Skip to main content

Advertisement

SpringerLink
Log in

Insect Pollination, More than Plant Nutrition, Determines Yield Quantity and Quality in Apple and Pear

  • Insect Pollinators
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

Agricultural yield is the result of multiple factors and ecological processes (e.g., pollination, fertilization, pest control). Understanding how the different factors interact is fundamental to designing management practices aimed to increase these yields, which are environmental friendly and sustainable over time. In this study, we focus on insect pollination and plant nutrition status, since they are two key factors that influence crop yield. The study was carried out in Northwest Patagonia Argentina, which is an area of intensive production of pears and apples of global importance, during the harvest seasons 2018 and 2019. The plant nutrition was estimated from leaf chlorophyll content. Biotic pollination benefits were evaluated by comparing fruit quantity (fruit to flower ratio) and quality (weight, size, and sugar concentration) from approximately 25 flowers exposed to pollinators and 25 flowers excluded to them per tree (a total of 160 apple trees and 130 pear trees). In addition, we estimated the visitation rate of pollinators to flowers and related it to fruit quality in apple. Despite different floral characteristics, we found in both crops a positive effect of insect pollination in both the quantity and the quality of the fruits. Interestingly, the nutrition of the trees, although variable, did not affect either the quantity or the quality of the fruits. Despite the weak effect of nutrition, we found no interaction between pollination and plant nutrition (i.e., additive effects). These results highlight the importance of agricultural practices that promote pollinators on farms.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig 1
Fig 2
Fig 3
Fig 4

Similar content being viewed by others

References

  • Aizen MA, Aguiar S, Biesmeijer JC, Garibaldi LA, Inouye DW, Jung C et al (2019) Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification. Glob Chang Biol. https://doi.org/10.1111/gcb.14736

  • Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88(2):271–281

    Article  PubMed  Google Scholar 

  • Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19(11):915–918

    Article  CAS  PubMed  Google Scholar 

  • Bartomeus I, Gagic V, Bommarco R (2015) Pollinators, pests and soil properties interactively shape oilseed rape yield. Basic Appl Ecol 16(8):737–745

    Article  Google Scholar 

  • Barton K (2018). MuMIn: multi-model inference. R package version 1.40.4. https://CRAN.R-project.org/package=MuMIn

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67(1):1–48. https://doi.org/10.18637/jss.v067.i01

    Article  Google Scholar 

  • Boreux V, Kushalappa CG, Vaast P, Ghazoul J (2013) Interactive effects among ecosystem services and management practices on crop production: pollination in coffee agroforestry systems. Proc Natl Acad Sci 110(21):8387–8392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brummer EC (1998) Diversity, stability, and sustainable American agriculture. Agron J 90(1):1–2

    Article  Google Scholar 

  • Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol. https://doi.org/10.1007/s00265-010-1029-6

  • Dag A, Stern RA, Shafir S (2005) Honey bee (Apismellifera) strains differ in apple (Malus domestica) pollen foraging preference. J Apic Res 44(1):15–20

    Article  Google Scholar 

  • Dar MA, Wani JA, Raina SK, Bhat MY, Malik MA (2015) Relationship of leaf nutrient content with fruit yield and quality of pear. J Environ Biol 36(3):649

    CAS  Google Scholar 

  • Díaz PC, Arenas A, Fernández VM, Susic Martin C, Basilio AM, Farina WM (2013) Honeybee cognitive ecology in a fluctuating agricultural setting of apple and pear trees. Behav Ecol 24(5):1058–1067

    Article  Google Scholar 

  • Dris R, Niskanen R, Fallahi E (1999) Relationships between leaf and fruit minerals and fruit quality attributes of apples grown under northern conditions. J Plant Nutr 22(12):1839–1851

    Article  CAS  Google Scholar 

  • Esparza G, DeJong TM, Weinbaum SA, & Klein I (2001). Effects of irrigation deprivation during the harvest period on yield determinants in mature almond trees. Tree Physiology, 21(14), 1073–1079. https://doi.org/10.1093/treephys/21.14.1073

