Large-scale monoculture reduces honey yield: The case of soybean expansion in Argentina
Introduction
Industrial agriculture based on the intensive cultivation of few crops, which prevails in several regions of the world (Foley, 2011), is associated with a profound transformation of production methods. In particular, the frequent use of genetically modified seeds, large inputs of agrochemicals and direct sowing, as well as of heavy machinery that covers large areas of land in less time have reduced cultivation and harvesting costs, leading to a reduction in labour costs (Kremen et al., 2012). Consequently, the spatial scale of production based on single crops has increased notably. These extensive monocultures have led to a simplification and homogenization of agricultural landscapes, posing challenges for biodiversity and the benefits derived from it (Bommarco et al., 2013; Aizen et al., 2019).
In particular, the dominance of monoculture in detriment of other land uses, together with the intensive use of non-selective herbicides, leads to a decrease in plant species diversity at both local and regional scales through different non-mutually exclusive mechanisms (Hillebrand et al., 2008). First, the expansion of arable land reduces areas dedicated to other productive activities such as raising livestock, which, at intermediate stocking rates, may actually increase plant species diversity in natural and semi-natural pastures (Smith et al., 2016). Second, monoculture expansion within agricultural lands is detrimental to crop diversity (Aizen et al., 2019). Third, demand for more cultivated land leads to the expansion of the agricultural frontier through the destruction of native forests and grasslands, with the consequent loss of large areas of natural and semi-natural vegetation (Gibbs et al., 2010). Finally, broad-spectrum herbicides eliminate not only target weeds but also vegetation growing on the edges of crop fields and roads, reducing plant diversity both inside and outside crop plots (Goulson et al., 2015; Potts et al., 2016). All these mechanisms lead to a loss of plant diversity with consequences for other trophic levels.
A reduction in plant diversity implies a loss in the amount, variety, and spatial and temporal availability of floral resources (nectar and pollen), which can strongly affect animals, such as bees (Apoidea), that feed exclusively upon these resources throughout their lives. Nectar provides mostly carbohydrates whereas pollen provides proteins, lipids, vitamins and minerals (De Groot, 1953; Haydak, 1970), with the nutritional value of floral resources varying between species and vegetation types (Keller et al., 2005; Odoux et al., 2012; Roulston and Cane, 2000). Nutritional requirements of bees may be inadequately satisfied when the habitat is dominated by extensive monocultures (Branchiccela et al., 2019; Brodschneider and Crailsheim, 2010; Naug, 2009). In fact, a pollinator-dependent monoculture represents an oversupply of a single floral resource only available for a few weeks, followed by a long period of food scarcity (Dolezal et al., 2019a; Requier et al., 2015). This strong reduction in the spatial diversity and temporal availability of floral resources may jeopardize bee survivorship as well as the pollination services provided by bees (Potts et al., 2010).
The honeybee (Apis mellifera), the most important species worldwide for honey production and managed pollination, depends on the access to diverse floral resources over time to survive and maintain healthy and productive colonies (Standifer, 1967; Herbert et al., 1977). Landscape homogenization, decreasing flower abundance and diversity, and different agrochemicals, including a plethora of pesticides, can affect honeybee colony performance by increasing the incidence of lethal and sub-lethal effects (Dolezal et al., 2016; Henry et al., 2012; Mullin et al., 2010; Scofield and Mattila, 2015; Smart et al., 2016; Yang et al., 2008). These sublethal effects can impact individual honeybee foraging efficiency (Dolezal et al., 2015; Toth et al., 2005), the capacity to deal with agrochemicals present in the environment (Di Pasquale et al., 2013, 2016; Goulson et al., 2015; Krupke et al., 2012; Tosi et al., 2017, 2018; Dolezal and Toth, 2018), and the ability to withstand pathogen infection (Di Pasquale et al., 2013, 2016; Dolezal et al., 2016, Dolezal et al., 2019b). The consequences of the additive and/or synergistic effects of these stressors on individuals can scale up to the health of entire beehives (Alaux et al., 2010; DeGrandi-Hoffman and Chen, 2015). In particular, hive development and productivity could be affected by pronounced cycles of bounty and dearth of floral resources associated with landscapes dominated by single crops (Dolezal et al., 2019b; Requier et al., 2017; Smart et al., 2016). Therefore, honey yield (i.e., honey production per hive) is expected to be negatively affected by the expansion of industrial agriculture.
