RESEARCH ARTICLE
Spatial Heterogeneity Regulates PlantPollinator Networks across Multiple Landscape Scales Eduardo Freitas Moreira1*, Danilo Boscolo2, Blandina Felipe Viana1 1 Zoology Department, Federal University of Bahia, UFBA, Salvador, Bahia, Brazil, 2 Faculty of Philosophy, Sciences and Literature of Ribeirão Preto, University of São Paulo, Ribeirão Preto, FFCLRP-USP, São Paulo, Brazil * [email protected]
a11111
Abstract
OPEN ACCESS Citation: Moreira EF, Boscolo D, Viana BF (2015) Spatial Heterogeneity Regulates Plant-Pollinator Networks across Multiple Landscape Scales. PLoS ONE 10(4): e0123628. doi:10.1371/journal. pone.0123628 Academic Editor: Paul Adam, University of New South Wales, AUSTRALIA Received: January 12, 2014 Accepted: March 5, 2015 Published: April 9, 2015 Copyright: © 2015 Moreira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The present work had funding support from the Brazilian governmental agencies: Conselho Nacional de Desenvolvimento Científico e Tecnológico(CNPq – URL: http://www.cnpq.br/ Edital MCT/CNPq/CT-AGRO - Nº 24/2009), who financed the purchase of equipment and field data collections campaigns; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - URL: http://www.capes.gov.br/index.php), who granted a scholarship during the master's degree course of Eduardo Freitas Moreira (first author). The funders had no role in study design, data
Mutualistic plant-pollinator interactions play a key role in biodiversity conservation and ecosystem functioning. In a community, the combination of these interactions can generate emergent properties, e.g., robustness and resilience to disturbances such as fluctuations in populations and extinctions. Given that these systems are hierarchical and complex, environmental changes must have multiple levels of influence. In addition, changes in habitat quality and in the landscape structure are important threats to plants, pollinators and their interactions. However, despite the importance of these phenomena for the understanding of biological systems, as well as for conservation and management strategies, few studies have empirically evaluated these effects at the network level. Therefore, the objective of this study was to investigate the influence of local conditions and landscape structure at multiple scales on the characteristics of plant-pollinator networks. This study was conducted in agri-natural lands in Chapada Diamantina, Bahia, Brazil. Pollinators were collected in 27 sampling units distributed orthogonally along a gradient of proportion of agriculture and landscape diversity. The Akaike information criterion was used to select models that best fit the metrics for network characteristics, comparing four hypotheses represented by a set of a priori candidate models with specific combinations of the proportion of agriculture, the average shape of the landscape elements, the diversity of the landscape and the structure of local vegetation. The results indicate that a reduction of habitat quality and landscape heterogeneity can cause species loss and decrease of networks nestedness. These structural changes can reduce robustness and resilience of plant-pollinator networks what compromises the reproductive success of plants, the maintenance of biodiversity and the pollination service stability. We also discuss the possible explanations for these relationships and the implications for landscape planning in agricultural areas.
PLOS ONE | DOI:10.1371/journal.pone.0123628 April 9, 2015
1 / 19
Landscape Effects on Plant-Pollinator Networks
collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist.
