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Organic farming improves pollination success in strawberries.
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PMID:  22355380     Owner:  NLM     Status:  MEDLINE    
Pollination of insect pollinated crops has been found to be correlated to pollinator abundance and diversity. Since organic farming has the potential to mitigate negative effects of agricultural intensification on biodiversity, it may also benefit crop pollination, but direct evidence of this is scant. We evaluated the effect of organic farming on pollination of strawberry plants focusing on (1) if pollination success was higher on organic farms compared to conventional farms, and (2) if there was a time lag from conversion to organic farming until an effect was manifested. We found that pollination success and the proportion of fully pollinated berries were higher on organic compared to conventional farms and this difference was already evident 2-4 years after conversion to organic farming. Our results suggest that conversion to organic farming may rapidly increase pollination success and hence benefit the ecosystem service of crop pollination regarding both yield quantity and quality.
Georg K S Andersson; Maj Rundlöf; Henrik G Smith
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Type:  Journal Article; Research Support, Non-U.S. Gov't     Date:  2012-02-15
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Title:  PloS one     Volume:  7     ISSN:  1932-6203     ISO Abbreviation:  PLoS ONE     Publication Date:  2012  
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Created Date:  2012-02-22     Completed Date:  2012-06-18     Revised Date:  2013-06-26    
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Nlm Unique ID:  101285081     Medline TA:  PLoS One     Country:  United States    
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Languages:  eng     Pagination:  e31599     Citation Subset:  IM    
Centre for Environmental and Climate Research, Lund University, Lund, Sweden.
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MeSH Terms
Fragaria / growth & development*
Organic Agriculture*

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Journal ID (nlm-ta): PLoS One
Journal ID (publisher-id): plos
Journal ID (pmc): plosone
ISSN: 1932-6203
Publisher: Public Library of Science, San Francisco, USA
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Andersson et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Received Day: 30 Month: 9 Year: 2011
Accepted Day: 12 Month: 1 Year: 2012
collection publication date: Year: 2012
Electronic publication date: Day: 15 Month: 2 Year: 2012
Volume: 7 Issue: 2
E-location ID: e31599
ID: 3280308
PubMed Id: 22355380
Publisher Id: PONE-D-11-19214
DOI: 10.1371/journal.pone.0031599

Organic Farming Improves Pollination Success in Strawberries Alternate Title:Organic Farming Improves Pollination
Georg K. S. Andersson12*
Maj Rundlöf23
Henrik G. Smith12
Dorian Q. Fulleredit1 Role: Editor
1Centre for Environmental and Climate Research, Lund University, Lund, Sweden
2Department of Biology, Lund University, Lund, Sweden
3Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden
University College London, United Kingdom
Correspondence: * E-mail:
Contributed by footnote: Conceived and designed the experiments: GA HS MR. Performed the experiments: GA. Analyzed the data: GA HS MR. Contributed reagents/materials/analysis tools: GA HS MR. Wrote the paper: GA HS MR.


Agricultural intensification, resulting in loss and degradation of natural and semi-natural habitats, threatens biodiversity [1], [2], [3] and associated ecosystem services [4], [5]. Pollination provided by wild pollinators can increase crop production and benefit wild plants [6], though recent declines in pollinator numbers has been suggested as one reason for pollination deficiency in crops ([6], [7] but see [8]). Although the major crops are not dependent on pollinators, large proportions of human nutrient supply come from pollinator dependent crops [9]. Hence it is important to understand how pollinators and pollination in the agricultural landscapes can be enhanced.

Organic farming has been proposed to be a means to alleviate the decreasing biodiversity in agricultural landscapes [10], [11], [12]. It mainly differs from conventional farming by the prohibition of most pesticides and inorganic fertilisers [13], necessitating more elaborate crop-rotations such as the use of nitrogen-fixing plants [14]. Organic farming has been shown to affect biodiversity of several taxonomic groups [15], [16], [17], [18], but effect strength and direction can vary with taxonomic group [19], scale [12] and landscape context [16]. However, current results suggest that management effects benefiting biodiversity may not necessarily translate into improved ecosystem services [20].

Pollinator diversity and abundance often benefit from organic farming [21], [22], [23], which may lead to improved pollination [17], [24], [25]. However, how pollination is influenced by farming practice is not thoroughly understood and studies have generated contrasting results [7], [26], [27], [28]. Effects of organic farming on pollination are not necessary simply related to pollinator richness or abundance as pollination rates may be modified by e.g. community composition, visitation frequencies, and foraging behaviour. Therefore it is important to first understand if the effects of organic farming on pollinator diversity and abundance translate into enhanced crop pollination, and then further examine the causes.