In Argentina, as in other South American countries, soybean is currently the emblematic commodity crop of industrial agriculture (Dros, 2004; Manzanal, 2017; Pengue and Altieri, 2005). The area dedicated to the cultivation of this oilseed was fairly insignificant at the beginning of 1970 (FAOSTAT, 2018). Since then, the greater profitability of agriculture compared to livestock, coupled with improvements in agricultural techniques, has led to a drastic transformation of the countryside (Cadenazzi, 2009; Pengue, 2001). This transformation involved, among others, a more continuous and intensive use of land cover for monoculture crop production, greater use of agrochemical inputs (fertilizers, herbicides and pesticides), and the employment of larger and more impacting machinery.
The release of genetically modified soybean in 1996 in Argentina was the foundational event that triggered the exponential growth of this crop in South America during the last decades (Satorre, 2005), also facilitated by a global economic context favourable to the export of primary products and commodities (Páez, 2016). The initial release and success of different varieties of genetically modified soybean into the Argentinean agricultural economy opened the door for the intensification of industrial agriculture. More specifically, the technological package associated with the cultivation of genetically modified soybean included: (1) use of soybean seeds resistant to glyphosate-based herbicides; (2) massive application of these herbicides for the control of weeds, along with other agrochemicals; (3) direct sowing or zero tillage; (4) use of heavy machinery for sowing and harvesting; and, consequently, (5) an increase in the spatial scale of production and the average area of cultivated lots (Cadenazzi, 2009; Dominguez and Sabatino, 2006; Kahl, 2012; Pengue and Altieri, 2005). Through this process of land-use change, soybean became the dominant crop (i.e. the one that individually has the largest cultivated area) in Argentinean agriculture (Aizen et al., 2009).
Even though Argentina is one of the main producers and exporters of honey worldwide, national beekeeping trends are showing critical signs of decreasing honey production (Requier et al., 2018; Sanchez et al., 2018). Although some soybean cultivars produce nectar accessible to the honeybee (Erickson, 1975; Erickson and Garment, 1979; Villanueva-Gutiérrez et al., 2014), the increase in soybean production has been hypothesized as the single most important cause of this decline (Blengino, 2013). Beekeeping activity is best-developed in the central region of the country, including the Pampas plain, home to 68 % of the beekeepers, 80 % of the hives (Ferrari et al., 2011), and 93 % of the exported honey production nationwide (Rabaglio and Castignani, 2015). This region also accounted for about 90 % of the total national soybean production between 2010–2018 (Agroindustry Open Data, 2018). Given the large geographical overlap between agriculture and beekeeping in Argentina, a detailed analysis of the link between temporal changes in soybean cultivation and honey production in recent decades at the country level is urgently needed to address the hypothesis that industrial agriculture has a negative effect on apiculture.
In this study, we assessed the impact of the industrial agriculture on beekeeping and honey production, using the rapid expansion of soybean cultivation in Argentina as a study case. First, we evaluated the temporal relation between soybean cultivated area and honey yield over 55 years in the long and short term (i.e., long-term trend and detrended variability, respectively). Then, we tested a causal model that considers five variables (i.e., soybean area, honey export value, number of hives, honey yield, and total honey production) to assess the influence of soybean area on Argentinean honey production. We hypothesized that expansion of soybean cultivation has negatively affected overall honey production mainly through changes in honey yield. Therefore, after the implementation of genetically modified soybean in 1996, which led to the intensification of industrial agriculture in Argentina, we predict (1) a progressive decrease in honey yield over time, (2) a negative relation between honey yield and soybean area once the long-term trend has been removed (fine-scale temporal coupling), and (3) an indirect negative effect of soybean area on total honey production mediated by decreasing yield.
