Next Article in Journal
The Effects of Using Sulfur and Organic Bedding on the Content of Macro- and Micronutrients and Biologically Active Substances in Winter Garlic Bulbs
Next Article in Special Issue
Successful Indoor Mass Storage of Honeybee Queens (Apis mellifera) during Winter
Previous Article in Journal
Rice Breeding in Vietnam: Retrospects, Challenges and Prospects
Previous Article in Special Issue
Changes of Physicochemical Properties of Starch Syrups Recommended for Winter Feeding of Honeybees during Storage
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Agriculture
Volume 11
Issue 5
10.3390/agriculture11050398
agriculture-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Direct Economic Impact Assessment of Winter Honeybee Colony Losses in Three European Countries

by
Despina Popovska Stojanov
1,
Lazo Dimitrov
1,
Jiří Danihlík
2,
Aleksandar Uzunov
3,4,
Miroljub Golubovski
5,
Sreten Andonov
3,6 and
Robert Brodschneider
7,*
1
Department of Agricultural Business, Economy and Rural Development, Institute of Agriculture, University Ss. Cyril and Methodius in Skopje, 1000 Skopje, North Macedonia
2
Department of Biochemistry, Faculty of Science, Palacký University, 783 71 Olomouc, Czech Republic
3
Department of Animal Biotechnology, Faculty of Agricultural Sciences and Food, University Ss. Cyril and Methodius in Skopje, 1000 Skopje, North Macedonia
4
Landesbetrieb Landwirtschaft Hessen—Bieneninstitut, 35274 Kirchhain, Germany
5
MacBee—Association for Conservation of Macedonian Native Honey Bee, 1483 Negorci, North Macedonia
6
Department Animal Breeding and Genetics, Swedish University of Agricultural Sciences, 750 07 Uppsala, Sweden
7
Institute of Biology, University of Graz, 8010 Graz, Austria
*
Author to whom correspondence should be addressed.
Agriculture 2021, 11(5), 398; https://doi.org/10.3390/agriculture11050398
Submission received: 1 April 2021 / Revised: 23 April 2021 / Accepted: 23 April 2021 / Published: 27 April 2021
(This article belongs to the Special Issue Emerging Problems of Modern Beekeeping)
Versions Notes

Abstract

:
Honeybees are of great importance because of their role in pollination as well as for hive products. The population of managed colonies fluctuates over time, and recent monitoring reports show different levels of colony losses in many regions and countries. The cause of this kind of loss is a combination of various factors, such as the parasitic mite Varroa destructor, viruses, pesticides, management practices, climate change, and other stress factors. Having in mind that the economic aspect of honeybee colony losses has not been estimated, a pioneer effort was made for developing a methodology that estimates the economic impact of honeybee colony losses. Winter loss data was based on 2993 answers of the COLOSS standard questionnaire survey of honeybee winter colony losses for 2016/2017. In addition, market and financial data were used for each country. In a comparative analysis, an assessment on the economic impact of colony losses in Austria, Czechia, and Macedonia was made. The estimation considered the value of the colonies and the potential production losses of the lost colonies and of surviving but weak colonies. The direct economic impact of winter honeybee colony losses in 2016/2017 in Austria was estimated to be about 32 Mio €; in Czechia, 21 Mio €; and in Macedonia, 3 Mio €. Economic impact reflects the different value levels in the three countries, national colony populations, and the magnitude of colony losses. This study also suggests that economic losses are much higher than the subsidies, which underlines the economic importance of honeybees for the agricultural sector.

