootstrap approach. To investigate any temporal difference among sites we pooled the data bimonthly (since in some months only one specimen was collected) and 95% confidence intervals were estimated. All analyses were performed using the EstimateS 9.1 software, which allows for the calculation of confidence intervals by utilizing the bootstrap procedure with 100 samples with replacement (Colwell, 2013). The degree of similarity was calculated by using the BiodiversityR package (Kindt and Coe, 2005) in R software (R Development Core Team, 2012), comparing the number of species per site and per month with the Jaccard index, from which dendrograms were derived. Finally, we used the RICH package v 1.01 in R for the estimation of accumulated average richness, which bases their calculations on a bootstrap algorithm that allows the estimation of 95% confidence intervals.

U = Urban, A = Agricultural, C = Conserved.

Table 1).

2.3. Bee sampling Collections were carried out from 07:00 to 12:00 h, once a month, from June 2014 to May 2015. Bee specimens were sampled using standard entomological nets along five linear transects, each one 500 m long and 5 m wide, in each site. Each transect was marked with a colored tape to unequivocally identify its location throughout the study. The order in which each transect was surveyed was randomized in each visit to reduce bias for time of the day during sampling. We standardized sampling effort by carefully establishing the time devoted to each site (60 min) and the number of times (4 times) the net (40 cm in diameter) was swept per meter on all flowering plants. This procedure has been shown to be effective for sampling bees (Brosi et al., 2008). Immediately after capture, bees were sacrificed with ethyl acetate, and deposited in appropriately labeled bottles. Specimens of the honeybee, Apis mellifera, were collected but not considered for the data analysis because the focus of this study was on diversity and abundance of wild native bees. Beekeeping is a very common activity in the Soconusco

3. Results 3.1. Bee diversity Overall, 2115 specimens were collected, belonging to 5 families, 35 genera and 79 species. Apidae was the most speciose family with 33 species (1202 specimens), followed by Halictidae (23 species, 787 specimens), Megachilidae (17 species, 74 specimens), Colletidae (3 species, 14 specimens) and Andrenidae (3 species, 38 specimens). Regarding number of genera, 18 belonged to Apidae, eight to 3

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Fig. 2. Rarefaction curve of the bee community in the four sampling sites.

3.2. Bee abundance

Halictidae, four to Megachilidae, three to Andrenidae and one to Colletidae. Of the 35 genera identified, Megachile was the most diverse with 12 species. On the other hand, Halictus and Lasioglossum had four species each, while the genera Centris, Ceratina, Coelioxys, Colletes, Melissodes and Xylocopa consisted of three species each. Sites S1 and S2 had the highest diversity and abundance followed by R2 and R1 (Table 1). Shannon and Simpson indexes show that all four sites had a similar diversity (He and Hu, 2005; Morris et al., 2014; Simpson, 1949), although R1 and R2 had the highest values (Table 1, Fig. 2). Site S2 showed the greatest diversity, and was higher than at sites S1, R2 and R1. However, no significant difference was found among sites (p = 0.16). A general pattern in diversity change over the study period can be described as follows: an increase during May and June at all sites, and a steady decrease from November to February (Fig. 3).

In site R1 we collected 117 specimens, the lowest number among the four sites (Fig. 4), followed by R2 (289 specimens), S2 (577 specimens) and S1 (885 specimens). However, according to the accumulation curves, the completeness of the sampling was lower in the R sites (< 60%, Table 1). Of the total number of bees, 54.9% were Halictidae, 33.7% Apidae, 6.5% Megachilidae, 3.3% Andrenidae, and 1.2% Colletidae. The three most abundant non-social species were Au. (Oxystoglossella) aurifera with 272 specimens, Lasioglossum (Dialictus) sp. with 140 and Exomalopsis (Exomalopsis) similis with 108, while the most abundant eusocial species were T. fuscipennis (195 specimens) and T. fulviventris (183 specimens). The analysis of the similarity index by site (Fig. 5) and the estimation of differences through confidence intervals show that R1 and R2 were highly similar in abundance and richness: site S2 had the highest abundance and richness recorded in the study, perhaps due to its larger

Fig. 3. Temporal variation in bee richness (mean ± 95% CI) during the study period. Confidence intervals were estimated using a bootstrap approach. 4