Introduction Studies on biological interactions have helped us understand how the emergent properties of mutualistic networks can contribute to the stability of biological systems facing environmental variation [1]. However, despite the importance of the spatial-temporal distribution and behavior of interacting species as major determinants of network structure [2,3], only few studies have explicitly analyzed the direct effects of landscape structure on a key mutualistic inter-specific interaction network, such as a plant-pollinator network [1,4]. Consequently, we still have a poor understanding of the way in which the surrounding environmental conditions can interfere with this process at the systemic level [4–7]. Nevertheless, recent empirical evidence suggests that mutualistic networks may not react as robustly to changes in the landscape as previously expected [4,8]. Landscape modifications strongly affect cross-pollination and plant sexual reproduction primarily by reducing the diversity and availability of pollinators [4]. This mechanism is based on the increased spatial isolation of populations and decreased supplies of floral resources and nesting sites [6]. Furthermore, most agricultural crops on the planet can benefit from or are dependent on pollination services, implying that the negative effects of agriculture on pollinators also reduce agricultural productivity [5,7,9,10]. This negative feedback threatens the sustainability of longterm agricultural production, with the decrease of stability and growth of agricultural yield [11,12]. However, regardless of their important contributions, all these previous studies suffer from serious limitations in terms of establishing clear guidelines for land-use planning. These limitations result from several conceptual and methodological issues. More specifically, there is a general lack of consensus on the negative effect of agriculture, given that results differ among biological groups, landscape definitions and study scales [1,4,6]. Most of these studies were based on a binary habitat-matrix landscape model, an approach which has strong limitations for many systems. Real landscapes are usually heterogeneous and much more complex than a representation with only two land cover classes. In addition, the organisms’ perception of their environment can vary greatly throughout their life history and among species. These principles imply that the definition of habitat must be species specific. Defining habitat for a whole community can thus be tricky and may not be feasible in many cases. A more realistic approach has been proposed by Fahrig et al [13], who suggest that the study of landscape effects on biological communities should be made from the perspective of landscape functional heterogeneity at proper scales. If we consider that communities are complex hierarchical systems, multi-level approaches become necessary for understanding the responses of the systems to disturbance [14]. Vegetation quality and landscape structure may affect the foraging behavior of pollinators at the local level [15,16], the number of pollinators present in the vicinity of the crops at a proximal surrounding landscape level [10,17] and the population’s dynamics at a broader landscape level, compatible with the maintenance of a large number of individuals [3,18]. Accordingly, the influence of each factor of interest at each level must be detected at its appropriate scale, and multiple-level approaches, which are uncommon in the literature, may be necessary to effectively understand these patterns [14,19]. In this study, we aimed to evaluate whether the characteristics of the plant-pollinator network are best explained by a relationship with the environmental characteristics at a single level or at multiple levels in a region with a diverse mosaic of agricultural and natural environments. More specifically, four alternative hypotheses were contrasted, three representing single-level influence (local vegetation, proximal landscape or broad landscape) and one representing multilevel influence. The four hypotheses were represented by corresponding models, and the best model was identified based on the Akaike information criterion through a model selection approach [20]. Additionally, to better understand the interplay between these
PLOS ONE | DOI:10.1371/journal.pone.0123628 April 9, 2015
2 / 19
Landscape Effects on Plant-Pollinator Networks
factors, we performed exploratory analyses to evaluate the relationship between the conversion of natural vegetation into cultivated areas and the other features of the landscape. We then discuss the possible implications of these relationships for land use management and the development of guidelines to reconcile the productivity of agricultural systems with biological conservation, enabling more sustainable land occupation.
Material and Methods Ethic issues and survey permits We attest that the field studies did not involve endangered or protected species. In accordance with the environmental legislation of Brazil (norm n°. 154/2007) we received in 07/15/2011 an authorization (N° 12023–3, authentication code N° 16512688) from the Brazilian Federal Environmental Agency (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis— IBAMA), for collection of biological material during the period between 10/2010 and 04/2012. For more details, please access the SISBIO (Sistema de Autorização e Informação em Biodiversidade), www.icmbio.gov.br/sisbio or contact the corresponding author (see above). In addition, the study was conducted on private land. For further information, please contact the Landowners Association Agropolo Mucuge/Ibicoara.
Study area The present study was conducted on lands managed by the Landowners Association “Agropolo Mucuge/Ibicoara”, which is an agricultural partnership of farms in Chapada Diamantina, Bahia, Brazil occupying the flattest area (197,931 ha) of the municipalities of Ibicoara and Mucugê (limits: 41°42’11” W, 12°43’36” S; 41°15’5” W, 12°43’52” S; 41°42’51” W, 13°44’8” S; 41°15’40” W, 13°44’ 23” S; Fig 1). The altitude varies between 900 and 1400 m a.s.l. According to the Köppen-Geiger classification, the climate is tropical savannah (Aw). There are two well-marked seasons, and the rains are concentrated in the summer [21]. The area has an average annual precipitation of 1281 mm, an annual average maximum temperature of 29°C and a minimum temperature of 19.8°C [22]. This region is dominated by several types of Brazilian savannah (Cerrado), ranging from open meadows to semideciduous forests, with considerable floristic variation among the physiognomies and including parkland and wooded savannah, which are prevalent. Parkland savannah is characterized by graminoid formations interspersed with isolated nanophanerophytes, whereas the wooded savannah has a continuous hemicryptophyte layer with patches of sparse nanophanerophytes [23]. According to Raunkiaer’s nanophanerophytes are woody, dwarf and stunted plants, ranging from 0.25 of 5 m high, whereas hemicryptophytes are herbaceous plants with gametes and shoots protected at the soil level by leafs and sheaths which die out the dry season [23]. The native vegetation types occur in gradients and/or interspersed nearby patches forming mosaics with variable degrees of heterogeneity.
