Review
Pollination contribution to crop yield is often context-dependent: A review of experimental evidence

https://doi.org/10.1016/j.agee.2019.04.022Get rights and content

Highlights

  • Soil properties and crop pests affect pollination contribution to yield.

  • Pollination and concomitant services often display synergistic relationships.

  • Crop traits might influence plant response to resource and pollen availability.

Abstract

Insect pollination is a well-studied ecosystem service that supports production in 75% of globally important crops. Although yield is known to be sustained and regulated by a bundle of ecosystem services and management factors, the contribution of pollination to yield has been mostly studied in isolation. Here, we compiled and reviewed research on the contribution of pollination to crop yield under different environmental conditions, where the potential interaction between pollination and other factors contributing to yield, such as nutrient availability and control of pests, was tested. Specifically, we explored whether pollination displayed synergistic, compensatory or additive effects with concomitant factors. The literature search resulted in 24 peer-reviewed studies for a total of 39 individual tests of interactions. Studies examined responses in 13 crops testing interactions both at the local and the landscape scale. Interactions between pollination and other factors influencing yield were observed for several crops and mostly displayed positive-synergistic relationships. Crop life-history traits such as pollination dependency were found to affect the plant response to variations in resource and pollen availability. Soil properties and crop pests might affect contribution of pollination to yield by altering the amount of resources a plant can allocate to reproduction, independently of the amount of pollen provided. Current management strategies to enhance pollinators might fail to increase pollination benefits in landscapes characterized by poor soil resources or ineffective pest control. We propose that our understanding of the effects of crop-pollinator interactions will benefit by focusing on plant traits and physiological responses. Combining knowledge from plant physiology and ecology with technological advances in agriculture is needed to design novel management strategies to maximize pollination benefits and support yields and reduce environmental impacts of food production.

Section snippets

Introduction: pollination benefits in agriculture

Supporting yields while minimizing negative environmental impacts of agriculture is a major challenge of our century. There are numerous biotic and abiotic factors that influence crop growth and yields, as well as their potential interactions (Lobell et al., 2009). The contribution of these factors in closing yield gaps can be enhanced by improving agronomic management (e.g. irrigation, fertilization, plant breeding, integrated pest management) and/or by integrating bundles of ecosystem

Methods: literature review and dataset investigation

We conducted a literature review consulting the online reference database ISI Web of Science (for details about selection criteria and process see Fig. S1). We selected all peer-reviewed studies where yield response to insect pollination (pollination benefits) was measured in crops and related to the experimental manipulation of at least one other concomitant ES or management factor below and/or above ground. Concomitant ES and management factors were usually quantified as the beneficial

General trends

First, we present the general patterns that emerged from the selected literature. Second, we discuss individual studies for soil factors and pest control, separately. Third, we explore the potential mechanisms driving interactions between pollination and concomitant factors.

The literature search resulted in 24 peer-reviewed studies for a total of 39 individual statistical tests of interactions (Tables 1 and S2). All the studies were published since 2004 and 80% was published since 2013. Studies

Potential mechanisms driving interactions between pollination and concomitant factors

Pollination and its contribution to seed formation is connected to plant physiological processes (Knight et al., 2005). We therefore suggest to explore how concomitant ES, crop management and crop life history traits alter resource availability for reproduction and resource allocation strategies in order to better understand the mechanisms driving the variability of pollination benefits in crop production.

Methodological approaches to study interactions

Understanding of how complex combinations of ES and management factors might affect pollination benefits will require several complementary approaches. Below, we review the weaknesses and strengths of the methodological approaches that have been used.

Study limitation and research gaps

Our review explores a recently emerged field of applied ecological research. The main limitation of our study is consequently the limited number of studies available on the topic. Moreover, the selected studies were performed in different cropping systems and with different experimental approaches, which is reflected in the variability of interactions observed. Nevertheless, the patterns emerged clearly show the importance of considering context dependency when managing pollination services and

Conclusions: implications for management

We found interactions between pollination and other factors influencing yield to be prevalent across several crops and mostly displaying positive-synergistic relationships. Soil properties and crop pests are expected to affect the contribution of pollination to yield by altering the amount of resources a plant can allocate to reproduction, independently of the amount of pollen provided. However, strategies to counteract pollination deficiency in crops have mainly consisted of interventions to

Acknowledgements

The research leading to these results has received funding from the European Community's Seventh Framework Programme under grant agreement no 311781, LIBERATION Project (www.fp7liberation.eu).