Past land-use can affect biodiversity during shorter or longer transition periods [29], [30], suggesting that there may be a time-lag between land-use change and resulting changes in biodiversity and abundance [30], [31]. The time-lag effect can have two main causes. First, time-lags may arise as a consequence of that organisms respond slowly to changes in habitat extension, distribution and quality, e.g. by slow dispersal, slow reproduction or both [32]. Second, diversity can respond to physical properties of the environment that change slowly themselves under the new regime, e.g. slow build-up of carbon in soil or formation of new patches of habitats. For example, a recent study showed such temporal patterns for transition time to organic farming on butterfly abundance [33]. This was attributed to a possible low carrying capacity of arable land for butterflies and a hence a steady slow increase in abundance over years with habitat improvement. Hence it can be hypothesized that effects of organic farming on pollination may not immediately be evident after conversion to organic farming. To our knowledge, this hypothesis has not been empirically tested.

We studied the effects of transition from conventional to organic farming on the pollination of strawberries, a crop that benefits from biotic pollination[34], [35], [36] and is visited by a wide range of pollinators, e.g. hoverflies and wild bees [37]. The main questions were (i) is the pollination success in strawberries higher on organic compared to conventional farms and (ii) is there a time-lag effect in pollination success since transition to organic farming.


All necessary permits were obtained for the described field studies. The farmers, on whose properties we conducted the study, were informed about, and approved, the studies before they started. The study was conducted on 12 farms in Scania, the southernmost part of Sweden, in 2009. Circular landscapes with a radius of 1 km around farms were digitized using ArcGIS 9.2 and characterized with information from the Integrated Administration and Control System, IACS, a database for agricultural land-use in Sweden administrated by the Swedish Board of Agriculture. We described land-use intensity using an index calculated as the proportion of annual crops and ley of all farmland and forest within the circular landscape, excluding e.g. urban areas and lakes. The index therefore reflects the proportion of the landscape under intensive cultivation. To avoid bias, in terms of organic farming being more common in complex landscapes [16], we selected all farms in landscapes where the proportion of intensively cultivated land was at least 70%.

The twelve farms were either conventionally managed (n = 4), recently transformed to organic farming (“new”, 2–4 years; n = 4) or under organic management for a longer time period (“old”, 14–24 years; n = 4). The organic farms were certified according to the Swedish certification organisation for organic products, KRAV, which mainly follows the European Council Regulation [13]. To assess pollination we established strawberry (Fragaria ananassa) plants as phytometers which we placed in 7.5 litre pots adjacent to field borders of spring wheat or barley to minimize the crop influence on pollinators. We placed the pots halfway down in the ground to reduce water loss and watered them when necessary. This method makes it possible to control for potential confounding factors such as soil-type. To make cross-pollination possible four pots of strawberries were used at each farm and placed just far enough to prevent the flowers to come into physical contact with each other. We used strawberries for two main reasons. First, a strawberry is an aggregated fruit where the pollination success can be assessed on each strawberry. This means that pollination success can be measured independent of total fruit set and thereby all variables apart from pollination success that may influence total fruit set. Strawberry pollination success is also increased by insect pollination [34], [35], [36]. Second, strawberries are an economically important crop in Sweden. We further address these issues in the discussion.

The phytometers were placed outside between June 2nd and August 8th, to allow visitation of native pollinators in the study landscapes. None of our farms had managed honeybees on them. The flowering period lasted from June 5th to July 3rd and all fully ripe strawberries were continuously collected. Pollination success was estimated by counting the numbers of malformations on each strawberry and the proportion of fully pollinated berries per farm. These malformations are formed when ovaries are not fertilised. The area of the receptacle holding these ovaries does then not swell up which results in a malformed strawberry [36]. The malformations we counted are thus areas of unfertilized achenes, or seeds, on the mature strawberry corresponding to the unpollinated stigmas and unfertilised ovaries, on the flower. On average 18.9±2.1 (SE) strawberries per farm were collected and counted for malformations.

We analysed pollination success (mean number of miss-formation and proportion fully pollinated strawberries) in relation to farming practice (conventional vs. organic) and in relation to age category (new organic vs. old organic) in R ver. 2.13.1 [38]. First, the overall difference between the three categories was tested in an ANOVA. Then we used a priori contrasts to test, first the difference between conventional and organic farming, and second the difference between new and old organic farms. To test the proportion of fully pollinated strawberries we used a generalized linear model assuming binomial error followed by same a priori contrast tests as above.