Selection of sampling units From a geographic information system (GIS) containing a SPOT image from the year 2008 (5 m spatial resolution) and information about the region's road network and field checks, 27 sampling units were selected (Fig 1, see also S1A Appendix). As criteria for this selection, we considered the density and stratification of the vegetation in each sampling unit and the proportion of cultivated area and landscape diversity, which was visually estimated from the image with a buffer of 3 km around each sampling point. The distribution of sampling units along the study area followed an orthogonal gradient between cultivated acreage and landscape diversity to minimize spatial autocorrelation. A buffer of 3 km was adopted as the minimum distance
PLOS ONE | DOI:10.1371/journal.pone.0123628 April 9, 2015
3 / 19
Landscape Effects on Plant-Pollinator Networks
Fig 1. Left side: A—highlighted in green, dark gray and light gray, the state of Bahia, Brazil and South America, respectively; B—At the center of the state of Bahia (green), the studied region, with the lands of the agricultural partnership in red and Chapada Diamantina National Park in purple; C—example of the 3 km buffer used for the selection of sampling units; D—arrangement of the 27 selected sampling units (red dots) in the study region and the land cover classification used for the calculation of landscape metrics. doi:10.1371/journal.pone.0123628.g001
between sampling units (minimum nearest neighbor distance = 4.6 km, mean = 25.5 km, maximum = 63.6 km). The final distribution of sampling units tended toward dispersion (nearest neighbor ratio: 1.36, Z score: 3.75, p
Spatial Heterogeneity Regulates PlantPollinator Networks across Multiple Landscape Scales Eduardo Freitas Moreira1*, Danilo Boscolo2, Blandina Felipe Viana1 1 Zoology Department, Federal University of Bahia, UFBA, Salvador, Bahia, Brazil, 2 Faculty of Philosophy, Sciences and Literature of Ribeirão Preto, University of São Paulo, Ribeirão Preto, FFCLRP-USP, São Paulo, Brazil * [email protected]
a11111
Abstract
OPEN ACCESS Citation: Moreira EF, Boscolo D, Viana BF (2015) Spatial Heterogeneity Regulates Plant-Pollinator Networks across Multiple Landscape Scales. PLoS ONE 10(4): e0123628. doi:10.1371/journal. pone.0123628 Academic Editor: Paul Adam, University of New South Wales, AUSTRALIA Received: January 12, 2014 Accepted: March 5, 2015 Published: April 9, 2015 Copyright: © 2015 Moreira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The present work had funding support from the Brazilian governmental agencies: Conselho Nacional de Desenvolvimento Científico e Tecnológico(CNPq – URL: http://www.cnpq.br/ Edital MCT/CNPq/CT-AGRO - Nº 24/2009), who financed the purchase of equipment and field data collections campaigns; Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES - URL: http://www.capes.gov.br/index.php), who granted a scholarship during the master's degree course of Eduardo Freitas Moreira (first author). The funders had no role in study design, data
Mutualistic plant-pollinator interactions play a key role in biodiversity conservation and ecosystem functioning. In a community, the combination of these interactions can generate emergent properties, e.g., robustness and resilience to disturbances such as fluctuations in populations and extinctions. Given that these systems are hierarchical and complex, environmental changes must have multiple levels of influence. In addition, changes in habitat quality and in the landscape structure are important threats to plants, pollinators and their interactions. However, despite the importance of these phenomena for the understanding of biological systems, as well as for conservation and management strategies, few studies have empirically evaluated these effects at the network level. Therefore, the objective of this study was to investigate the influence of local conditions and landscape structure at multiple scales on the characteristics of plant-pollinator networks. This study was conducted in agri-natural lands in Chapada Diamantina, Bahia, Brazil. Pollinators were collected in 27 sampling units distributed orthogonally along a gradient of proportion of agriculture and landscape diversity. The Akaike information criterion was used to select models that best fit the metrics for network characteristics, comparing four hypotheses represented by a set of a priori candidate models with specific combinations of the proportion of agriculture, the average shape of the landscape elements, the diversity of the landscape and the structure of local vegetation. The results indicate that a reduction of habitat quality and landscape heterogeneity can cause species loss and decrease of networks nestedness. These structural changes can reduce robustness and resilience of plant-pollinator networks what compromises the reproductive success of plants, the maintenance of biodiversity and the pollination service stability. We also discuss the possible explanations for these relationships and the implications for landscape planning in agricultural areas.
