1. bookVolume 28 (2020): Issue 1 (June 2020)
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Pollination Efficiency of Managed Bee Species (Apis mellifera and Bombus pauloensis) in Highbush Blueberry (Vaccinium corymbosum) Productivity

Pablo Cavigliasso,
Pablo Cavigliasso,
Fernando Bello,
Fernando Bello,
Maria Fernanda Rivadeneira,
Maria Fernanda Rivadeneira,
Nicolas Oscar Monzon,
Nicolas Oscar Monzon,
Gerardo Pablo Gennari and
Gerardo Pablo Gennari and
Marina Basualdo
Marina Basualdo
Published Online: 30 Jun 2020
Volume & Issue: Volume 28 (2020) - Issue 1 (June 2020)
Page range: 57 - 64
Received: 01 Sep 2019
Accepted: 01 Mar 2020
Journal of Horticultural Research's Cover Image
Journal of Horticultural Research
Journal Details
License
Format
Journal
eISSN
2353-3978
First Published
30 Jul 2013
Publication timeframe
2 times per year
Languages
English
INTRODUCTION

Bees are some of the most important insect pollinators. The evaluation of how different bee species select and use certain resources within their environment is important to understand fundamental ecological processes in agroecosystems (Gill et al. 2016; Campbell et al. 2018). In intensive agricultural areas, it has been documented that several species of wild bees are threatened and declining (Garibaldi et al. 2013; Cariveau & Winfree 2015). At the same time, the abundance of populations of managed honey bees (mostly Apis mellifera) decreases to provide services in crops with high dependence on entomophilic pollination (Agüero et al. 2018; Requier et al. 2018). Understanding how bees use the resources provided by crops of massive flowering is essential to develop meaningful agricultural management plans that both sustain bee populations and maximize the potential pollination service they may provide to farmers (Pasquet et al. 2008).

Vaccinium is a large genus of plants with many cultivated species. Blueberry (Vaccinium corymbosum L.) is a very important crop in Argentina, with more than 2700 ha cultivated. This intensive agricultural practice reduces the heterogeneity of habitats; it helps to create a large mass of homogeneous flowers and, consequently, rapidly changes the composition and diversity of pollinators (Steffan-Dewenter et al. 2005; Chacoff & Aizen 2006; Tylianakis et al. 2008).

Although some cultivars of blueberry are autogamous, cross-pollination is generally the rule. The bell-shaped pendant form of the flower discourages self-pollination via wind or gravity. Bee pollination is essential for a maximum blueberry production (Chiasson & Argall 1996) and honey bee, A. mellifera L., is the most widespread for blueberry pollination (Free 1993) as the introduction of honey bees’ hives in orchard significantly increases the production (Aras et al. 1996; Basualdo et al. 2007). On the other hand, bumblebees probably coevolved with similar-type vegetation (Heinrich 2004) and a reciprocal adaptation has made bumblebees ideal pollinators of blueberry (Desjardins & De Oliveira 2006). The bumblebee's behavioral characteristic is buzz pollination, which induces anther dehiscence, and consequently, the release of a large amount of pollen (Goulson 2010; De Luca & Vallejo-Marín 2013), and their foraging capacity in a wide range of ambient temperature (Goulson et al. 2010), makes it an effective blueberry pollinator (Buchmann 1983). Several papers have demonstrated the pollinating effectiveness of Bombus spp.; most of them are from cold temperate climate (Tuell et al. 2008; Stephen et al. 2009), but utilization of the neotropical species, Bombus pauloensis, for blueberry pollination has not been documented. Methods for rearing of this native species from South America have been developed and the use of B. pauloensis commercial colonies has been evaluated in Argentina for blueberry (Basualdo et al. 2013), strawberry, kiwi, and tomato pollination (Basualdo & Rodríguez 2009).

Recent studies have demonstrated that wild pollinators enhance fruit setting of crops, where managed pollinators such as honey bees or bumblebees are being used (Garibaldi et al. 2013; Milfont et al. 2013; Breeze et al. 2014). The contribution of wild pollinators would be valuable for blueberry pollination because plants bloom at the end of winter with low temperatures.

The objective of this work is to assess the effect of pollination carried out by B. pauloensis and A. mellifera on fruit formation and physicochemical characteristics that determine the quality of the V. corymbosum ‘Emerald’ fruit. In this context, we tested the prediction that pollinator assemblages with more species benefit V. corymbosum ‘Emerald’ production and the quality of fruit. We also elucidated the relationship between the frequency of visits (FVs) of each pollinator individually and the production, weight, seed number, and the internal quality of berries.