1. Introduction

Honeybees are economically important managed pollinators for crops and wild plants [1,2,3,4,5]. Though they are not solely responsible for the pollination of cultivated crops, their exact economic contribution to agricultural production is difficult to estimate [6]. Still, losses of honeybee colonies have extensive economic consequences. Next to pollination, the honeybees’ economic importance lays in the production of hive products such as honey, pollen, beeswax, propolis, bee venom, and royal jelly. Honeybee colonies, nucs, and packages are important trade products too [7]. Honey is by far the most important product and is globally traded [8]. In Europe, most beekeepers are backyard or sideline beekeepers producing for the local market, but there are also a few professional beekeeping operations making a regular income from beekeeping and hive products [9,10].
In temperate climates, winter is a critical period for honeybee colonies. With no forage available, a colony relies on food reserves hoarded in the hive for thermoregulation and brood rearing. Though there can be a natural baseline mortality assumed, winter colony losses due to colony mortality or queen failure vary greatly among winters and from region to region. For example, an overall loss rate of 20.9% was recorded in the winter of 2016/2017 according to the COLOSS study conducted in many European and some non-European countries [11]. There are similar reports of loss rates of managed honeybee colonies from other continents [12,13,14,15,16,17]. The COLOSS survey performed in spring 2017 recorded losses of production colonies of 23.4% in Austria, 15.0% in the Czech Republic, and 22.5% in the Republic of Macedonia [11].
In the European subspecies of the Western honeybee, Apis mellifera, the parasitic mite Varroa destructor hampers winter survival by reducing the longevity of worker bees [18,19]. By feeding on bee tissues, varroa is also a vector of honeybee viruses [20]. A clear association between mite infestation levels in autumn and honeybee winter colony losses has been demonstrated in Austria by Morawetz et al. [21]. Other factors, such as further pests and pathogens, hive management by beekeepers, loss of forage, and pesticides impact colony health [22,23,24,25,26,27]. A pan-European epidemiological study demonstrated that honeybee colony survival greatly depends on beekeeper education and disease control [28]. One possible explanation for the variation of colony losses between different winters are the prevailing weather conditions, not only during winter, but also before, that influence growth and development of the honeybee colony, and hence also of the varroa mite population [29].
Honeybee colony losses can be compensated, which results in rather stable or even increasing numbers of colonies managed in certain regions, though decreasing honeybee populations have also been reported [17,30,31]. Such compensations in colony numbers are achieved by beekeepers splitting colonies. Such splitting, in turn, is accompanied by financial expenses. Achieving economically sustainable colony levels and the role of economic factors in the long-term decline of honeybee stocks in the United States has been studied in the Rocky Mountain region by Jones Ritten et al. [32]. In this study, we aim to estimate the direct economic impact of winter honeybee colony losses on the apicultural sector of three European countries, Austria, Czech Republic, and the Republic of Macedonia. While focusing on the costs directly affecting beekeeping, the indirect costs—e.g., through lost pollination of agricultural crops—were not examined in this study, as this was already established for Europe, the United States, and the world [2,33,34]. The honeybee colony numbers of the three countries are in the midfield of the European apicultural sector [10], and the loss rates of winter 2016/2017 [11] were used for analysis.

2. Materials and Methods

2.1. Data Collection

The data on winter honeybee colony losses were collected by the citizen science crowdsourcing concept in Austria (AT), Czech Republic (CZ), and Republic of Macedonia (MK) in spring 2017. Beekeepers voluntarily participated in this survey coordinated by COLOSS. These standardised annual surveys among beekeepers on colony losses are well-established in all three countries [11,25,30,35,36,37,38]. The survey is promoted via various channels, including websites and beekeeping magazines, and is open for every beekeeper, even anonymously. The questionnaire included questions on the number of wintered colonies, colony losses, and weak colonies after winter. In MK, the COLOSS questionnaire was supplemented with questions referring to market and financial data. For AT and CZ, the average honey production, and the average market price per kilogram of honey for the calculations were based on the average national data from referenced or official sources [39,40]. For MK, honey production and its market price were obtained for the different geographic regions from the questionnaire.

2.2. Economic Estimation

The value of the total losses is a sum of the value of losses as a consequence of the lost colonies and as a result of the weak colonies (Equation (1)).
V T L = V L l c + V L w c ,
where
  • VTL = Value of total losses;
  • VLlc = Value of losses as a result of lost colonies;
  • VLwc = Value of losses as a result of weak colonies.
The value of the losses as a consequence of the lost colonies (VLlc) was calculated as a sum of the value of the lost honeybee colonies (their number multiplied by the price per colony) and the value of the lost production that could have been obtained from these colonies (the number of lost colonies multiplied by the average honey production per colony and the price of the honey—Equation (2)):
V L l c = L c × P c + L c × H c × P h ,
where
  • VLlc = Value of losses as a result of lost colonies;
  • Lc = Number of lost colonies;
  • Pc = Price per colony;
  • Hc = Honey yields per colony;
  • Ph = Price per one kg honey.
The value of the losses as a result of the weak colonies (VLwc) is estimated only on the basis of the value of the lost honey production (Equation (3)). The calculations are made based on the presumption that there are no differences between the lost honey yields from a strong and a weak colony.
V L w c = W c × H c × P h ,
where
  • VLwc = Value of losses as a result of weak colonies;
  • Wc = Number of weak colonies;
  • Hc = Honey yields per colony;
  • Ph = Price per one kg honey.
The average economic losses per one lost colony were calculated by dividing the total value of the losses, as a consequence of the lost colonies, with the total number of lost colonies. Economic losses per one weak colony were calculated by dividing the total value of the losses because of the weak colonies with the total number of weak colonies. The economic losses per one colony before winter start were calculated by dividing the value of the total losses with the total number of colonies before winter, i.e., the total number of colonies in the sample.
In our calculations, we only included the costs beekeepers are confronted with. In the evaluation, we did not include the parameters about protection, feeding, and working hours per beehive because of their extreme variations and complexity. We also did not include any indirect costs deriving from colony losses, e.g., due to loss of crop yield by reduced pollination, but we exclusively focused on the direct costs the beekeepers are facing. By multiplying the average financial losses per one colony before the beginning of the winter with the total number of colonies in each country, the total value of economic losses was extrapolated to the national level. Where possible (MK and CZ), a comparison between the data from the economic losses and the state subsidies was made.