The global ANOVA model showed a significant effect of farming practice (conventional, new organic, old organic) on mean number of malformations (F2,8 = 7.5, p = 0.015). The mean number of malformations on strawberries was lower on organic farms (0.63±0.089; mean ± SE), compared to conventional farms 1.26±0.14 (t8 = −3.74, p = 0.0057; Fig. 1). There was also an effect of farming practice on the proportion of fully pollinated berries (z10 = 2.86, p = 0.0043) with a higher proportion of fully pollinated berries on organic farms (0.45±0.081) compared to conventional farms 0.17±0.037 (z10 = 2.77, p = 0.0055; Fig. 2). The number of malformations did not differ between new (0.71±0.08) and old (0.54±0.16) organic farms (t8 = −0.96, p = 0.37), nor did the proportion fully pollinated berries, 0.40 and 0.51 on new and old organic farms, respectively (z = −1.14, p = 0.26).


Pollination potential in strawberries was significantly higher on organic compared to conventional farms, shown by the fewer malformations on berries and a higher proportion of fully pollinated berries. However, we found no effect of time since transition to organic farming on either the number of malformations or the proportion of fully pollinated strawberries. This suggests that the increase in pollination success occurs already within a few years after conversion to organic farming. As butterfly and plant species richness has been found to increase rapidly after transition to organic farming [33], our result suggest that pollinator richness may respond rapidly as well.

The few studies previously examining the effect of organic farming on seed-set, some of which has been on wild plants [17], [39], have found varied results. Turnip rape-seed on organic farms had less pollination deficit than rape-seed on conventional farms [27] whereas seed-set in petunias did not differ between farming practices [26]. Strawberries, as an aggregate fruit, allowed us to assess pollination on each individual berry and consequently compare the actual pollination success between farms. A caveat when estimating pollination success on plants with non-aggregate fruits is that a number of factors other than pollination can influence seed set. Non-aggregated fruits, or simple fruits, can have many seeds but they come from a flower with only one pistil. Thus, as each seed can be affected by predation, be aborted or just not develop for various reasons, it is harder to relate the number off seeds in such types of fruits to the pollination success. Aggregate fruits come from one flower with many pistils where every ovary forms one seed, in strawberries an achene. This has the advantage that, as in the case of the strawberries, each individual strawberry, shows the pollination success. In our study 45% of the strawberries were fully pollinated on organic farms with only 17% being fully pollinated on conventional ones. In one earlier study [7] watermelons were found to receive sufficient pollen deposition to allow production of fully developed fruits on every second organic farm, but not on any conventional farm. However, no significant difference between farming practices in pollination services remained after accounting for isolation from natural habitats [7]. In the present study any confounding landscape factors were explicitly controlled for in the design of the field experiments.

Possible explanations for the higher pollination success may be a higher abundance, visitation frequency or a higher diversity of pollinators, which has been shown to be supported by organic farms [22], [23]. Several studies suggest a correlation between pollinator diversity and fruit-set [24], [40], [41]. However, in strawberries, the influence of farming practice on pollination success may not result from a higher diversity of pollinators per se at organic farms, but may be a consequence of community composition of pollinators [7]. Chagnon et al. [42] showed that the quality of strawberries is affected by the composition of pollinator communities, with large- and average-sized apoids pollinating the top and small-sized apoids pollinating the bottom and sides of strawberries. However, single visits by honeybees, large hoverflies and small solitary bees contributed equally to pollination of strawberries [34] indicating that no group alone is most important. Based on our results it remains to be tested if there is a higher number of functionally important pollinator groups at organic farms or if other explanations, such as an increase in pollinator abundance, can account for the increased pollination success.

Our results suggest that increased pollination success mediated by organic farming may increase both crop yield quantity and quality on farms growing strawberries. This is economically important since approximately 11 000 tonnes of strawberries are produced annually in Sweden according to Swedish board of Agriculture statistics, 2011 and 40 million tonnes globally [43]. However, since we use phytometers, our results are not directly related to estimates of differences in crop pollination at a farm scale. First, we did not determine if strawberry plants compensate for low pollination success by e.g. producing more berries. Second, the effects may be scale-dependent hence farms with whole fields of strawberries the pattern in relation to farming practice may be different compared to a limited number of strawberry plants. In order to link our results to production in strawberry fields, simultaneous measurements of pollination in both fields and phytometers will be required.

To further determine the relationship between farming practice and the functions pollinators provide enhances our understanding of measures needed to preserve pollinators. Although the mechanistic cause for the observed differences in pollination success between farming practices remains unknown in our study, effects were present at recently transformed farms. Combined with results on other ecosystem services, our results imply that agri-environment schemes should be evaluated both directly after implementation and over a longer term.