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sample size. The similarity index by month (Fig. 6) shows a clear separation between the dry and the rainy seasons, and thus the importance of climate in bee community changes. 4. Discussion The aim of this study was to investigate the temporal abundance and diversity of native bees in an agricultural landscape dominated by soybean in which some patches of conserved natural habitats can be found. Our results indicate that native bees are abundant in our study site, though samplings in truly conserved areas in the region should be made to compare the impact of agriculture. Given the variety of sizes, morphologies and behaviors, the native bee species that we found can pollinate a greater range of plant species than by A. mellifera alone (Garibaldi et al., 2013; Klein et al., 2007), thus their importance should not be underestimated in our study region. Our results do not differ in the number of bees collected in smallscale agricultural landscapes in other studies (Brosi et al., 2008, 2007; Liow et al., 2001; Smith-Pardo and González, 2007) despite the potential impacts that the use of herbicides could have on plants that are used as shelter or food (Brower et al., 2012). A similar bee diversity and richness was found in all four sampling sites. The greatest wealth and abundance was observed at sites S1 and S2, which had no conserved patches; in addition, 78% of the specimens collected came from these sites, so the contribution of sites R1 and R2 was quite low, even though they had adjacent preserved patches. However, the completeness of the sampling was lower in the R sites (< 60%) compared to the S sites (> 70), so it is expected that when completing 100% sampling, the sites would have similar species richness (Table 1). Such data contrast with those reported by Morandin and Winston (2005), who detected lower bee richness and a consequent deficit of pollination in transgenic canola crops compared to conventional and organic crops. O´Brien (2018) also reported that on sites cultivated with resistant herbicide canola, seminatural habitats around agricultural fields, which contained non-cultivated flowering plants, were eliminated. In fact, abundance and diversity of bee species in natural ecosystems and in agroecosystems based on organic farming practices are larger than in other agricultural ecosystems, seemingly because they provide the resources needed for their survival (Banaszak, 1996; Calabuig, 2000; Holzschuh et al., 2006; Potts et al., 2003). However, the 27.5% of forest in the R sites seemingly do not compensate for the loss of conserved areas in the S sites. By incorporating samplings from Protected Areas we could measure the effect of agriculture on bee populations and thus determine whether our findings reflect an increase or a decrease in abundance and diversity. Additionally, a temporal and landscape view of the agroecosystem can bring further explanation elements as to why in fully anthropized S sites we found high bee diversity. First, the agroecosystem has plenty of weeds and shrubs that are not subject to herbicide control and thus provide food to bees. It was common to observe bees foraging on these plants. Actually, the climatic conditions of the study region help this type of vegetation to endure successfully even in the toughest conditions, like in the dry season (Croxton et al., 2002; Kim et al., 2006). Seemingly the characteristic patchy conditions and connectivity of the landscape in our study sites guarantee that nesting substrates, pollen and nectar are continuously available, allowing the survival of bees within their foraging range (Fierro et al., 2012; Gathmann and Tscharntke, 2002; Greenleaf et al., 2007; Ricketts, 2004). In this regard, Calabuig (2000) found a positive correlation between the abundance and diversity of bees and the wealth of plants in the borders of croplands in a region of Denmark. Thus it seems that ruderal plants, and not merely roads in the borders of croplands, may minimize the impact of intensive farming practices (Kwaiser and Hendrix, 2008; Ockinger and Smith, 2007; Oleksa et al., 2013). In conclusion, allowing secondary ecological succession might help reducing the negative effect of agriculture on bee abundance and diversity (Klein et al., 2007; Kwaiser and Hendrix, 2008), which eventually can have a positive effect on the

Fig. 4. Temporal variation in bee abundance in the sampling sites during the study period.

Fig. 5. Similarity index by site. Dendrogram constructed using Jaccard indexes estimated from richness and abundance data.

Fig. 6. Similarity index by month. Dendrogram constructed using Jaccard indexes estimated from richness and abundance data.