3. Results

In total, our survey covered 1656 beekeeping operations from AT, 1191 from CZ, and 320 from MK. Atypical beekeeping operations with more than two times standard deviation from the mean of the total value of losses within a class were excluded from the sample. This means that data from 1570 beekeepers with 31,096 colonies were left for economic loss assessment in AT, which covers 8.8% from the total 354,080 colonies [39] in the country before winter 2016/2017. In CZ, data from 1118 beekeepers with 22,701 colonies were analysed, which covers 3.3% from the total 693,069 colonies in 2016 (official data on request from the Ministry of Agriculture of the Czech Republic). In MK, data from 305 beekeepers with 17,348 colonies were analysed with a coverage of 17.1% of the total number of 101,669 colonies before winter 2016/2017 [41]. For the analysis, the sample was stratified based on the size of beekeeping operations, i.e., the number of colonies per beekeeping operation in six classes. Each class was individually analysed for normal distribution of the total value of the losses. The size classes of beekeeping operations in the three countries are shown in Table 1.
This estimation considers colony mortality during winter 2016/2017, the value of the lost colonies, and potential honey production losses from the lost and weak colonies. The values used for the calculations are shown in Table 2.
The results of the economic analysis showed that the total financial losses for the sampled population of beekeeping operations in AT were about 2.8 million € (2,813,052 €) in 2017 (Table 3). Around 2.0 million € (2,085,444 €) or 74% of total economic losses were from the lost colonies and circa 0.8 million € (727,608 €) or 26% of economic losses derived from the weak colonies. Total economic losses in CZ amounted to 0.7 million € (700,955 €). The losses from the lost colonies exceeded 0.5 million € (533,133 €), or 76%, from the total losses and near 0.2 million € (167,823 €), or 24%, were from the weak colonies. For MK, the total losses exceeded 0.5 million € (518,507 €). Most of them came from the lost colonies, or 0.4 million (422,696 €). This is 82% of the total financial losses, whereas the odd 18% were from the weak colonies estimated at around 0.1 million (95,811 €).
The average economic losses per beekeeping operation size class were different in all three countries. In AT, they ranged between 525 € for the category of beekeepers with up to 10 colonies and 32,255 € for beekeeping operations with more than 150 colonies. In CZ, the average economic losses per beekeeping operation varied between 164 € and 6531 €, and in MK, they amounted from 402 € to 3278 € (Table 4).
In AT, we calculated the economic losses per lost colony to be 318 € and per weak one to be 168 €. In CZ, economic losses per colony are 209 € per lost colony and 119 € per weak colony, while in MK, the average economic losses are 120 € per lost colony and 46 € per weak colony, respectively (Table 5). Based on this, and the number of colonies in each state (Table 2), the total national economic losses are estimated. This is about 32 Mio € in Austria, 21 Mio € in Czechia, and 3 Mio € in Macedonia (Table 5).