Competing Interests: The authors have declared that no competing interests exist.

Funding: This work was supported by The Swedish Reseasrch Council FORMAS:; Grant number in 2009: 1680. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

We thank the farmers for letting us work on their fields and the field assistants for invaluable support. Thanks also to Johan Ekroos and Klaus Birkhofer for valuable comments and suggestions on the manuscript.

1. Kleijn D,Kohler F,Baldi A,Batary P,Concepcion ED,et al. Year: 2009On the relationship between farmland biodiversity and land-use intensity in Europe.Proceedings of the Royal Society B-Biological Sciences276903909
2. Krebs JR,Wilson JD,Bradbury RB,Siriwardena GM. Year: 1999The second Silent Spring?Nature400611612
3. Potts SG,Biesmeijer JC,Kremen C,Neumann P,Schweiger O,et al. Year: 2010Global pollinator declines: trends, impacts and drivers.Trends in Ecology & Evolution2534535320188434
4. Tilman D,Fargione J,Wolff B,D'Antonio C,Dobson A,et al. Year: 2001Forecasting agriculturally driven global environmental change.Science29228128411303102
5. Geiger F,Bengtsson J,Berendse F,Weisser WW,Emmerson M,et al. Year: 2010Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland.Basic and Applied Ecology1197105
6. Klein AM,Vaissière BE,Cane JH,Steffan-Dewenter I,Cunningham SA,et al. Year: 2007Importance of pollinators in changing landscapes for world crops.Proceedings of the Royal Society B: Biological Sciences274303313
7. Kremen C,Williams NM,Thorp RW. Year: 2002Crop pollination from native bees at risk from agricultural intensification.Proceedings of the National Academy of Sciences991681216816
8. Ghazoul J,Koh LP. Year: 2010Food security not (yet) threatened by declining pollination.Frontiers in Ecology and the Environment8910
9. Eilers EJ,Kremen C,Smith Greenleaf S,Garber AK,Klein A-M. Year: 2011Contribution of Pollinator-Mediated Crops to Nutrients in the Human Food Supply.PLoS One6e2136321731717
10. Hole DG,Perkins AJ,Wilson JD,Alexander IH,Grice PV,et al. Year: 2005Does organic farming benefit biodiversity?Biological Conservation122113130
11. Rundlöf M,Edlund M,Smith HG. Year: 2010Organic farming at local and landscape scales benefits plant diversity.Ecography33514522
12. Bengtsson JN,Ahnstrom J,Weibull AC. Year: 2005The effects of organic agriculture on biodiversity and abundance: a meta-analysis.Journal of Applied Ecology42261269
13. ECCouncil Regulation (EC) on organic production and labelling of organic products and repealing.Union E2092/91834/2007Official Journal of the European Union European Council
14. Stockdale EA,Lampkin NH,Hovi M,Keatinge R,Lennartsson EKM,et al. Year: 2001Agronomic and environmental implications of organic farming systemsAdvances in AgronomyAcademic Press261262
15. Roschewitz I,Gabriel D,Tscharntke T,Thies C. Year: 2005The effects of landscape complexity on arable weed species diversity in organic and conventional farming.Journal of Applied Ecology42873882
16. Rundlöf M,Smith HG. Year: 2006The effect of organic farming on butterfly diversity depends on landscape context.Journal of Applied Ecology4311211127
17. Gabriel D,Tscharntke T. Year: 2007Insect pollinated plants benefit from organic farming.Agriculture, Ecosystems & Environment1184348
18. Smith H,Dänhardt J,Lindström Å,Rundlöf M. Year: 2010Consequences of organic farming and landscape heterogeneity for species richness and abundance of farmland birds.Oecologia1621071107920213151
19. Fuller RJ,Norton LR,Feber RE,Johnson PJ,Chamberlain DE,et al. Year: 2005Benefits of organic farming to biodiversity vary among taxa.Biology Letters143143417148225
20. Diekötter T,Wamser S,Wolters V,Birkhofer K. Year: 2010Landscape and management effects on structure and function of soil arthropod communities in winter wheat.Agriculture, Ecosystems & Environment137108112
21. Holzschuh A,Steffan-Dewenter I,Kleijn D,Tscharntke T. Year: 2007Diversity of flower-visiting bees in cereal fields: effects of farming system, landscape composition and regional context.Journal of Applied Ecology444149
22. Rundloef M,Nilsson H,Smith HG. Year: 2008Interacting effects of farming practice and landscape context on bumblebees.Biological Conservation141417426
23. Holzschuh A,Steffan-Dewenter I,Tscharntke T. Year: 2008Agricultural landscapes with organic crops support higher pollinator diversity.Oikos117354361