MATERIALS AND METHODS
Study area

The experiment was conducted on a commercial blueberry (V. corymbosum L.) plantation situated in Entre Ríos Province (31°19′40.35″ S, 58°05′00.45″ W), Argentina. Six-year-old plants of ‘Emerald’ grown at a distance of 1 m between plants and 3 m between rows (3333 plants per 1 ha) were evaluated. Standard commercial management including pruning, fertilization, control of weed, pests and diseases, and frost protection was performed during the growing season. Blueberry production constitutes 1050 ha of the area, which is equivalent to 35% of the Argentine production (Engler et al. 2008).

Pollination experiment

This research was carried out during the blooming of blueberry, V. corymbosum ‘Emerald’, from 20 July to 30 August, on a 1 ha plot. Each treatment included four rows of length 15 m (a total of 60 plants). Four treatments were performed: open pollination, B. pauloensis F. pollination, A. mellifera L. pollination, and autogamy. The honey bee and bumblebee treatments were performed in insect-proof isolation cages (10 × 15 × 4 m). For B. pauloensis treatment, a commercial colony (Brometan®) with 100 individuals was used. For A. mellifera, one honey bee colony was kept in a single-standard Langstroth hive with seven frames covered by bees and four broods. In the treatment for autogamy evaluation, individual complete plants were surrounded by a special insect-proof mesh.

For each treatment, five plants were randomly chosen and the flowering stage was evaluated by tagging three branches per plant. Branches, located in different orientations, were selected to diminish the effect of shading on the formation of fruits. Fruit setting was calculated based on the proportion of flowers in the branches that developed into berries.

Frequency of floral visitors

In order to assess the pollination treatments, observations on the FVs were made for each treatment, monitoring 10–20 flowers of the tagging branches during 5 weeks over the flowering period. Records were made between 10 and 16 h during a 5-min period; 150 observations for a total of 12.5 h were performed. For open pollination, the number of insects visiting blueberry flowers was recorded whenever the weather was suitable for insects’ activity. Results are expressed as the average number of bees per flower per 5 min.

Fruit setting and quality

In each treatment, a bucket of approximately 250 g of fruit per plant was collected and stored in a refrigerated chamber (Frutitec 15 m3, Mod M 2500HT Coiron S.A.) at 1 °C for 24 h. At the time of analyzing their size and internal quality, the fruits were conditioned at 20 °C to standardize the measurements. For each sample, 15 berries were chosen from the initial pool, for which the size and reproductive variables were estimated. Firmness was assessed for each blueberry using a non-destructive compression test, simulating a very gentle squeeze with the fingers using a TA.XT Plus Texture Analyzer (Stable Micro Systems, UK) equipped with a 5-kg load cell and a 75-mm cylinder aluminum probe. Each blueberry was compressed 10% equatorially. Fruit mass was obtained with a digital scale (CS Series, OHAUS, USA) of 0.1 g of precision. The number of fertilized seeds per fruit was counted. The fruit moisture content was determined using an oven (DHG-924, PeetLab) at 65 °C for 24 h and an analytical scale (PA214, OHAUS, USA) with an accuracy of ±0.0001 g. At the same time, the internal quality of each sample from a fruit homogenate of 5 g was measured. The concentration of total soluble solids (TSS%) was estimated using an Abbe refractometer (ATAGO, 1-T, Tokyo, Japan). The total acidity of the fruit (TA%) was measured by titrating the juice with 0.1 M NaOH to an end point of pH 8.2 using Oakton series pH 11 pH meter. This procedure was repeated three times during the harvest season at 10%, 50%, and 80% fruit maturing of the lot studied.

Statistical analysis

Data were analyzed by generalized linear mixed model (GLMM). The variable responses for the number of fruits formed per branch, FVs during 5 min, fruit mass (g), compression force (g), number of seeds per fruit, TSS% (expressed as Brix), TA%, maturity index (MI, calculated as the quotient between TSS and TA), and the average dry mass were the fixed analyzed parameters used to characterize the treatments. For the fruits formed, the random variables “plant/branches” with a binomial-type error distribution were included. For the variables FV, mass, firmness, and number of seeds, the fixed character “date of harvest” was added and as a random variable, only “plant” was used and, in this case, a negative binomial-type error distribution was used. For the internal quality estimators, the time was included as the random variable, the best fit present was the one with gamma distribution. The glmer and glmer.nb function of the package “lme4” version 1.1–12 was used to estimate the models using the statistical software “R i368 3.5.1” (R Development Core Team 2013).