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Acknowledgements

productivity of many crops (Klein et al., 2007, 2003; Kremen et al., 2002). The Shannon and the Simpson indexes (Table 1) did not show significant differences among all four sites, despite our sampling sites had different levels of antrophization (Dolven et al., 2013). Again, this is probably due to incomplete samplings in sites with less agriculture, as shown by accumulation curves. Meneses-Calvillo et al. (2010) reported Shannon indexes above 3 in most of their sampling sites in conserved areas within a tropical forest in southern Mexico, indicating high bee diversity, which is not very different from our results. It is known that floral richness shows a positive association with the abundance and richness of bees, which in turn correlates positively with the abundance of shrubs and trees in the margins of croplands (Morrison et al., 2017). Larger margins have a greater proportion of perennials and are more crucial for bee survival in intensive cropping areas than in heterogeneous landscapes. Such findings indicate that the preservation of wide margins with high richness of flowering plants, comprising perennial and arboreal species, could support a dense and diverse community of bees (Croxton et al., 2002; Morrison et al., 2017; PérezMarcos et al., 2017). Accordingly, the role of season in bee diversity and abundance is clear: the highest number of specimens was captured in June-July and the lowest in November-February. One important factor in this respect is that the rainy season begins in May, resulting in the presence of a greater abundance and diversity of plants and flowers for bees (Kearns and Oliveras, 2009). The inclusion of pollinator-friendly plants near crop fields is recommended to minimize the impact of agriculture. It is expected that these strips will support the flow of pollinators from surroundings to the crop fields, thus assisting pollination (Blaauw and Isaacs, 2014; Sidhu and Joshi, 2016; Williams et al., 2015). Moreover, by increasing the diversity of both crops and wildflowers patches next to crop fields a continuous source of pollen and nectar is provided to bees, a practice that may likely be easier for adoption by farmers (O´Brien and Arathi, 2018).