4. Discussion

Our study is the first to calculate the direct economic impact of winter losses of managed honeybee colonies. We used raw data of loss rates from the 2017 COLOSS investigation [11] and economic data originally surveyed from beekeepers (Macedonia) or obtained from official national documents (Austria, Czech Republic). Scientific studies on beekeeping economics so far mostly considered the honey market [8,17], consumer preferences [42,43], pollination services [5,44,45,46], or queen trade [7]. Only very little research has been done on the impact of honeybee diseases on beekeeping economics and the economic sustainability of beekeeping [32,47]. For treatment of honeybee colonies against the parasitic mite V. destructor, a number of different methods are available [48,49]. Sound analysis of the economics of different varroa treatments (including decision support systems [50]) or monitoring tools for the economic accounts of stock [51] have only become available recently. To better illustrate the importance of economic and efficient hive management and the financial loss for the apicultural sector, we estimated the direct economic costs of honeybee winter colony losses in three European countries based on real 2016/2017 colony-loss rates collected from almost 3000 beekeepers. We included the price of honeybee colonies, honey production, and prices and financial losses from surviving but weak colonies, which were assumed to produce no honey the following year.
Surprisingly, few data on regional parameters required for our analysis, such as average honey yield or price of honey, are available from scientific sources, probably because the market of bee products is not regulated or properly examined. Therefore, data collection via questionnaires or consultancy of authoritative documents are needed, just like we did in this study. The assessment of economic parameters is further complicated, for example, by regional variations in honey prices, not to speak about different prices of different honeys depending on quality or floral origin [51,52]. Having in mind the variation in the prices, yields, and colony losses, and that these variations are correlated with the size of the beekeeper operation, it is recommended to incorporate economic data as an integrated part of the international COLOSS questionnaire or similar surveys in order to enable more precise assessments of the economic losses of the apicultural sector in the future. For example, in MK, we noticed a variance in average colony price (from 74 to 80 € per colony), average honey yield (8 to 11 kg per colony), and average honey prices (5 to 6 € per kg) between the classes according to the size of the beekeeping operation, i.e., the number of colonies per beekeeping operation. Our study, therefore, set the parameters needed for the extension of our economic estimations to other countries or larger entities such as the European Union. We also want to note that extension of our method to other countries with different structure of the apicultural sector (larger beekeeping operations, different degrees of professional beekeeping) may need separate attention [10]. In our study, backyard and sideline beekeeping prevailed, though especially in MK, a notable number of larger beekeeping operations also exist that responded to our data collection (Table 1). Again, one of the most critical points is the availability of the different data types (good estimates of colony numbers, colony loss rates, prices for bees and bee products, honey yield) that need to be integrated into economic estimations. In that manner, building capacity and motivation of beekeepers to perform regular bookkeeping and record-keeping can significantly contribute towards a more precise impact assessment of honeybee colony losses.
The results from the extrapolation on a national level showed that in AT, the estimated economic losses were 32,031,305 €; in CZ, 21,400,401 €; and in MK, 3,038,741 € (Table 5). As the information about the national structure of the beekeeping operations according to operation size was deficient, we were not able to perform any analysis of sample representativeness. Additionally, while the highest share of the sample in AT and CZ were small beekeeper operations with less than 20 colonies (77% and 73%, which reflects previous studies [9,30]), in MK, the highest portion (65%) of surveyed beekeeping operations manage between 51 and 100 colonies. Additionally, the average economic losses per colony before the start of the winter vary between different beekeeping operation sizes and at the same time, between countries (Table 5). The highest value in AT can be explained by the high prices for honey and honeybee colonies (Table 2). In their study focusing on the United States, Rucker et al. [53] suggested that colony collapse disorder has a surprisingly small economic impact because of adaptations such as increasing pollination fees. For Europe, and the presented countries, honey is the most important product, and no steep increase in honey price has been observed [8].
The economic impact assessment of winter honeybee colony losses can also be a useful tool for policymakers for planning and developing strategies and support measures for the beekeeping sector. It becomes evident from our analysis that the economic losses are higher than the national support measures. For MK, the estimated national losses of 3,038,741 € were almost 1 million euro higher than the financial payment of 130,435,200 MKD or 2,120,898 € for the registered surviving winter colonies in 2017 [54]. The situation is even more pronounced in the case of CZ, where the total subsidy paid was 105,000,000 CZK or 4,038,461 € for wintered colonies, which is more than five times lower than the estimated losses of 21,400,401 € in the following winter [55]. For AT, the estimated losses were 32,031,305 €, but due to the absence of data on subsidies, no comparison was made.
Our methodology should be further extended to assess other consequences from colony losses, such as direct impact on economic losses from the potential loss of yields from other bee products (royal jelly, pollen, wax, etc.) or pollination fees, additional extra costs (labour, feeding, etc.) and losses from beekeeper’s practices (splitting as compensation for the lost colonies), but also impact to indirect losses, primarily from the pollination role of the bees.
The direct costs of honeybee colonies reported in this study very likely make up only a small portion of the real economic impacts of honeybee colony losses. We did not include any economic impacts from a possibly reduced pollination service provided by the honeybees [2,5,6,34]. However, our estimated costs are the minimum costs that certainly affect beekeepers. In the end, if we take into consideration the indirect losses, primarily from the pollination of agricultural crops and wildlife biodiversity, we can conclude that economic losses from honeybee colony losses are quite beyond the results presented in this paper, which supports investments in colony health to reduce loss rates. Another example for a loss we have not included, and which is probably difficult to measure economically, is the loss of valuable breeding stock.
In the three countries, a large proportion of beekeepers are hobbyist or sideline beekeepers. Each year they re-establish the colonies lost during winter on their own expenses, by making colony splits, breeding queens, etc. [30]. The economic effect of labour for doing this was not included in our estimations, hence, further research is required to picture the economic magnitude of colony losses more precisely for society. Our study also confirms that reducing colony losses by efficient treatments against diseases or other actions greatly lowers the economic pressure on beekeeping operations [47,50]. This could impede the recession of honeybee colonies, and active beekeepers, in many Western countries [17,31,56]. Measures to reduce economic losses from colony losses include enhancement of extension capacities for beekeeper education and spreading good apicultural practice [28,36,57,58], raising awareness for the use of native or locally adapted honeybee stock [59,60,61], encouraging honeybee breeding initiatives and programs for genetic improvement by considering the relevance of local adaptation [62], considering colony vitality and varroa resistance as imperative breeding goals [63,64,65], and propagating best-practice varroa treatments that are tailored for the local conditions [66,67]. Though these actions and practices are also costly [68], subsidies could be used to facilitate these, and revenue would strengthen the apicultural sector. Another opportunity to safeguard economically sustainable beekeeping is the increase in revenue from hive products through higher prices [8].