RESULTS
FVs of pollinators and fruit setting

FVs showed significant differences among the three treatments (F = 15.78, p < 0.0001). The FV in open pollination was 0.03 per flower per 5 min. In this treatment, the composition of observed visitor species was A. mellifera (89.09%), two species of Vespidae (5.45%) and Syrphidae (3.64%), and one of Zygaenidae. It has been found that the visiting frequency of A. mellifera under cage was about five times higher than under B. pauloensis cage and about 40% higher than under open pollination (Fig. 1).

Fig. 1

Frequency of visits at entomophilous pollination. Different letters denote significant differences among treatments (p < 0.05)

To evaluate if there are differences in the percentage of fruits formed according to the different treatments, a total of 2672 flowers were monitored. Autogamy ranged from 0% to 0.38%. Fruit set was significantly smaller (~4.5 times) compared to the entomophilous pollination (Table 1).

Fruit yield and quality parameters of blueberry depending on the type of pollination

ParametersAutogamyApis melliferaBombus pauloensisOpen pollinationWald test
FP
Fruit setting0.14 (±0.03) C0.80 (±0.03) A0.71 (±0.04) B0.75 (±0.04) B151.25<0.0001
Seeds per fruit1.09 (±0.11) C10.97 (±0.84) B11.73 (±0.89) B15.00 (±1.08) A157.83<0.0001
Firmness (g)183.38 (±3.73) B273.34 (±5.21) A268.13 (±5.11) A268.13 (±4.47) A55.45<0.0001
Mass of fruit (g)1.62 (±0.10) B3.19 (±0.16) A3.06 (±0.15) A3.19 (±0.14) A21.01<0.0001
Average dry matter (%)14.46 (±0.42) A14.24 (±0.41) A13.88 (±0.40) AB13.16 (±0.35) B3.490.0216
Total soluble solids (%)13.81 (±0.35) A12.69 (±0.33) B13.01 (±0.34) A12.07 (±0.31) C18.610.0001
Total acidity (%)0.62 (±0.07) A0.73 (±0.08) A0.70 (±0.08) A0.72 (±0.07) A0.490.6885
Maturity index22.09 (±2.65) A17.66 (±2.05) A18.97 (±2.21) A17.03 (±1.91) A1.420.2464

Note: Values obtained through the best GLMM (generalized linear mixed model), using a criterion of lower AIC (Akaike information criterion), for the selected estimators to compare the effect of different types of entomophilous pollination. Fisher's LSD (least significant difference) test was used to represent the differences between treatments. The letter “A” denotes the highest average value. Means with a common letter are not significantly different (p > 0.05). The presented values include the temporal and inter-plant variability, being expressed as mean (±standard error).

Among the entomophilous pollination treatments, pollination with A. mellifera was significantly highest, reaching 0.8 fruits formed per branch. No significant differences were detected between an open pollination and bumble bee pollination.

Fruit quality parameters

Significant differences among treatments were detected in the number of seeds. The seed number produced at autogamy was significantly low and 10–15 times lower than under the other treatments. At the open pollination, the highest seed number per fruit, reaching an average of 15 seeds per fruit, was obtained, whereas in fruits obtained under cages, an average of 10.97 and 11.73 seeds per fruit were formed for honey bee and bumblebee, respectively (Table 1).

Comparing the entomophilous pollination treatments, there were no differences detected in the fruit mass (from 3.06 to 3.19 g) and fruit firmness, while the average fruit mass produced under autogamy was 1.62 g. The average dry matter of the fruit obtained under autogamy and pollination with A. mellifera was significantly higher as compared with the fruits obtained at open pollination. The percentage of soluble solids was the highest in fruits obtained under autogamy condition and on pollination by B. pauloensis (13.01 and 13.81, respectively), while the soluble solids of fruits pollinated in open system and by A. mellifera was 12.07 and 12.69%, respectively. Acidity and maturity index were not significantly different between the treatments.

DISCUSSION

Our work evaluated an important aspect of blueberry production – influence of different types of pollination on fruit set and quality. This study highlights the issue of a necessity to introduce specific pollinators on blueberry plantations.