  • Farkas A, Orosz-Kovács Z (2003) Nectar secretion dynamics of Hungarian local pear cultivars. Plant Syst Evol 238(1–4):57–67

    Article  Google Scholar 

  • Free JB (1993). Insect pollination of crops (No. Ed. 2). Academic press, p 684

  • Free JB, Williams IH (1974) Influence of the location of honeybee colonies on their choice of pollen sources. J Appl Ecol 11(3):925. https://doi.org/10.2307/2401754

    Article  Google Scholar 

  • Garibaldi LA, Andersson GK, Requier F, Fijen TP, Hipólito J, Kleijn D, …, & Rollin O (2018). Complementarity and synergisms among ecosystem services supporting crop yield. Global Food Security, 17, 38–47

  • Garratt MP, Breeze TD, Jenner N, Polce C, Biesmeijer JC, Potts SG (2014) Avoiding a bad apple: insect pollination enhances fruit quality and economic value. Agric Ecosyst Environ 184:34–40

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geslin B, Aizen MA, Garcia N, Pereira AJ, Vaissière BE, Garibaldi LA (2017) The impact of honey bee colony quality on crop yield and farmers’ profit in apples and pears. Agric Ecosyst Environ 248:153–161

    Article  Google Scholar 

  • Gils S, Putten WH, Kleijn D (2016) Can above-ground ecosystem services compensate for reduced fertilizer input and soil organic matter in annual crops? J Appl Ecol 53(4):1186–1194

    Article  Google Scholar 

  • González-Varo JP, Biesmeijer JC, Bommarco R, Potts SG, Schweiger O, Smith HG, Steffan-Dewenter I, Szentgyörgyi H, Woyciechowski M, Vilà M (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28(9):524–530

    Article  PubMed  Google Scholar 

  • Groeneveld JH, Tscharntke T, Moser G, Clough Y (2010) Experimental evidence for stronger cacao yield limitation by pollination than by plant resources. Perspect Plant Ecol Evol Syst 12(3):183–191

    Article  Google Scholar 

  • Hoying S, Fargione M, Iungerman K (2004) Diagnosing apple tree nutritional status: leaf analysis interpretation and deficiency symptoms. N YFruit Q 12(11):16–19

    Google Scholar 

  • Jackson JE (2003) The biology of apples and pears. Cambridge University Press, Cambridge, pp 268–317

    Book  Google Scholar 

  • Klein AM, Hendrix SD, Clough Y, Scofield A, Kremen C (2015) Interacting effects of pollination, water and nutrients on fruit tree performance. Plant Biol 17(1):201–208

    Article  PubMed  Google Scholar 

  • Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B: biological sciences 274(1608):303–313

    Article  PubMed  Google Scholar 

  • Maccagnani B, Burgio G, Stanisavljevic LZ, Maini S (2007) Osmia cornuta management in pear orchards. Bull Insectol 60(1):77

    Google Scholar 

  • Maccagnani B, Ladurner E, Santi F, Burgio G (2003) Osmia cornuta (Hymenoptera, Megachilidae) as a pollinator of pear (Pyrus communis): fruit-and seed-set. Apidologie 34(3):207–216

    Article  Google Scholar 

  • Marini L, Tamburini G, Petrucco-Toffolo E, Lindström SA, Zanetti F, Mosca G, Bommarco R (2015) Crop management modifies the benefits of insect pollination in oilseed rape. Agric Ecosyst Environ 207:61–66

    Article  Google Scholar 

  • Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277(5325):504–505

    Article  CAS  PubMed  Google Scholar 

  • Neilsen D, Hogue EJ, Neilsen GH, Parchomchuk P (1995) Using SPAD-502 values to assess the nitrogen status of apple trees. HortScience 30(3):508–512

    Article  Google Scholar 

  • Neilsen GH, Neilsen D, Ferree DC, Warrington IJ (2003) Nutritional requirements of apple. In: Ferree DC, Warrington IJ (eds) Apples: botany, Production and Uses. CABI Publishing, Wallingford, pp 267–302

