Landscape composition influences pollinators and pollination services in perennial biofuel plantings
Introduction
Biofuel cropping systems are one alternative to non-renewable energy sources and are seen as an integral component of a sustainable energy policy. In the United States, an annual target of 35 billion gallons of ethanol by 2022 has been proposed, including a mandate that 57% of this capacity come from renewable fuels such as bioenergy crops (Tyner, 2008). Annual crops such as corn and perennial crops such as mixed grasslands are being investigated as potential bioenergy crops. Large scale changes in land cover are a potential consequence of future expansion of bioenergy crop production, which may have significant impacts on biodiversity. As a result, biofuel production systems are being compared for their ability to produce biomass while also conserving biodiversity and the provision of multiple ecosystem services (James et al., 2010, Landis and Werling, 2010, Wu et al., 2012, Jarchow and Liebman, 2012).
Incorporating perennial biofuel crops such as native grasslands into agricultural landscapes has the potential for significant effects on biodiversity and the ecosystem services provided to agricultural systems. Empirical studies have consistently found that increasing plant diversity positively impacts arthropod diversity (Siemann et al., 1998, Knops et al., 1999, Koricheva et al., 2000, Scherber et al., 2010), and recent research on biofuel cropping systems also revealed that annual and perennial biofuel crops differentially support beneficial arthropods (Werling et al., 2011). In particular, the abundance and diversity of pollinators were higher in perennial biofuel crops (e.g. prairie and switchgrass) compared to the annual bioenergy crop corn (Gardiner et al., 2010). Developing bioenergy cropping systems that are productive yet support diverse pollinator communities may offer a strategy for energy production that concurrently conserves biodiversity and promotes ecosystem services that are valuable to agricultural and semi-natural landscapes. In agricultural landscapes across the United States, crop pollination is valued at $3 billion per year (Losey and Vaughan, 2006), while globally approximately 87% of flowering plants rely on pollination for fruit and seed set (Ollerton et al., 2011). Although the value of pollination services provided to natural systems has yet to be quantified, it is expected to exceed the value provided to agricultural systems (LeBuhn et al., 2013).
The selection of bioenergy crops for expanded production has the potential to affect pollinators by modifying the diversity and composition of agricultural landscapes. At the local (field) scale, bioenergy crops in the Upper Midwest region of the United States will range from monocultures of annual crops, such as corn, to diverse mixtures of perennial grasses and forbs. The selection of bioenergy crops will substantially affect plant diversity at local scales, influencing the availability of pollen, nectar, and nesting habitat which are primary drivers of pollinator abundance and diversity (Holzschuh et al., 2011, Stanley and Stout, 2013, Nicholls and Altieri, 2013). At larger spatial scales, the addition of bioenergy crops will also change landscape composition. Rising corn prices have recently spurred the conversion of marginal lands into annual bioenergy crops such as corn, which has expanded monoculture plantings and lowered landscape diversity (Wright and Wimberly, 2013). In contrast, adding diverse perennial grassland mixtures could increase landscape diversity and augment the amount of semi-natural habitat needed to support beneficial organisms. Agricultural systems with higher proportions of semi-natural habitat and greater diversity of land use are positively correlated with bee abundance and diversity (Holzschuh et al., 2007, Klein et al., 2012, Kennedy et al., 2013). Furthermore, the proportion of semi-natural habitat in the landscape surrounding pollinator-dependent crops seems integral to maximizing pollination due to the food and nesting resources available to support native bee populations (Winfree et al., 2007, Klein et al., 2012, Holzschuh et al., 2012). These results suggest that diverse perennial bioenergy cropping systems have the potential to facilitate pollinator conservation and increase pollination services across broad spatial scales.
Understanding how the expansion of different biofuel cropping systems will shape landscape composition and subsequently affect biodiversity and ecosystem services will be critical to developing a sustainable bioenergy policy. Our aim in this research was to determine whether pollinators and pollination services vary in response to the amount of perennial grasslands in the surrounding landscape. We selected 20 agricultural fields along a gradient of low to high amounts of perennial grassland in the surrounding landscape to sample bees and measure pollination services. We predicted that (1) bee abundance and diversity would be positively correlated with the amount of perennial grassland, (2) bee community composition would change across the gradient of low to high grassland cover, and (3) pollination services would increase as the proportion of grassland increased in the landscape surrounding fields.
Section snippets
Study sites
To measure the effect of landscape composition on bees and pollination services, we identified 20 soybean fields in Michigan, USA that varied in their proportions of surrounding perennial grassland and were at least 3 km apart (Fig. 1). Soybean fields were used as study sites because they occur in various landscape contexts, and the soybean crop, a monoculture intensively managed for weeds, limits variability (e.g. plant diversity, management practices) at the field scale. In addition, the
Community composition
Overall, 248 bee pollinators of sunflower including 37 bee species were collected during 75 h of observation (Supplementary data B, Table B1). Bee community composition was significantly different across the gradient of low to high grassland cover. A NMDS ordination indicated bee communities were significantly different between sites with high and low grassland cover (Fig. 2, ANOSIM, r = 0.55, P = 0.001) but were similar between sites with intermediate and low and between intermediate and high
Discussion
This study highlights the role of grasslands in supporting bees and pollination services across agricultural landscapes and their potential importance within a sustainable biofuels policy. Here, we find that (1) bee abundance was positively correlated with the amount of grassland in the surrounding landscape, (2) bee diversity increased as the amount of forest increased in the landscape surrounding sites, (3) community composition was different in landscapes with high and low proportions of
Conclusions
As demand for renewable sources of energy increase, biofuel crop production is expected to expand, providing a unique opportunity to reshape the composition of agricultural landscapes. Our results demonstrated increasing proportions of grassland habitat were positively correlated with higher bee abundance and that increased bee abundance positively affected pollination services delivered to a pollination-dependent plant. Policy to encourage perennial grass production could significantly
Acknowledgments
A special thanks to the participating landowners and Ben Werling who established our network of sites. Thanks to Ashley McNamara, Lindsey Pudlo, Jon Roney, and Laura Maihofer who provided invaluable field assistance and Jason Gibbs who provided bee identifications. This research was funded by the U.S. DOE Great Lakes Bioenergy Research Center (DOE Office of Science BER DE-FC02-07ER64494) and by USDA-NIFA (grant 2012-67009-20146).