The results show that V. corymbosum ‘Emerald’ is highly dependent on entomophilous pollination for optimal production and producing high-quality fruits. Similar results were reported for the cultivars ‘Northland’ and ‘Patriot’ (MacKenzie 1997), where both honey bees and bumblebees could provide adequate pollination service. Fruit setting did not increase at open pollination with wild insect visitation. This result disagrees with the data obtained by Garibaldi et al. (2013), who concluded that fruit setting could be maximized by wild pollinators in crops such as blueberry and almond, which are stocked with high densities of honey bee colonies. In the pollination mediated by A. mellifera, the highest number of fruits was set, which agrees with the results of Sampson and Cane (2000) and Javorek et al. (2002), who reported high fruit production of rabbiteye and lowbush blueberry due to pollination by honey bees. These results can be attributed to the high FVs of honey bees (0.05 visits per flower per 5 min) in caged plots, grown in conditions with no competing flowers of other plant species and wild insects.

Although we did not quantify the pollen deposition in different treatments, we considered the number of seeds as an indirect estimator of reproductive success (Dafni 1992). The number of seeds and, consequently, reproductive success was the highest on open pollination plots, where there was a stronger influence of honey bee visitation (89%) and a lower proportion of wild pollinators. The combined action of pollinators improved pollen deposition on the stigmas, this agrees with the data reported for other crops (Garibaldi et al. 2013, 2017). Despite the fact that the FVs on open pollinated plants was much lower than those made by honey bees under cages, the seed production was ~27% higher, evidencing a synergistic interaction between honey bees and wild pollinators. Bumblebees are considered the most efficient pollinators of blueberry due to the fact that they generate buzz pollination, through which the pollen is released. This non-Apis population carries a high amount of pollen in its body (De Luca & Vallejo-Marín 2013) and could enhance pollen deposition on the stigmas. Even though the stocking rate of bumblebees used in our cage resulted in adequate fruit setting, colonies with more individuals could even improve the productivity.

Berries pollinated in open system had more seeds, lower soluble solids, and consequently, higher water content resulting in better firmness, that is a component of a good fruit quality. Apparently, the relationship between seed setting and water content of fruit is regulated by gibberellins; therefore, both adequate pollination and nutrition are very important for the quality of fruit (Cano-Medrano & Darnell 1997).

This is the first report of the useful service of B. pauloensis in blueberry pollination. The use of native bees is relevant, since in some South American countries such as Chile, exotic bumblebee species such as Bombus ruderatus and Bombus terrestris were imported for commercial pollination; consequently, these species invaded Argentina, producing a considerable ecological impact on native bees (Morales 2007). Therefore, the incorporation of this native species would be an advantage, avoiding the use of invasive species and, furthermore, improving the productivity of V. corymbosum crops. Finally, we conclude that in the conditions of our trial, pollinator assemblages benefit some aspects of quality, but not the productivity of blueberries. Additional research is needed to understand interspecific behavioral relationships, such as competence or synergy, between A. mellifera and B. pauloensis in blueberry cultivation before incorporating them into blueberry production systems as an agent that provides an ecosystem service.

Fig. 1

Frequency of visits at entomophilous pollination. Different letters denote significant differences among treatments (p < 0.05)
Frequency of visits at entomophilous pollination. Different letters denote significant differences among treatments (p < 0.05)

Fruit yield and quality parameters of blueberry depending on the type of pollination

ParametersAutogamyApis melliferaBombus pauloensisOpen pollinationWald test
FP
Fruit setting0.14 (±0.03) C0.80 (±0.03) A0.71 (±0.04) B0.75 (±0.04) B151.25<0.0001
Seeds per fruit1.09 (±0.11) C10.97 (±0.84) B11.73 (±0.89) B15.00 (±1.08) A157.83<0.0001
Firmness (g)183.38 (±3.73) B273.34 (±5.21) A268.13 (±5.11) A268.13 (±4.47) A55.45<0.0001
Mass of fruit (g)1.62 (±0.10) B3.19 (±0.16) A3.06 (±0.15) A3.19 (±0.14) A21.01<0.0001
Average dry matter (%)14.46 (±0.42) A14.24 (±0.41) A13.88 (±0.40) AB13.16 (±0.35) B3.490.0216
Total soluble solids (%)13.81 (±0.35) A12.69 (±0.33) B13.01 (±0.34) A12.07 (±0.31) C18.610.0001
Total acidity (%)0.62 (±0.07) A0.73 (±0.08) A0.70 (±0.08) A0.72 (±0.07) A0.490.6885
Maturity index22.09 (±2.65) A17.66 (±2.05) A18.97 (±2.21) A17.03 (±1.91) A1.420.2464

