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.
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
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
Bartomeus I, Gagic V, Bommarco R (2015) Pollinators, pests and soil properties interactively shape oilseed rape yield. Basic Appl Ecol 16(8):737–745
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
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
Brummer EC (1998) Diversity, stability, and sustainable American agriculture. Agron J 90(1):1–2
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
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
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
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
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
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
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
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
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
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
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
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
Jackson JE (2003) The biology of apples and pears. Cambridge University Press, Cambridge, pp 268–317
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
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
Maccagnani B, Burgio G, Stanisavljevic LZ, Maini S (2007) Osmia cornuta management in pear orchards. Bull Insectol 60(1):77
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
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
Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277(5325):504–505
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
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
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
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
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
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
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for statistical computing, Vienna URL https://www.R-project.org/
Ruel JJ, Ayres MP (1999) Jensen’s inequality predicts effects of environmental variation. Trends Ecol Evol 14(9):361–366
Tamburini G, Berti A, Morari F, Marini L (2016) Degradation of soil fertility can cancel pollination benefits in sunflower. Oecologia 180(2):581–587
Tamburini G, Lami F, Marini L (2017) Pollination benefits are maximized at intermediate nutrient levels. Proc R Soc B Biol Sci 284(1860):20170729
Tilman D (1999) Global environmental impacts of agricultural expansion: the need for sustainable and efficient practices. Proc Natl Acad Sci 96(11):5995–6000
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
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
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
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
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13744-020-00763-0