24. Hoehn P,Tscharntke T,Tylianakis JM,Steffan-Dewenter I. Year: 2008Functional group diversity of bee pollinators increases crop yield.Proceedings of the Royal Society B: Biological Sciences27522832291
25. Klein A-M,Steffan-Dewenter I,Tscharntke T. Year: 2003Fruit set of highland coffee increases with the diversity of pollinating bees.Proceedings of the Royal Society B: Biological Sciences270955961
26. Brittain C,Bommarco R,Vighi M,Settele J,Potts SG. Year: 2010Organic farming in isolated landscapes does not benefit flower-visiting insects and pollination.Biological Conservation14318601867
27. Morandin LA,Winston ML. Year: 2005Wild bee abundance and seed production in conventional, organic, and genetically modified canola.Ecological Applications15871881
28. Ekroos J,Hyvönen T,Tiainen J,Tiira M. Year: 2010Responses in plant and carabid communities to farming practises in boreal landscapes.Agriculture, Ecosystems & Environment135288293
29. Lindborg R,Eriksson O. Year: 2004Historical landscape connectivity affects present plant species diversity.Ecology8518401845
30. Bissonette JA,Storch I. Year: 2007Temporal Dimensions of Landscape Ecology. First edNew YorkSpringer
31. Andersson GKS,Rundlöf M,Smith HG. Year: 2010Time lags in biodiversity response to farming practices.Boatman ND,Green M,Holland J,Marshall J,Renwick A,et al.Aspects of Applied Biology; 2010; University of Leicester, Oadby, UKAssociation of Applied Biologists38138422319070
32. With KA. Year: 2007Invoking the Ghost of Landscapes Past to Understand the Landscape Ecology of the present…and the Future.Bissonette JA,Storch ITemporal Dimensions of Landscape Eology First edNew YorkSpringer4358
33. Jonason D,Andersson GKS,Öckinger E,Rundlöf M,Smith HG,et al. Year: 2011Assessing the effect of the time since transition to organic farming on plants and butterflies.Journal of Applied Ecology4854355021731110
34. Albano S,Salvado E,Duarte S,Mexia A,Borges PAV. Year: 2009Pollination effectiveness of different strawberry floral visitors in Ribatejo, Portugal: selection of potential pollinators. Part 2.Advances in Horticultural Science23246253
35. Lopez-Medina J,Palacio-Villegas A,Vazquez-Ortiz E. Year: 2006Misshaped fruit in strawberry, an agronomic evaluation.Acta Horticulturae7087778
36. Free JB. Year: 1993Insect Pollination of CropsLondonAcademic Press
37. Albano S,Salvado E,Duarte S,Mexia A,Borges PAV. Year: 2009Floral visitors, their frequency, activity rate and Index of Visitation Rate in the strawberry fields of Ribatejo, Portugal: selection of potential pollinators. Part 1.Advances in Horticultural Science23238245
38. R Development Core TeamYear: 2011R: A Language and Environment for Statistical Computing. 2.14.0 edVienna, AustriaR Foundation for Statistical Computing
39. Power EF,Stout JC. Year: 2011Organic dairy farming: impacts on insect–flower interaction networks and pollination.Journal of Applied Ecology48561569
40. Klein AM. Year: 2009Nearby rainforest promotes coffee pollination by increasing spatio-temporal stability in bee species richness.Forest Ecology and Management25818381845
41. Vergara CH,Badano EI. Year: 2009Pollinator diversity increases fruit production in Mexican coffee plantations: The importance of rustic management systems.Agriculture, Ecosystems & Environment129117123
42. Chagnon M,Gingras J,De Oliveira D. Year: 1993Complementary aspects of strawberry pollination by honey and indigenous bees (Hymenoptera).Journal of Economic Entomology86416420
43. FAO. Year: 2011Crop production database (2008).Food and Agricultural Organisation of the United Nations


[Figure ID: pone-0031599-g001]
doi: 10.1371/journal.pone.0031599.g001.
Figure 1  Mean number of malformations.

The mean number of malformations on strawberries from plants on organic and conventional farms. Boxes represent 25th and 75th of the sample, dots the median and error-bars the minimum and maximum values respectively.

[Figure ID: pone-0031599-g002]
doi: 10.1371/journal.pone.0031599.g002.
Figure 2  Proportion of fully pollinated strawberries.

The proportion of fully pollinated strawberries, i.e. having no malformations, from plants on organic and conventional farms. Boxes represent 25th and 75th of the sample, dots the median and error-bars the minimum and maximum values respectively.

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