    Chapter  Google Scholar 

  • Neto CB, Carranca C, Clemente J, de Varennes A (2011) Assessing the nitrogen nutritional status of young non-bearing ‘rocha’pear trees grown in a mediterranean region by using a chlorophyll meter. J Plant Nutr 34(5):627–639

    Article  CAS  Google Scholar 

  • Porro D, Dorigatti C, Stefanini M, Ceschini A (2001) Use of spad meter in diagnosis of nutritional status in apple and grapevine. Acta Hortic 564:243–252

    Article  CAS  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010a) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353

    Article  PubMed  Google Scholar 

  • Potts SG, Roberts SP, Dean R, Marris G, Brown MA, Jones R, ... & Settele J (2010b). Declines of managed honey bees and beekeepers in Europe. J Apic Res, 49(1), 15–22

  • Ramírez F, Davenport TL (2013) Apple pollination: a review. Sci Hortic 162:188–203

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna URL https://www.R-project.org/

    Google Scholar 

  • Ruel JJ, Ayres MP (1999) Jensen’s inequality predicts effects of environmental variation. Trends Ecol Evol 14(9):361–366

    Article  CAS  PubMed  Google Scholar 

  • Tamburini G, Berti A, Morari F, Marini L (2016) Degradation of soil fertility can cancel pollination benefits in sunflower. Oecologia 180(2):581–587

    Article  PubMed  Google Scholar 

  • Tamburini G, Lami F, Marini L (2017) Pollination benefits are maximized at intermediate nutrient levels. Proc R Soc B Biol Sci 284(1860):20170729

    Article  Google Scholar 

  • Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci 96(11):5995–6000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vicens N, Bosch J (2000) Pollinating efficacy of Osmia cornuta and Apis mellifera (Hymenoptera: Megachilidae, Apidae) on ‘Red Delicious’ apple. Environ Entomol 29(2):235–240

    Article  Google Scholar 

Download references

Acknowledgments

We thank owners and managers of the farms for opening their doors. We also want to thank Néstor Pérez-Méndez who made valuable comments on the previous version of the manuscript and to Adrián González Chaves, Maria Ramos, Dulce Gómez Carella, Tatiana Machado de Souza, Eduardo Moreira, Rafaela Santos, Alberto Girotto, Joana Ferreira, and Grecia de Groot who assisted in the field.

Funding

This work was financially supported by the Agencia Nacional de Promoción Científica y Tecnológica (PICT 2015-2333).

Author information

Authors and Affiliations

  1. Univ Nacional de Río Negro, Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural, San Carlos de Bariloche, Río Negro, Argentina

    P L Hünicken & L A Garibaldi

  2. Consejo Nacional de Investigaciones Científicas y Técnicas, Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural, San Carlos de Bariloche, Río Negro, Argentina

    P L Hünicken & L A Garibaldi

  3. Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural, Sede Andina, UNRN, Viedma, Argentina

    P L Hünicken & L A Garibaldi

  4. Instituto Biodiversidad y Medio Ambiente (INIBIOMA), Univ Nacional del Comahue-CONICET, Grupo de Ecología de la Polinización, San Carlos de Bariloche, Río Negro, Argentina

    C L Morales

  5. Centro PYME, Agencia de Desarrollo Económico del Neuquén, Neuquén, Argentina

    N García

Authors
  1. P L Hünicken
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C L Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. N García
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L A Garibaldi
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LAG and PLH conceived the idea and designed the study. PLH and NG collected the data. PLH analyzed the data with substantial inputs from LAG. PLH, LAG, and CLM led the writing of the manuscript. All authors gave final approval for publication.

Corresponding author

Correspondence to P L Hünicken.

Additional information

Edited by Claudia Inês Silva – UNESP

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Materials

ESM 1

(DOC 74 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hünicken, P.L., Morales, C.L., García, N. et al. Insect Pollination, More than Plant Nutrition, Determines Yield Quantity and Quality in Apple and Pear. Neotrop Entomol 49, 525–532 (2020). https://doi.org/10.1007/s13744-020-00763-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-020-00763-0

Keywords

Search

Navigation