Section snippets
Materials and methods
We retrieved data from the United Nations Food and Agriculture Organization (FAO) database (FAOSTAT, 2018), which was analysed with different statistical techniques using the free software R (version 3.4.2) (R Core Team, 2015). From FAOSTAT (2018), we obtained annual values of land area cultivated with soybean (actually reported as harvested area), total number of beehives, and total honey production in Argentina between 1961 and 2016. We checked this FAO data against national statistics (see
Results
Soybean occupied <0.01 % of the total cultivated area of Argentina in 1961, representing ca. 1000 ha (Fig. 1a, Table S3). The segmented regression estimated two break points in the rate of expansion of soybean area, the first in 1975 (P < 0.001; CI = 1971–1978) and the second in 1995 (P < 0.001; CI = 1993–1997) (Fig. 2a). Since 1975, soybean cultivation began to expand at an average rate of 282,797 ha year−1, reaching an area of approximately 6,000,000 ha harvested in 1995. The area cultivated
Discussion
Industrial agriculture, which implies a radical landscape transformation and the intense use of agrochemical inputs, can affect other productive activities. This is the case of beekeeping that depends on the presence of diverse nutritional resources for the honeybee at landscape scale. Our results support the hypothesis that in Argentina the intensification of industrial agriculture, based on the release of transgenic soybean in 1996, has had a strong impact on honey production.
In particular,
Conclusions
Industrial agriculture, currently dominant in several agricultural regions of the world, has introduced numerous stressors that can directly and indirectly affect bees and other insects. We provide evidence that a decrease in honey yield can be linked to soybean monoculture intensification in Argentina since 1996. Future experimental and correlative studies should test the underlying mechanisms, interactions and synergies.
More generally, this study contributes to the growing scientific evidence
Author contributions
GSDG, MAA, AS & CLM conceived the idea and the analyses. GSDG collected data. GSDG & MAA performed analyses. GSDG wrote the initial manuscript. All co-authors contributed significantly to improving the manuscript. All authors gave final approval for publication.
Funding
This work is part of the “Safeguarding Pollination Services in a Changing World: theory into practice” (SURPASS2), an international collaboration funded by the Newton Fund Latin American Biodiversity Programme, awarded through the UKRI Natural Environment Research Council (NERC) NE/S011870/1 and the National Council of Scientific and Technological Research of Argentina (CONICET) RD 1984-19. Support from the National Fund for Scientific and Technological Research of Argentina (FONCYT) [PICT
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.
Acknowledgements
We thank Amy Toth, Ron Miksha, Gherardo Bogo and Pablo Hünicken for constructive comments on an early version of this manuscript, and INTA ProApi, Beekeepers Association of the Comarca and the Secretary of Urban and Periurban Agriculture of Bariloche for their support.
References (98)
- et al.
The truth about honeybees
New Sci.
(2009) - et al.
The global stock of domesticated honeybee is growing slower than agricultural demand for pollination
Curr. Biol.
(2009) - et al.
Ecological intensification: harnessing ecosystem services for food security
Trends Ecol. Evol.
(2013) - et al.
Nutrition, immunity and viral infections in honeybee
Curr. Opin. Insect Sci.
(2015) - et al.
Feedbacks between nutrition and disease in honeybee health
Curr. Opin. Insect Sci.
(2018) - et al.
The role of soybean production as an underlying driver of deforestation in the South American Chaco
Glob. Environ. Change
(2017) - et al.
Positive outcomes between crop diversity and agricultural employment worldwide
Ecol. Econ.
(2019) Nutritional stress due to habitat loss may explain recent honeybee colony collapses
Biol. Conserv.
(2009)- et al.