Agüero J.I., Rollin O., Torretta J.P., Aizen M.A., Requier F., Garibaldi L.A. 2018. Honey bee impact on plants and wild bees in natural habitats. Ecosistemas 27(2): 60–69. DOI: 10.7818/ecos.1365. [in Spanish with English abstract]AgüeroJ.I.RollinO.TorrettaJ.P.AizenM.A.RequierF.GaribaldiL.A.2018Honey bee impact on plants and wild bees in natural habitatsEcosistemas272606910.7818/ecos.1365[in Spanish with English abstract]Open DOISearch in Google Scholar

Aras P., De Oliveira D., Savoie L. 1996. Effect of a honey bee (Hymenoptera: Apidae) gradient on the pollination and yield of lowbush blueberry. Journal of Economic Entomology 89(5): 1080–1083. DOI: 10.1093/jee/89.5.1080.ArasP.De OliveiraD.SavoieL.1996Effect of a honey bee (Hymenoptera: Apidae) gradient on the pollination and yield of lowbush blueberryJournal of Economic Entomology8951080108310.1093/jee/89.5.1080Open DOISearch in Google Scholar

Basualdo M., Rodríguez E.M., Bedascarrasbure E., De Jong D. 2007. Selection and estimation of the heritability of sunflower (Helianthus annuus) pollen collection behavior in Apis mellifera colonies. Genetics and Molecular Research 6(2): 374–381.BasualdoM.RodríguezE.M.BedascarrasbureE.De JongD.2007Selection and estimation of the heritability of sunflower (Helianthus annuus) pollen collection behavior in Apis mellifera coloniesGenetics and Molecular Research62374381Search in Google Scholar

Basualdo M., Rodríguez E.M. 2009. Resultados de la evaluación de la actividad de forrajeo de Bombus pauloensis en tomate. Informe Técnico. Convenio Brometán–INTA. Tandil, Argentina, 10 p. [in Spanish]BasualdoM.RodríguezE.M.2009Resultados de la evaluación de la actividad de forrajeo de Bombus pauloensis en tomateInforme Técnico. Convenio Brometán–INTA.Tandil, Argentina10[in Spanish]Search in Google Scholar

Basualdo M., Messina N., Rodríguez E., Rivadeneira M.F. 2013. Bombus atratus (Hymenoptera: Apidae) como polinizador de arándanos (Vaccinium corymbosum L.). 36 Argentinian Horticulture Congress, Abstract of Fruticulture. 24–26 September 2013, Tucumán, Argentina, abstract 329. Horticultura Argentina 32(79): 127. [in Spanish]BasualdoM.MessinaN.RodríguezE.RivadeneiraM.F.2013Bombus atratus (Hymenoptera: Apidae) como polinizador de arándanos (Vaccinium corymbosum L.). 36 Argentinian Horticulture Congress, Abstract of Fruticulture. 24–26 September 2013, Tucumán, Argentina, abstract 329Horticultura Argentina3279127[in Spanish]Search in Google Scholar

Breeze T.D., Vaissière B.E., Bommarco R., Petanidou T., Seraphides N., Kozák L. et al. 2014. Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe. PLoS ONE 9(1); e82996, 8 p. DOI: 10.1371/journal.pone.0082996.BreezeT.D.VaissièreB.E.BommarcoR.PetanidouT.SeraphidesN.KozákL.2014Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across EuropePLoS ONE91e829968 p.10.1371/journal.pone.0082996388543824421873Open DOISearch in Google Scholar

Buchmann S.L. 1983. Buzz pollination in angiosperms. Jones C.E., Little R.J. (Eds.), Handbook of experimental pollination biology. Scientific and Academic Editions, USA, pp. 73–113.BuchmannS.L.1983Buzz pollination in angiospermsJonesC.E.LittleR.J.(Eds.),Handbook of experimental pollination biologyScientific and Academic EditionsUSA73113Search in Google Scholar

Campbell J.W., Kimmel C.B., Bammer M., Stanley-Stahr C., Daniels J.C., Ellis J.D. 2018. Managed and wild bee flower visitors and their potential contribution to pollination services of low-chill high-bush blueberry (Vaccinium corymbosum L.; Ericales: Ericaceae). Journal of Economic Entomology 111(5): 2011–2016. DOI: 10.1093/jee/toy215.CampbellJ.W.KimmelC.B.BammerM.Stanley-StahrC.DanielsJ.C.EllisJ.D.2018Managed and wild bee flower visitors and their potential contribution to pollination services of low-chill high-bush blueberry (Vaccinium corymbosum L.; Ericales: Ericaceae)Journal of Economic Entomology11152011201610.1093/jee/toy21530010801Open DOISearch in Google Scholar