References (67)
The complex responses of social stingless bees (Apidae: Meliponini) to tropical deforestation
For. Ecol. Manage.
(2009)- et al.
Landscape context and habitat type as drivers of bee diversity in European annual crops
Agric. Ecosyst. Environ.
(2009) - et al.
On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray–Curtis coefficient for denude assemblages
J. Exp. Mar. Biol. Ecol.
(2006) - et al.
Garden flowers: insect visits and the floral reward of horticulturally-modified variants
Ann. Bot.
(1999) - et al.
Native or exotic? Double or single? Evaluating plants for pollinator-friendly gardens
Ann. Bot.
(2001) - et al.
Flower constancy in bumblebees: a test of the trait variability hypothesis
Anim. Behav.
(2005) - et al.
Spontaneous flower constancy and learning in honey bees as a function of colour
Anim. Behav.
(1997) - et al.
Landscapes with wild bee habitats enhance pollination, fruit set and yield of sweet cherry
Biol. Conserv.
(2012) - et al.
Impacts of coffee agroforestry management on tropical bee communities
Biol. Conserv.
(2010) - et al.
Intensification of agriculture, landscape composition and wild bee communities: a large scale study in four European countries
Agric. Ecosyst. Environ.
(2010)
Solitary bee abundance and species richness in dynamic agricultural landscapes
Agric. Ecosyst. Environ.
Influence of habitat and landscape perenniality on insect natural enemies in three candidate biofuel crops
Biol. Control
Crop flower visitation by honeybees, bumblebees and solitary bees: behavioral differences and diversity responses to landscape
Agric. Ecosyst. Environ.
Simulated impact of future biofuel production on water quality and water cycle dynamics in the Upper Mississippi river basin
Biomass Bioenergy
Null hypothesis testing: problems, prevalence, and an alternative
J. Wildl. Manage.
PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods
Bee community shifts with landscape context in a tropical countryside
Ecol. Appl.
Model Selection and Multimodel Inference: A Practical Information—Theoretic Approach
Characterizing floral specialization by bees: analytical methods and a revised lexicon for oligolecty
PRIMER v6: User Manual/Tutorial
Change in Marine Communities: An Approach to Statistical Analysis and Interpretation
Two bee-pollinated plant species show higher seed production when grown in gardens compared to Arable Farmland
PLoS One
Insect Pollination of Crops
Pollinator diversity and specialization in relation to flower diversity
Oikos
Implications of three biofuel crops for beneficial arthropods in agricultural landscapes
Bioenergy Res.
Stability of pollination services decreases with isolation from natural areas despite honey bee visits
Ecol. Lett.
Foraging ranges of solitary bees
J. Anim. Ecol.
Floral diversity and the facilitation of pollination
J. Ecol.
Revision of the metallic Lasioglossum (Dialictus) of eastern North America (Hymenoptera: Halictidae: Halictini)
Zootaxa
Bee foraging ranges and their relationship to body size
Oecologia
Increased bumblebee abundance along the margins of a mass flowering crop: evidence for pollinator spill-over
Oikos
Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context
J. Appl. Ecol.
Expansion of mass-flowering crops leads to transient pollinator dilution and reduced wild plant pollination
Proc. R. Soc. B-Biol. Sci.
Cited by (68)
Importance of maternal resources in pollen limitation studies with pollinator gradients: A case study with sunflower
2022, Agriculture, Ecosystems and EnvironmentCitation Excerpt :This broad dominance of honey bees enabled us to get the pollinator gradient we were looking for within the fields by moving away from the PS, defined by where honey bee colonies were placed. However, in areas where sunflower is native (eastern North America; Blackman et al., 2011), honey bees often visit heads in small numbers compared to wild bees (e.g. Posey et al., 1986; Bennett and Isaacs, 2014; Todd et al., 2016; Mallinger and Prasifka, 2017a; Mallinger et al., 2019). In Asia, some other Apis species also visit sunflower fields in large numbers (e.g. Jadhav et al., 2011; Ali et al., 2015; Said et al., 2017; Devaramane et al., 2018).
Supply chain configuration of sustainable aviation fuel: Review, challenges, and pathways for including environmental and social benefits
2021, Renewable and Sustainable Energy ReviewsBee (Apoidea) community response to perennial grass treatments managed for livestock production and conservation
2021, Agriculture, Ecosystems and EnvironmentRapid measurement of the adult worker population size in honey bees
2021, Ecological IndicatorsPollinator presence in orchards depends on landscape-scale habitats more than in-field flower resources
2020, Agriculture, Ecosystems and EnvironmentInfluence of the Conservation Reserve Program (CRP) and playa wetlands on pollinator communities in the Southern High Plains, USA
2020, Journal of Environmental Management