5. Conclusions

Our pilot study on periodic costs of losses of managed honeybee colonies brought the first estimation of the economic importance of the apicultural sector as part of the agricultural economy. The applied model is relatively simple, but nevertheless provides first values of national economic impacts and differences among countries, mainly based on the different value levels in the three countries, national colony populations, and the magnitude of the colony loss rate. Following our pilot effort to estimate the direct economic impact of winter colony losses of managed honeybees, further research and broadening to more countries where COLOSS data is available is recommended, including temporal series to detect long-term trends. To set the economic losses reported in this article in relation to the economics of the apicultural sector, a thorough analysis of the economics of the whole sector is required. Policymakers may act in reducing economic impact of honeybee colony losses by supporting known factors contributing to colony survival and further research to improve colony health.

Author Contributions

Conceptualization, D.P.S., L.D., J.D., A.U., M.G., S.A., R.B.; methodology, D.P.S. and L.D.; formal analysis, D.P.S.; writing—original draft preparation, D.P.S.; writing—review and editing, R.B.; visualization, R.B.; funding acquisition, J.D., A.U., R.B. All authors have read and agreed to the published version of the manuscript.

Funding

Open access funding provided by University of Graz. The work was supported by Scientific & Technological Cooperation Austria—Macedonia (Project No. MK January 2016) and by AKTION, Austrian-Czech bilateral project (Project No. 74p4). Austrian data was collected within the Austrian project “Zukunft Biene” (Grant No.: 100,972).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank the participating beekeepers in all three countries and the COLOSS research association (prevention of honeybee colony losses) for stimulating discussions. Special thanks go to Macedonian beekeepers MSc Borche Pavlov and Branko Sokolov for the generous support and contribution during the development of the calculation model and methodology.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Breeze, T.D.; Bailey, A.P.; Baelcombe, K.G.; Potts, S.G. Pollination services in the UK: How important are honeybees? Agric. Ecosyst. Environ. 2011, 142, 137–143. [Google Scholar] [CrossRef] [Green Version]
  2. Gallai, N.; Salles, J.-M.; Settele, J.; Vaissière, B.E. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol. Econ. 2009, 68, 810–821. [Google Scholar] [CrossRef]
  3. Klein, A.M.; Vaissiere, B.E.; Cane, J.H.; Steffan-Dewenter, I.; Cunningham, S.A.; Kremen, C.; Tscharntke, T. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 2007, 274, 303–313. [Google Scholar] [CrossRef] [Green Version]
  4. Williams, I.H. The dependence of crop production within the European Union on pollination by honey bees. Agric. Zool. Rev. 1994, 6, 229–257. [Google Scholar]
  5. Southwick, E.E.; Southwick, L., Jr. Estimating the economic value of honey bees (Hymenoptera: Apidae) as agricultural pollinators in the United States. J. Econ. Entomol. 1992, 85, 621–633. [Google Scholar] [CrossRef]
  6. Garibaldi, L.A.; Steffan-Dewenter, I.; Winfree, R.; Aizen, M.A.; Bommarco, R.; Cunningham, S.A.; Kremen, C.; Carvalheiro, L.G.; Harder, L.D.; Afik, O.; et al. Wild Pollinators Enhance Fruit Set of Crops Regardless of Honey Bee Abundance. Science 2013, 339, 1608–1611. [Google Scholar] [CrossRef]