Global pollinator declines: trends, impacts and drivers
Trends Ecol. Evol.
(2010) - et al.
Proximity to a forest leads to higher honey yield: another reason to conserve
Biol. Conserv.
(2009)
A 3-year survey of Italian honeybee-collected pollen reveals widespread contamination by agricultural pesticides
Sci. Total Environ.
Transformation dynamics of the natural cover in the dry chaco ecoregion: A plot level geo-database from 1976 to 2012
J. Arid Environ.
Chronic exposure to glyphosate induces transcriptional changes in honey bee larva: a toxicogenomic study
Environ. Poll.
Agroindustry Secretary, Ministry of Production and Labor, Argentina
Expansión de la soja y diversidad de la agricultura argentina
Ecol. Austral
Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification
Glob. Change Biol.
Diet effects on honeybee immunocompetence
Biol. Lett.
Análisis polínico de mieles de la región chaqueña: comparación del origen floral entre las zonas: domo central y esteros, cañadas y selvas de ribera
Revista de Investigaciones Agropecuarias
Sector apícola 2013. Informe de coyuntura 3
Impact of nutritional stress on the honeybee colony health
Sci. Rep.
Nutrition and health in honey bees
Apidologie
Biogeografía de América Latina. Washington DC: Programa Regional de Desarrollo Científico y Tecnológico
De granero a aceitera del mundo. Las exportaciones agrarias argentinas entre 1930 y 1970
Agroalimentaria
Pollinator dependence of Argentinean agriculture: current status and temporal analysis
Am. J. Plant Sci. Biotechnol.
Protein and amino acid requirements of the honeybee (Apis mellifera L.)
Physiol. Comp. Oecol.
Influence of pollen nutrition on honeybee health: Do pollen quality and diversity matter?
PLoS One
Variations in the availability of pollen resources affect honeybee health
PLoS One
Native habitat mitigates feast–famine conditions faced by honeybee in an agricultural landscape
Proc. Natl. Acad. Sci. U. S. A.
Interacting stressors matter: diet quality and virus infection in honeybee health
R. Soc. Open Sci.
Pollen contaminated with field-relevant levels of cyhalothrin affects honeybee survival, nutritional physiology, and pollen consumption behaviour
J. Econ. Ento.
Intensively cultivated landscape and varroa mite infestation are associated with reduced honeybee nutritional state
PLoS One
Con la soja al cuello: Crónicas de un país hambriento productor de divisas
Manejo del boom de la soya: Dos escenarios sobre la expansión de la producción de la soya en América del Sur. AID Environment
Effect of honeybee on yield of three soybean cultivars
Crop Sci.
Soya-bean flowers: nectary ultrastructure, nectar guides, and orientation on the flower by foraging honeybee
J. Apic. Res.
Commission Implementing Regulation (EU) 2018/783, 2018/784 and 2018/785. Off. J. Eur. Union
Food and Agriculture Organization Corporate Statistical Database
Stages of Soybean Development, Special Report 80
La apicultura argentina y sus regiones. Una visión panorámica. Consejo Federal de Inversiones
Declaración de la ciudad de Montevideo. Congreso Latinoamericano de Apicultura
Can we feed the world & sustain the planet?
Sci. Am.
Seguridad alimentaria, medioambiente y nuestros hábitos de consumo
Ecol. Austral
Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s
Proc. Natl. Acad. Sci. U. S. A.
Bee declines driven by combined stress from parasites, pesticides, and lack of flowers
Science
Agriculture expansion and deforestation in seasonally dry forests of north-west Argentina
Environ. Conserv.
Honey bee nutrition
Annu. Rev. Entomol.
A common pesticide decreases foraging success and survival in honeybee
Science
Optimum protein levels required by honeybee (Hymenoptera, Apidae) to initiate and maintain brood rearing
Apidologie
Effects of field-realistic doses of glyphosate on honeybee appetitive behaviour
J. Exp. Biol.
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