We acknowledge CONACYT for the Ph.D. scholarship granted to Jovani Ruiz-Toledo for his studies and COCYTECH for the economic help through the program “Beca-tesis de posgrado”. This study was part of the SAGARPA-CONACyT 291,333 grant. We are also grateful to Phillipe Sagot and Jorge Mérida for the help given in the identification of bee specimens, as well as Agustín Méndez, Miguel Cigarroa and Miguel Guzmán for the logistical support in bee collection. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2019.106807. References Banaszak, J., 1996. Ecological bases of conservation of wild bees. In: Matheson, A., Buchmann, S.L., O’Toole, C., Westrich, P., Williams, I.H. (Eds.), The Conservation of Bees. T Academic Press, London, UK, pp. 55–62. Bárberi, P., Burgio, G., Dinelli, G., Moonen, A.C., Otto, S., Vazzana, C., Zanin, G., 2010. Functional biodiversity in the agricultural landscape: relationships between weeds and arthropod fauna. Weed Res. 50, 388–401. https://doi.org/10.1111/j.1365-3180. 2010.00798.x. Blaauw, B.R., Isaacs, R., 2014. Flower plantings increase wild bee abundance and the pollination services provided to a pollination-dependent crop. J. Appl. Ecol. 51, 890–898. https://doi.org/10.1111/1365-2664.12257. Brosi, B., Daily, G., Ehrlich, P., 2007. Bee community shifts with landscape context in a tropical countryside. Ecol. Appl. 17, 418–430. Brosi, B., Daily, G., Shih, T., Oviedo, F., Durán, G., 2008. The effects of forest fragmentation on bee communities in tropical countryside. J. Appl. Ecol. 45, 773–783. https://doi.org/10.1111/j. Brower, L.P., Taylor, O.R., Williams, E.H., Slayback, D., Zubieta, R.R., Ramírez, M.I., 2012. Decline of monarch butterflies overwintering in Mexico: is the migratory phenomenon at risk? Insect Conserv. Divers. 5, 95–100. https://doi.org/10.1111/j. 1752-4598.2011.00142.x. Calabuig, I., 2000. Solitary Bees and Bumble Bees in a Danish Agricultural Landscape. University of Copenhagen. Carvalheiro, L.G., Veldtman, R., Shenkute, A.G., Tesfay, G.B., Pirk, C.W.W., Donaldson, J.S., Nicolson, S.W., 2011. Natural and within-farmland biodiversity enhances crop productivity. Ecol. Lett. 14, 251–259. https://doi.org/10.1111/j.1461-0248.2010. 01579.x. Cassman, K., 1999. Ecological intensification of cereal production systems : yield potential, soil quality, and precision agriculture. Proc. Natl. Acad. Sci. U.S.A. 96, 5952–5959. Centro Meteorológico Nacional, 2017. Precipitación a Nivel Nacional Y Por Entidad Federativa. México. . Colwell, R.K., 2013. EstimateS: Statistical Estimation of Species Richness and Shared Species From Samples. Version 9.1.0 Persistent. Costanza, R., Arge, R., Groot, R., De Farber, S., Hannon, B., Limburg, K., Naeem, S., Neill, R.V.O., 1997. The value of the world’s ecosystem services and natural capital. Nature 387, 253–260. Croxton, P.J., Carvell, C., Mountford, J.O., Sparks, T.H., 2002. A comparison of green lanes and field margins as bumblebee habitat in an arable landscape. Biol. Conserv. 107, 365–372. Delucchi, V., 1997. Una nuova frontiera: la gestione ambientale come prevenzione. In: In: Prota, R., Pantaleoni, R. (Eds.), Atti Della Giornata Sulle Strategie Bio-Ecologiche Di Lotta Contro Gli Organismi Nocivi., vol. 11. Sassari, Italy, pp. 35–57. Dolven, J.K., Alve, E., Rygg, B., Magnusson, J., 2013. Defining past ecological status and in situ reference conditions using benthic foraminifera : a case study from the Oslofjord. Norway. Ecol. Indic. 29, 219–233. Ernoult, A., Vialatte, A., Butet, A., Michel, N., Rantier, Y., Jambon, O., Burel, F., 2013. Grassy strips in their landscape context, their role as new habitat for biodiversity. Agric. Ecosyst. Environ. 166, 15–27. https://doi.org/10.1016/j.agee.2011.06.020. Ferrier, S., Ninan, K.N., Leadley, P., Alkemade, R., Acosta, L.A., Akçakaya, H.R., Brotons, L., Cheung, W.W.L., Christensen, V., Harhash, K.A., Kabubo-Mariara, J., Lundquist, C., Obersteiner, M., Pereira, H.M., Peterson, G., Pichs-Madruga, R., Ravindranath, N.H., Rondinini, C., Wintle, B.A., 2016. IPBES (2016): The Methodological Assessment Report on Scenarios and Models of Biodiversity and Ecosystem Services. Bonn, Germany. Fierro, M.M., Cruz-López, L., Sánchez, D., Villanueva-Gutiérrez, R., Vandame, R., 2012. Effect of biotic factors on the spatial distribution of stingless bees (Hymenoptera: apidae, Meliponini) in fragmented neotropical habitats. Neotrop. Entomol. 41, 95–104. Frankie, G.R.T., Schindler, M.H., Ertter, B., Przybylski, M., 2002. Bees in Berkeley. Fremontia 30, 50–58. Gardiner, M., Landis, D., Gratton, C., Difonzo, C., O´Neal, M., Chacón, M., Wayo, M., Schmidt, N., Mueller, E., Heimpel, G., 2009. Landscape diversity enhances biological control of an introduced crop pest in the north-central USA. Ecol. Appl. 19, 143–154. Garibaldi, L., Aizen, M., Klein, A.M., Cunningham, S., Harder, L.D., 2011. Global growth

5. Conclusions The diversity of the bee community was similar in our four study sites, either 100% anthropized and used mainly for agriculture, or 72.5% anthropized and hosting some forest remnants. Despite sampling in preserved areas is missing as a point of reference to fully interpret our data, our first conclusion is that even 27.5% of forest is not enough to compensate for bee diversity losses in agricultural areas of southern Mexico. However, the studied agroecosystems allowed for the maintenance of part of the wild bee community, and therefore of their pollination service to the crops. Therefore, the diversity of weeds and bushes on the margins of croplands should not be reduced, because doing so would likely worsen the bee populations and promote diversity decline (Haughton et al., 2003; Mänd et al., 2002; Osborne et al., 2016; Sáez et al., 2014). Actually, the findings by Fierro et al. (2012) indicate that even in highly disturbed grasslands in our study region, the management that local people give to these pieces of land, which includes the cultivation of native tree species to delimit property boundaries, are important in bee survival. Finally, even if the presence of conserved patches seem to contribute to the richness or abundance of bees (Frankie et al., 2002; Vaudo et al., 2012), a further study including better preserved areas and more extensive samplings would help determining the minimum percentage of forest needed to fully preserve the diversity of bees. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper 6

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