Cano-Medrano R., Darnell R.L. 1997. Cell number and cell size in parthenocarpic vs. pollinated blueberry (Vaccinium ashei) fruits. Annals of Botany 80(4): 419–425. DOI: 10.1006/anbo.1997.0462.Cano-MedranoR.DarnellR.L.1997Cell number and cell size in parthenocarpic vs. pollinated blueberry (Vaccinium ashei) fruitsAnnals of Botany80441942510.1006/anbo.1997.0462Open DOISearch in Google Scholar

Cariveau D.P., Winfree R. 2015. Causes of variation in wild bee responses to anthropogenic drivers. Current Opinion in Insect Science 10: 104–109. DOI: 10.1016/j.cois.2015.05.004CariveauD.P.WinfreeR.2015Causes of variation in wild bee responses to anthropogenic driversCurrent Opinion in Insect Science1010410910.1016/j.cois.2015.05.00429587998Open DOISearch in Google Scholar

Chacoff N.P., Aizen M.A. 2006. Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forest. Journal of Applied Ecology 43(1): 18–27. DOI: 10.1111/j.1365-2664.2005.01116.x.ChacoffN.P.AizenM.A.2006Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forestJournal of Applied Ecology431182710.1111/j.1365-2664.2005.01116.xOpen DOISearch in Google Scholar

Chiasson G., Argall J. 1996. Pollination of wild blueberries. Wild blueberry fact sheet number B.1.0. New Brunswick Department of Agriculture and Rural Development, Fredericton, Canada. www2.gnb.ca/content/gnb/en/departments/10/agriculture/content/crops/wild_blueberries/pollination.htmlChiassonG.ArgallJ.1996Pollination of wild blueberries. Wild blueberry fact sheet number B.1.0New Brunswick Department of Agriculture and Rural DevelopmentFredericton, Canadawww2.gnb.ca/content/gnb/en/departments/10/agriculture/content/crops/wild_blueberries/pollination.htmlSearch in Google Scholar

Dafni A. 1992. Pollination ecology: A practical Approach. Practical Approach Series 110. Oxford University Press, 250 p.DafniA.1992Pollination ecology: A practical Approach. Practical Approach Series 110Oxford University Press250Search in Google Scholar

De Luca P.A., Vallejo-Marín M. 2013. What's the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination. Current Opinion in Plant Biology 16(4): 429–435. DOI: 10.1016/j.pbi.2013.05.002.De LucaP.A.Vallejo-MarínM.2013What's the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollinationCurrent Opinion in Plant Biology16442943510.1016/j.pbi.2013.05.00223751734Open DOISearch in Google Scholar

Desjardins È.C., De Oliveira D. 2006. Commercial bumble bee Bombus impatiens (Hymenoptera: Apidae) as a pollinator in lowbush blueberry (Ericale: Ericaceae) fields. Journal of Economic Entomology 99(2): 443–449. DOI: 10.1093/jee/99.2.443.DesjardinsÈ.C.De OliveiraD.2006Commercial bumble bee Bombus impatiens (Hymenoptera: Apidae) as a pollinator in lowbush blueberry (Ericale: Ericaceae) fieldsJournal of Economic Entomology99244344910.1093/jee/99.2.443Open DOISearch in Google Scholar

Engler P., Rodríguez M., Cancio R., Handloser M., Vera L.M. 2008. Zonas AgroEconómicas Homogéneas, Entre Ríos. Descripción ambiental, socioeconómica y productiva. Instituto Nacional de Tecnología Agropecuaria, Buenos Aires, Argentina, 150 p. [in Spanish]EnglerP.RodríguezM.CancioR.HandloserM.VeraL.M.2008Zonas AgroEconómicas Homogéneas, Entre Ríos. Descripción ambiental, socioeconómica y productivaInstituto Nacional de Tecnología AgropecuariaBuenos Aires, Argentina150[in Spanish]Search in Google Scholar

Free J.B. 1993. Insect pollination of crops, 2nd ed. Academic Press, London, UK, 684 p.FreeJ.B.1993Insect pollination of crops2nd ed.Academic PressLondon, UK684Search in Google Scholar