  7. Bixby, M.; Hoover, S.E.; McCallum, R.; Ibrahim, A.; Ovinge, L.; Olmstead, S.; Pernal, S.F.; Zayed, A.; Foster, L.J.; Guarna, M.M. Honey bee queen production: Canadian costing case study and profitability analysis. J. Econ. Entomol. 2020, 113, 1618–1627. [Google Scholar] [CrossRef]
  8. García, N.L. The Current Situation on the International Honey Market. Bee World 2018, 95, 89–94. [Google Scholar] [CrossRef]
  9. Brodschneider, R.; Moosbeckhofer, R.; Crailsheim, K. Surveys as a tool to record winter losses of honey bee colonies: A two year case study in Austria and South Tyrol. J. Apic. Res. 2010, 49, 23–30. [Google Scholar] [CrossRef]
  10. Chauzat, M.P.; Cauquil, L.; Roy, L.; Franco, S.; Hendrikx, P.; Ribière-Chabert, M. Demographics of the European apicultural industry. PLoS ONE 2013, 8, e79018. [Google Scholar] [CrossRef] [PubMed]
  11. Brodschneider, R.; Gray, A.; Adjlane, N.; Ballis, A.; Brusbardis, V.; Charrière, J.D.; Chlebo, R.; Coffey, M.F.; Dahle, B.; de Graaf, D.C.; et al. Multi-country loss rates of honey bee colonies during winter 2016/2017 from the COLOSS survey. J. Apic. Res. 2018, 57, 452–457. [Google Scholar] [CrossRef] [Green Version]
  12. Kulhanek, K.; Steinhauer, N.; Rennich, K.; Caron, D.M.; Sagili, R.R.; Pettis, J.S.; Ellis, J.D.; Wilson, M.E.; Wilkes, J.T.; Tarpy, D.R.; et al. A national survey of managed honey bee 2015-2016 annual colony losses in the USA. J. Apic. Res. 2017, 56, 328–340. [Google Scholar] [CrossRef] [Green Version]
  13. Lee, K.V.; Steinhauer, N.; Rennich, K.; Wilson, M.E.; Tarpy, D.R.; Caron, D.M.; Rose, R.; Delaplane, K.S.; Baylis, K.; Lengerich, E.J.; et al. A national survey of managed honey bee 2013–2014 annual colony losses in the USA. Apidologie 2015, 46, 292–305. [Google Scholar] [CrossRef] [Green Version]
  14. Pirk, C.W.; Human, H.; Crewe, R.M.; van Engelsdorp, D. A survey of managed honey bee colony losses in the Republic of South Africa—2009 to 2011. J. Apic. Res. 2014, 53, 35–42. [Google Scholar] [CrossRef]
  15. Requier, F.; Andersson, G.K.S.; Oddi, F.J.; Garcia, N.; Garibaldi, L.A. Perspectives from the Survey of Honey Bee Colony Losses During 2015–2016 in Argentina. Bee World 2018, 95, 9–12. [Google Scholar] [CrossRef]
  16. Van Engelsdorp, D.; Hayes, J.; Underwood, R.M.; Pettis, J.S. A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. J. Apic. Res. 2010, 49, 7–14. [Google Scholar] [CrossRef] [Green Version]
  17. Van Engelsdorp, D.; Meixner, M.D. A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J. Invertebr. Pathol. 2010, 103, 80–95. [Google Scholar] [CrossRef] [PubMed]
  18. Amdam, G.V.; Hartfelder, K.; Norberg, K.; Hagen, A.; Omholt, S.W. Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): A factor in colony loss during overwintering? J. Econ. Entomol. 2004, 97, 741–747. [Google Scholar] [CrossRef]
  19. Dooremalen, C.; Cornelissen, B.; Poleij-Hok-Ahin, C.; Blacquière, T. Single and interactive effects of Varroa destructor, Nosema spp., and imidacloprid on honey bee colonies (Apis mellifera). Ecosphere 2018, 9, e02378. [Google Scholar] [CrossRef] [Green Version]
  20. Traynor, K.S.; Mondet, F.; de Miranda, J.R.; Techer, M.; Kowallik, V.; Oddie, M.A.; Chantawannakul, P.; McAfee, A. Varroa destructor: A complex parasite, crippling honey bees worldwide. Trends Parasitol. 2020, 36, 592–606. [Google Scholar] [CrossRef]