PLOS ONE | DOI:10.1371/journal.pone.0123628 April 9, 2015
1 / 19
Landscape Effects on Plant-Pollinator Networks
collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist.
Introduction Studies on biological interactions have helped us understand how the emergent properties of mutualistic networks can contribute to the stability of biological systems facing environmental variation [1]. However, despite the importance of the spatial-temporal distribution and behavior of interacting species as major determinants of network structure [2,3], only few studies have explicitly analyzed the direct effects of landscape structure on a key mutualistic inter-specific interaction network, such as a plant-pollinator network [1,4]. Consequently, we still have a poor understanding of the way in which the surrounding environmental conditions can interfere with this process at the systemic level [4–7]. Nevertheless, recent empirical evidence suggests that mutualistic networks may not react as robustly to changes in the landscape as previously expected [4,8]. Landscape modifications strongly affect cross-pollination and plant sexual reproduction primarily by reducing the diversity and availability of pollinators [4]. This mechanism is based on the increased spatial isolation of populations and decreased supplies of floral resources and nesting sites [6]. Furthermore, most agricultural crops on the planet can benefit from or are dependent on pollination services, implying that the negative effects of agriculture on pollinators also reduce agricultural productivity [5,7,9,10]. This negative feedback threatens the sustainability of longterm agricultural production, with the decrease of stability and growth of agricultural yield [11,12]. However, regardless of their important contributions, all these previous studies suffer from serious limitations in terms of establishing clear guidelines for land-use planning. These limitations result from several conceptual and methodological issues. More specifically, there is a general lack of consensus on the negative effect of agriculture, given that results differ among biological groups, landscape definitions and study scales [1,4,6]. Most of these studies were based on a binary habitat-matrix landscape model, an approach which has strong limitations for many systems. Real landscapes are usually heterogeneous and much more complex than a representation with only two land cover classes. In addition, the organisms’ perception of their environment can vary greatly throughout their life history and among species. These principles imply that the definition of habitat must be species specific. Defining habitat for a whole community can thus be tricky and may not be feasible in many cases. A more realistic approach has been proposed by Fahrig et al [13], who suggest that the study of landscape effects on biological communities should be made from the perspective of landscape functional heterogeneity at proper scales. If we consider that communities are complex hierarchical systems, multi-level approaches become necessary for understanding the responses of the systems to disturbance [14]. Vegetation quality and landscape structure may affect the foraging behavior of pollinators at the local level [15,16], the number of pollinators present in the vicinity of the crops at a proximal surrounding landscape level [10,17] and the population’s dynamics at a broader landscape level, compatible with the maintenance of a large number of individuals [3,18]. Accordingly, the influence of each factor of interest at each level must be detected at its appropriate scale, and multiple-level approaches, which are uncommon in the literature, may be necessary to effectively understand these patterns [14,19]. In this study, we aimed to evaluate whether the characteristics of the plant-pollinator network are best explained by a relationship with the environmental characteristics at a single level or at multiple levels in a region with a diverse mosaic of agricultural and natural environments. More specifically, four alternative hypotheses were contrasted, three representing single-level influence (local vegetation, proximal landscape or broad landscape) and one representing multilevel influence. The four hypotheses were represented by corresponding models, and the best model was identified based on the Akaike information criterion through a model selection approach [20]. Additionally, to better understand the interplay between these
PLOS ONE | DOI:10.1371/journal.pone.0123628 April 9, 2015
2 / 19
Landscape Effects on Plant-Pollinator Networks
factors, we performed exploratory analyses to evaluate the relationship between the conversion of natural vegetation into cultivated areas and the other features of the landscape. We then discuss the possible implications of these relationships for land use management and the development of guidelines to reconcile the productivity of agricultural systems with biological conservation, enabling more sustainable land occupation.