Garibaldi L.A., Steffan-Dewenter I., Winfree R., Aizen M.A., Bommarco R., Cunningham S.A. et al. 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339(6127): 1608–1611. DOI: 10.1126/science.1230200GaribaldiL.A.Steffan-DewenterI.WinfreeR.AizenM.A.BommarcoR.CunninghamS.A.2013Wild pollinators enhance fruit set of crops regardless of honey bee abundanceScience33961271608161110.1126/science.123020023449997Open DOISearch in Google Scholar

Garibaldi L.A., Gemmill-Herren B., D’Annolfo R., Graeub B.E., Cunningham S.A., Breeze T.D. 2017. Farming approaches for greater biodiversity, livelihoods, and food security. Trends in Ecology and Evolution 32(1): 68–80. DOI: 10.1016/j.tree.2016.10.001.GaribaldiL.A.Gemmill-HerrenB.D’AnnolfoR.GraeubB.E.CunninghamS.A.BreezeT.D.2017Farming approaches for greater biodiversity, livelihoods, and food securityTrends in Ecology and Evolution321688010.1016/j.tree.2016.10.001Open DOISearch in Google Scholar

Gill R.J., Baldock K.C.R., Brown M.J.F., Cresswell J.E., Dicks L.V., Fountain M.T. et al. 2016. Protecting an ecosystem service: Approaches to understanding and mitigating threats to wild insect pollinators. In: Woodward G., Bohan D.A. (Eds.), Ecosystem Services: From Biodiversity to Society, part 2. Advances in Ecological Research 54: 135–206. DOI: 10.1016/bs.aecr.2015.10.007.GillR.J.BaldockK.C.R.BrownM.J.F.CresswellJ.E.DicksL.V.FountainM.T.2016Protecting an ecosystem service: Approaches to understanding and mitigating threats to wild insect pollinatorsIn:WoodwardG.BohanD.A.(Eds.),Ecosystem Services: From Biodiversity to Society, part 2. Advances in Ecological Research5413520610.1016/bs.aecr.2015.10.007Open DOISearch in Google Scholar

Goulson D. 2010. Bumblebees: Behaviour, ecology, and conservation, 2nd ed. Oxford University Press, 317 p.GoulsonD.2010Bumblebees: Behaviour, ecology, and conservation2nd ed.Oxford University Press317Search in Google Scholar

Goulson D., Lepais O., O’Connor S., Osborne J.L., Sanderson R.A., Cussans J. et al. 2010. Effects of land use at a landscape scale on bumblebee nest density and survival. Journal of Applied Ecology 47(6): 1207–1215. DOI: 10.1111/j.1365-2664.2010.01872.x.GoulsonD.LepaisO.O’ConnorS.OsborneJ.L.SandersonR.A.CussansJ.2010Effects of land use at a landscape scale on bumblebee nest density and survivalJournal of Applied Ecology4761207121510.1111/j.1365-2664.2010.01872.xOpen DOISearch in Google Scholar

Heinrich B. 2004. Bumblebee economics. Harvard University Press, USA, 245 p.HeinrichB.2004Bumblebee economicsHarvard University PressUSA245Search in Google Scholar

Javorek S.K., Mackenzie K.E., Vander Kloet S.P. 2002. Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium). Annals of the Entomological Society of America 95(3): 345–351. DOI: 10.1603/0013-8746(2002)095[0345:cpeabh]2.0.co;2.JavorekS.K.MackenzieK.E.Vander KloetS.P.2002Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium)Annals of the Entomological Society of America95334535110.1603/0013-8746(2002)095[0345:cpeabh]2.0.co;2Open DOISearch in Google Scholar

MacKenzie K.E. 1997. Pollination requirements of three highbush blueberry (Vaccinium corymbosum L.) cultivars. Journal of the American Society for Horticultural Science 122(6): 891–896. DOI: 10.21273/jashs.122.6.891.MacKenzieK.E.1997Pollination requirements of three highbush blueberry (Vaccinium corymbosum L.) cultivarsJournal of the American Society for Horticultural Science122689189610.21273/jashs.122.6.891Open DOISearch in Google Scholar

Milfont M. de O., Rocha E.E.M., Lima A.O.N., Freitas B.M. 2013. Higher soybean production using honeybee and wild pollinators, a sustainable alternative to pesticides and autopollination. Environmental Chemistry Letters 11(4): 335–341. DOI: 10.1007/s10311-013-0412-8.Milfont M. deO.RochaE.E.M.LimaA.O.N.FreitasB.M.2013Higher soybean production using honeybee and wild pollinators, a sustainable alternative to pesticides and autopollinationEnvironmental Chemistry Letters11433534110.1007/s10311-013-0412-8Open DOISearch in Google Scholar