  21. Morawetz, L.; Köglberger, H.; Griesbacher, A.; Derakhshifar, I.; Crailsheim, K.; Brodschneider, R.; Moosbeckhofer, R. Health status of honey bee colonies (Apis mellifera) and disease-related risk factors for colony losses in Austria. PLoS ONE 2019, 14, e0219293. [Google Scholar] [CrossRef]
  22. Döke, M.A.; Frazier, M.; Grozinger, C.M. Overwintering honey bees: Biology and management. Curr. Opin. Insect Sci. 2015, 10, 185–193. [Google Scholar] [CrossRef]
  23. Goulson, D.; Nicholls, E.; Botías, C.; Rotheray, E.L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 2015, 347, 1255957. [Google Scholar] [CrossRef]
  24. Steinmann, N.; Corona, M.; Neumann, P.; Dainat, B. Overwintering is Associated with Reduced Expression of Immune Genes and Higher Susceptibility to Virus Infection in Honey Bees. PLoS ONE 2015, e0129956. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. van der Zee, R.; Pisa, L.; Andonov, S.; Brodschneider, R.; Charrière, J.-D.; Chlebo, R.; Coffey, M.F.; Crailsheim, K.; Dahle, B.; Gajda, A.; et al. Managed honey bee colony losses in Canada, China, Europe, Israel and Turkey, for the winters of 2008-9 and 2009-10. J. Apic. Res. 2012, 51, 100–114. [Google Scholar] [CrossRef]
  26. van der Zee, R.; Brodschneider, R.; Brusbardis, V.; Charrière, J.-D.; Chlebo, R.; Coffey, M.F.; Dahle, B.; Drazic, M.M.; Kauko, L.; Kretavicius, J.; et al. Results of international standardised beekeeper surveys of colony losses for winter 2012-2013: Analysis of winter loss rates and mixed effects modelling of risk factors for winter loss. J. Apic. Res. 2014, 53, 19–34. [Google Scholar] [CrossRef] [Green Version]
  27. Kuchling, S.; Kopacka, I.; Kalcher-Sommersguter, E.; Schwarz, M.; Crailsheim, K.; Brodschneider, R. Investigating the role of landscape composition on honey bee colony winter mortality: A long-term analysis. Sci. Rep. 2018, 8, 12263. [Google Scholar] [CrossRef]
  28. Jacques, A.; Laurent, M.; Epilobee Consortium Ribière-Chabert, M.; Saussac, M.; Bougeard, S.; Budge, G.E.; Hendrikx, P.; Chauzat, M.P. A pan-European epidemiological study reveals honey bee colony survival depends on beekeeper education and disease control. PLoS ONE 2017, 12, e0172591. [Google Scholar] [CrossRef] [Green Version]
  29. Switanek, M.; Crailsheim, K.; Truhetz, H.; Brodschneider, R. Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate. Sci. Total Environ. 2017, 579, 1581–1587. [Google Scholar] [CrossRef]
  30. Brodschneider, R.; Brus, J.; Danihlík, J. Comparison of apiculture and winter mortality of honey bee colonies (Apis mellifera) in Austria and Czech Republic. Agric. Ecosyst. Environ. 2019, 274, 24–32. [Google Scholar] [CrossRef]
  31. Moritz, R.F.A.; Erler, S. Lost colonies found in a data mine: Global honey trade but not pests or pesticides as a major cause of regional honeybee colony declines. Agric. Ecosyst. Environ. 2016, 216, 44–50. [Google Scholar] [CrossRef]
  32. Jones Ritten, C.; Peck, D.; Ehmke, M.; Patalee, M.B. Firm efficiency and returns-to-scale in the honey bee pollination services industry. J. Econ. Entomol. 2018, 111, 1014–1022. [Google Scholar] [CrossRef] [PubMed]