Material and Methods Ethic issues and survey permits We attest that the field studies did not involve endangered or protected species. In accordance with the environmental legislation of Brazil (norm n°. 154/2007) we received in 07/15/2011 an authorization (N° 12023–3, authentication code N° 16512688) from the Brazilian Federal Environmental Agency (Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renováveis— IBAMA), for collection of biological material during the period between 10/2010 and 04/2012. For more details, please access the SISBIO (Sistema de Autorização e Informação em Biodiversidade), www.icmbio.gov.br/sisbio or contact the corresponding author (see above). In addition, the study was conducted on private land. For further information, please contact the Landowners Association Agropolo Mucuge/Ibicoara.
Study area The present study was conducted on lands managed by the Landowners Association “Agropolo Mucuge/Ibicoara”, which is an agricultural partnership of farms in Chapada Diamantina, Bahia, Brazil occupying the flattest area (197,931 ha) of the municipalities of Ibicoara and Mucugê (limits: 41°42’11” W, 12°43’36” S; 41°15’5” W, 12°43’52” S; 41°42’51” W, 13°44’8” S; 41°15’40” W, 13°44’ 23” S; Fig 1). The altitude varies between 900 and 1400 m a.s.l. According to the Köppen-Geiger classification, the climate is tropical savannah (Aw). There are two well-marked seasons, and the rains are concentrated in the summer [21]. The area has an average annual precipitation of 1281 mm, an annual average maximum temperature of 29°C and a minimum temperature of 19.8°C [22]. This region is dominated by several types of Brazilian savannah (Cerrado), ranging from open meadows to semideciduous forests, with considerable floristic variation among the physiognomies and including parkland and wooded savannah, which are prevalent. Parkland savannah is characterized by graminoid formations interspersed with isolated nanophanerophytes, whereas the wooded savannah has a continuous hemicryptophyte layer with patches of sparse nanophanerophytes [23]. According to Raunkiaer’s nanophanerophytes are woody, dwarf and stunted plants, ranging from 0.25 of 5 m high, whereas hemicryptophytes are herbaceous plants with gametes and shoots protected at the soil level by leafs and sheaths which die out the dry season [23]. The native vegetation types occur in gradients and/or interspersed nearby patches forming mosaics with variable degrees of heterogeneity.
Selection of sampling units From a geographic information system (GIS) containing a SPOT image from the year 2008 (5 m spatial resolution) and information about the region's road network and field checks, 27 sampling units were selected (Fig 1, see also S1A Appendix). As criteria for this selection, we considered the density and stratification of the vegetation in each sampling unit and the proportion of cultivated area and landscape diversity, which was visually estimated from the image with a buffer of 3 km around each sampling point. The distribution of sampling units along the study area followed an orthogonal gradient between cultivated acreage and landscape diversity to minimize spatial autocorrelation. A buffer of 3 km was adopted as the minimum distance
PLOS ONE | DOI:10.1371/journal.pone.0123628 April 9, 2015
3 / 19
Landscape Effects on Plant-Pollinator Networks
Fig 1. Left side: A—highlighted in green, dark gray and light gray, the state of Bahia, Brazil and South America, respectively; B—At the center of the state of Bahia (green), the studied region, with the lands of the agricultural partnership in red and Chapada Diamantina National Park in purple; C—example of the 3 km buffer used for the selection of sampling units; D—arrangement of the 27 selected sampling units (red dots) in the study region and the land cover classification used for the calculation of landscape metrics. doi:10.1371/journal.pone.0123628.g001
between sampling units (minimum nearest neighbor distance = 4.6 km, mean = 25.5 km, maximum = 63.6 km). The final distribution of sampling units tended toward dispersion (nearest neighbor ratio: 1.36, Z score: 3.75, p