Morales C.L. 2007. Introduction of no native bumblebees (Bombus): causes, ecological consequences and perspectives. Ecología Austral 17: 51–65. [in Spanish with English abstract]MoralesC.L.2007Introduction of no native bumblebees (Bombus): causes, ecological consequences and perspectivesEcología Austral175165[in Spanish with English abstract]Search in Google Scholar

Pasquet R.S., Peltier A., Hufford M.B., Oudin E., Saulnier J., Paul L. et al. 2008. Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distances. Proceedings of the National Academy of Sciences 105(36): 13456–13461. DOI: 10.1073/pnas.0806040105.PasquetR.S.PeltierA.HuffordM.B.OudinE.SaulnierJ.PaulL.2008Long-distance pollen flow assessment through evaluation of pollinator foraging range suggests transgene escape distancesProceedings of the National Academy of Sciences10536134561346110.1073/pnas.0806040105Open DOISearch in Google Scholar

Requier F., Andersson G.K.S., Oddi F.J., Garcia N., Garibaldi L.A. 2018. Perspectives from the survey of honey bee colony losses during 2015–2016 in Argentina. Bee World 95(1): 9–12. DOI: 10.1080/0005772x.2018.1413620.RequierF.AnderssonG.K.S.OddiF.J.GarciaN.GaribaldiL.A.2018Perspectives from the survey of honey bee colony losses during 2015–2016 in ArgentinaBee World95191210.1080/0005772x.2018.1413620Open DOISearch in Google Scholar

Sampson B.J., Cane J.H. 2000. Pollination efficiencies of three bee (Hymenoptera: Apoidea) species visiting rabbiteye blueberry. Journal of Economic Entomology 93(6): 1726–1731. DOI: 10.1603/0022-0493-93.6.1726.SampsonB.J.CaneJ.H.2000Pollination efficiencies of three bee (Hymenoptera: Apoidea) species visiting rabbiteye blueberryJournal of Economic Entomology9361726173110.1603/0022-0493-93.6.1726Open DOISearch in Google Scholar

Steffan-Dewenter I., Potts S.G., Packer L. 2005. Pollinator diversity and crop pollination services are at risk. Trends in Ecology and Evolution 20(12): 651–652. DOI: 10.1016/j.tree.2005.09.004.Steffan-DewenterI.PottsS.G.PackerL.2005Pollinator diversity and crop pollination services are at riskTrends in Ecology and Evolution201265165210.1016/j.tree.2005.09.004Open DOISearch in Google Scholar

Stephen W.P., Rao S., White L. 2009. Abundance, diversity and foraging contribution of bumble bees to blueberry production in Western Oregon. Acta Horticulturae 810: 557–562. DOI: 10.17660/acta-hortic.2009.810.73.StephenW.P.RaoS.WhiteL.2009Abundance, diversity and foraging contribution of bumble bees to blueberry production in Western OregonActa Horticulturae81055756210.17660/acta-hortic.2009.810.73Open DOISearch in Google Scholar

Tuell J.K., Fiedler A.K., Landis D., Isaacs R. 2008. Visitation by wild and managed bees (Hymenoptera: Apoidea) to eastern U.S. native plants for use in conservation programs. Environmental Entomology 37(3): 707–718. DOI: 10.1603/0046-225x(2008)37[707:vbwamb]2.0.co;2.TuellJ.K.FiedlerA.K.LandisD.IsaacsR.2008Visitation by wild and managed bees (Hymenoptera: Apoidea) to eastern U.S. native plants for use in conservation programsEnvironmental Entomology37370771810.1603/0046-225x(2008)37[707:vbwamb]2.0.co;2Open DOISearch in Google Scholar

Tylianakis J.M., Didham R.K., Bascompte J., Wardle D.A. 2008. Global change and species interactions in terrestrial ecosystems. Ecology Letters 11(12): 1351–1363. DOI: 10.1111/j.1461-0248.2008.01250.x.TylianakisJ.M.DidhamR.K.BascompteJ.WardleD.A.2008Global change and species interactions in terrestrial ecosystemsEcology Letters11121351136310.1111/j.1461-0248.2008.01250.xOpen DOISearch in Google Scholar

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