References (70)

  • E.L. Korpela et al.

    Can pollination services, species diversity and conservation be simultaneously promoted by sown wildflower strips on farmland?

    Agric. Ecosyst. Environ.

    (2013)
  • D. Lucas–Barbosa

    Integrating studies on plant–pollinator and plant–herbivore interactions

    Trends Plant Sci.

    (2016)
  • L. Marini et al.

    Crop management modifies the benefits of insect pollination in oilseed rape

    Agric. Ecosyst. Environ.

    (2015)
  • T. Perrot et al.

    Bees increase oilseed rape yield under real field conditions

    Agric. Ecosyst. Environ.

    (2018)
  • D.S. Powlson et al.

    Soil management in relation to sustainable agriculture and ecosystem services

    Food Policy

    (2011)
  • A. St–Martin et al.

    Soil compaction and insect pollination modify impacts of crop rotation on nitrogen fixation and yield

    Basic Appl. Ecol.

    (2016)
  • G. Tamburini et al.

    Drought and soil fertility modify fertilization effects on aphid performance in wheat

    Basic Appl. Ecol.

    (2018)
  • M. Toledo-Hernández et al.

    Neglected pollinators: can enhanced pollination services improve cocoa yields? A review

    Agric. Ecosyst. Environ.

    (2017)
  • W. Zhang et al.

    Ecosystem services and dis–services to agriculture

    Ecol. Econ.

    (2007)
  • N.A. Barber et al.

    Effects of above–and belowground herbivory on growth, pollination, and reproduction in cucumber

    Oecologia

    (2011)
  • N.A. Barber et al.

    Herbivory reduces plant interactions with above‐and belowground antagonists and mutualists

    Ecology

    (2012)
  • I. Bartomeus et al.

    Contribution of insect pollinators to crop yield and quality varies with agricultural intensification

    PeerJ

    (2014)
  • B.R. Blaauw et al.

    Flower plantings increase wild bee abundance and the pollination services provided to a pollination‐dependent crop

    J. Appl. Ecol.

    (2014)
  • A.J. Bloom et al.

    Resource limitation in plants–an economic analogy

    Annu. Rev. Ecol. Syst.

    (1985)
  • V. Boreux et al.

    Interactive effects among ecosystem services and management practices on crop production: pollination in coffee agroforestry systems

    Proc. Natl. Acad. Sci. U. S. A.

    (2013)
  • M.M. Bos et al.

    Caveats to quantifying ecosystem services: fruit abortion blurs benefits from crop pollination

    Ecol. Appl.

    (2007)
  • M. Burd

    The Haig-Westoby model revisited

    Am. Nat.

    (2008)
  • L.G. Carvalheiro et al.

    Natural and within‐farmland biodiversity enhances crop productivity

    Ecol. Lett.

    (2011)
  • D.R. Campbell et al.

    Resource and pollen limitations to lifetime seed production in a natural plant population

    Ecology

    (1993)
  • A. Classen et al.

    Complementary ecosystem services provided by pest predators and pollinators increase quantity and quality of coffee yields

    Proc. R. Soc. Lond. B Biol. Sci.

    (2014)
  • D.M. Finney et al.

    Functional diversity in cover crop polycultures increases multifunctionality of an agricultural system

    J. Appl. Ecol.

    (2017)
  • S.J. Forbes et al.

    Increased pollinator habitat enhances cacao fruit set and predator conservation

    Ecol. Appl.

    (2017)
  • L.A. Garibaldi et al.

    Wild pollinators enhance fruit set of crops regardless of honey bee abundance

    Science

    (2013)
  • L.A. Garibaldi et al.

    From research to action: enhancing crop yield through wild pollinators

    Front. Ecol. Environ.

    (2014)
  • L.A. Garibaldi et al.

    Incremental contribution of pollination and other ecosystem services to agricultural productivity

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