Influence of landscape composition on wild bee communities: Effects of functional landscape heterogeneity
Introduction
Globally, agriculture and pastures are the greatest source of anthropogenic land use and land cover change with largely negative consequences for biodiversity (Tscharntke et al., 2005; Foley et al., 2011; Newbold et al., 2015). Conventional agricultural development typically simplifies the structure and species composition of natural habitats, leading to habitat fragmentation and homogenization (Foley et al., 2005). Reconciling agricultural expansion and intensification with biodiversity conservation and economic development remains one of the greatest challenges facing a growing human population. For this reason, it is necessary to understand that the diversity-productivity relationship refers to a pattern of increasing ecosystem primary production associate with increasing species richness (Lambers et al., 2004). In this context, spatial heterogeneity of land cover types (Cardinale et al., 2000) promotes the coexistence of species by more finely partitioning resources within the landscape (Tilman and Kareiva, 2018).
Spatial heterogeneity can be defined as a mosaic of habitats and their functional roles in the landscape (Fahrig et al., 2011). Functional landscape heterogeneity refers to the presence of resources that play a functional role in each habitat (for example, food, nesting sites, dispersal routes of bees) to support a species or groups of species (e.g., bees can distinguish land cover types using criteria such as floristic and edaphic conditions, see Cane, 1991). This dimension of landscape heterogeneity includes two main components: (a) compositional heterogeneity, which is the number of habitats and the proportion of different types of coverage (e.g., percentage of coverage with "forest plantations"), and b) the configurational heterogeneity that refers to the complexity of the landscape (for example, in two areas with the same number and proportion of their coverage, the configurational heterogeneity is given by the size and spatial ordering of their patches) (Fahrig and Nuttle, 2005). Both components represent "habitat heterogeneity" (number of habitat patches and ecotone length per unit area; see Duelli, 1997).
The effects of landscape heterogeneity on pollinators and associated pollination services have been estimated in various ways (Goulson et al., 2008, Potts et al., 2003; Brosi et al., 2008; Schaffers et al., 2008; Kennedy et al., 2013; Hopfenmüller et al., 2014; Steckel et al., 2014; Dainese et al., 2019). Most of these studies found that pollinators benefit from greater heterogeneity in landscape composition (compositional heterogeneity as the percentage of cover of natural habitats foster pollinator species) (Martin et al., 2019). However, estimating these effects in wild bee populations has been somewhat neglected with most of the focus on mass flowering crops that provide a large amount of resources (Diekötter et al., 2014). In this regard, different types of habitats are associated with different botanical communities (Hyvönen and Salonen, 2002) and, therefore, provide different food resources (Blitzer et al., 2012; Mandelik et al., 2012; Hass et al., 2018).
In the last two decades, Argentina has experienced two primary types of land conversion: (1) land-use change associated with intensive agriculture and pasture, and (2) afforestation, mainly, to Pinus taeda and Eucalyptus grandis plantations for wood, pulp, and biomass energy (Baldi and Paruelo, 2008; Azpiroz et al., 2012). Afforested plantations are expanding rapidly across South America because of favorable policies that promote plantation forestry to increase the supply of domestic wood (e.g., Argentine law No 25.080 and extend No 27.487).
In this study, we examined wild bee communities of the Espinal region, in Entre Ríos, Argentina and how they are influenced by the main land uses in this area: forest plantations, pasture/croplands, mixed uses areas (fruticulture farms of citrus and blueberry with little blocks of Eucalyptus plantations), and native espinal savanna. We surveyed wild bees (flowering period 2014–2015) in these four lands uses and compared wild bee abundance, richness and species diversity. Based on past research, we hypothesized that wild bee communities (abundance, richness and species diversity) are in part structured by landscape compositional and configurational heterogeneity. We expect that the number of habitat classes, percentage of predominant plant cover (compositional heterogeneity) and the diversity of floral resources (configurational heterogeneity) that define the Espinal region influence the structure of wild bee communities due to the different nutritional requirements and degree of specialization. In this way, this research will clarify how spatial heterogeneity and different land uses affect wild bee communities in this region.
Section snippets
Study area description
We conducted our research inside of the Espinal phytogeographic region, specifically in the Ñandubayzal and Selva de Montiel (sclerophyte forest with a predominance of Prosopis affinis) (Oyarzabal et al., 2018). The sites selected were all within of Entre Rios province, Argentina, near the city of Concordia (31°24′S 58°2′W). This generally flat area is crisscrossed by small streams and rivers that drain into Río Uruguay to the east and the Río Paraná to the west, with gently rolling hills, and
Results
We identified 3407 individuals’ “bees” from 96 species within 5 families: Andrenidae (9 spp.), Apidae (38 spp.), Colletidae (2 spp.), Halictidae (29 spp.), and Megachillidae (18 spp.) (Table A.7). From the wild bee community, the Halictidae family stands out with the highest abundance (33.81 % of the total) and the family Apidae with the highest species richness (38.54 % of the total), with Colletidae being the family with the lowest representation (2 species with 4 total individuals). Among
Discussion
Wild bee community diversity increased with floral resource abundance and diversity at the landscape scale, and was influenced by the structure of the landscape. Forest plantations supported the lowest bee diversity and abundance. Land uses with greater habitat richness (mixed uses), agriculture, and native espinal savanna, contained similarly higher bee species richness, each with a distinct assemblage of species. These patterns were largely explained by the availability of flower resources
Conclusions
These results demonstrate that habitats modified by humans can contribute important resources for certain bee communities, although oligolectic species (bee species that collect pollen from a limited number of plant species) are particularly sensitive to the loss of native habitats related to some preferred floral species (Rollin et al., 2015). Even so, by thoughtfully integrating natural and anthropogenic components of the landscape, it is to support diverse pollinator communities and
Authors contributions
P.C., C.C.P. and J.L. conceived the ideas and jointly designed the field methodology and bee sampling while P.C. and N.P.C. designed the floral resourse index analysis portion of the project; P.C., C.C.P. and N.P.C. contributed equally to the writing of the manuscript; P.C. and C.C.P. collected the samples; P.C. identified the bees and completed data analysis. This work was supported by the National Science Foundation Partnerships in International Research and Education grant (No. 1243444) to
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.
Acknowledgments
This research was supported by the National Science Foundation Partnerships for International Research and Education program (grant num. 1243444), the USDA McIntire–Stennis program, and the Michigan Technological University Graduate School Finishing Fellowship program. The authors are deeply appreciative of the INTA extension agents, particularly L. Roman, who helped build connections with the many landowners and farmers who permitted us to sample on their lands, and special thanks to Dr.
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