  33. Calderone, N.W. Insect pollinated crops, insect pollinators and US agriculture: Trend analysis of aggregate data for the period 1992-2009. PLoS ONE 2012, 7, e37235. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  34. Lippert, C.; Feuerbacher, A.; Narjes, M. Revisiting the economic valuation of agricultural losses due to large-scale changes in pollinator populations. Ecol. Econ. 2021, 180, 106860. [Google Scholar] [CrossRef]
  35. Gray, A.; Brodschneider, R.; Adjlane, N.; Ballis, A.; Brusbardis, V.; Charrière, J.D.; Chlebo, R.; FCoffey, M.; Cornelissen, B.; Amaro da Costa, C.; et al. Loss rates of honey bee colonies during winter 2017/18 in 36 countries participating in the COLOSS survey, including effects of forage sources. J. Apic. Res. 2019, 58, 479–485. [Google Scholar] [CrossRef] [Green Version]
  36. Gray, A.; Adjlane, N.; Arab, A.; Ballis, A.; Brusbardis, V.; Charrière, J.D.; Chlebo, R.; Coffey, M.F.; Cornelissen, B.; Amaro da Costa, C.; et al. Honey bee colony winter loss rates for 35 countries participating in the COLOSS survey for winter 2018–2019, and the effects of a new queen on the risk of colony winter loss. J. Apic. Res. 2020, 59, 744–751. [Google Scholar] [CrossRef]
  37. Van der Zee, R.; Gray, A.; Holzmann, C.; Pisa, L.; Brodschneider, R.; Chlebo, R.; Coffey, M.F.; Kence, A.; Kristiansen, P.; Mutinelli, F.; et al. Standard survey methods for estimating colony losses and explanatory risk factors in Apis mellifera. J. Apic. Res. 2013, 52, 1–36. [Google Scholar] [CrossRef] [Green Version]
  38. Brodschneider, R.; Gray, A.; Van der Zee, R.; Adjlane, N.; Brusbardis, V.; Charrière, J.D.; Chlebo, R.; Coffey, M.F.; Crailsheim, K.; Dahle, B.; et al. Preliminary analysis of loss rates of honey bee colonies during winter 2015/16 from the COLOSS survey. J. Apic. Res. 2016, 55, 375–378. [Google Scholar] [CrossRef] [Green Version]
  39. Grüner Bericht. In Bericht über die Situation der Österreichischen Land- und Forstwirtschaft Im Jahr 2016, 58th ed.; Bundesministerium für Land- und Forstwirtschaft, Umwelt und Wasserwirtschaft: Vienna, Austria, 2017.
  40. Krejčík, P. Situační a Výhledová Zpráva Včely, Ministery of Agriculture, Czech Republic, November 2017. Available online: http://eagri.cz/public/web/file/578792/SVZ_Vcely_2017_A4_final.pdf (accessed on 26 April 2021).
  41. Ministry of Agriculture, Forestry and Water Economy, Yearly Agriculture Report, 2016, Skopje. Available online: http://www.mzsv.gov.mk/CMS/Upload/docs/jdi/%D0%93%D0%BE%D0%B4%D0%B8%D1%88%D0%B5%D0%BD%20%D0%B7%D0%B5%D0%BC%D1%98%D0%BE%D0%B4%D0%B5%D0%BB%D1%81%D0%BA%D0%B8%20%D0%B8%D0%B7%D0%B2%D0%B5%D1%88%D1%82%D0%B0%D1%98%20%202016.pdf (accessed on 26 April 2021).
  42. Murphy, M.; Cowan, C.; Henchion, M.; O’Reilly, S. Irish consumer preferences for honey: A conjointapproach. Br. Food J. 2000, 102, 585–598. [Google Scholar] [CrossRef]
  43. Brščić, K.; Šugar, T.; Poljuha, D. An empirical examination of consumer preferences for honey in Croatia. Appl. Econ. 2017, 49, 5877–5889. [Google Scholar] [CrossRef]
  44. Champetier, A.; Sumner, D.A.; Wilen, J.E. The bioeconomics of honey bees and pollination. Environ. Resour. Econ. 2015, 60, 143–164. [Google Scholar] [CrossRef]
  45. Lee, H.; Sumner, D.A.; Champetier, A. Pollination markets and the coupled futures of almonds and honey bees: Simulating Impacts of shifts in demands and costs. Am. J. Agric. Econ. 2019, 101, 230–249. [Google Scholar] [CrossRef] [Green Version]
  46. Rucker, R.R.; Thurman, W.N.; Burgett, M. Honey bee pollination markets and the internalisation of reciprocal benefits. Am. J. Agric. Econ. 2012, 94, 956–977. [Google Scholar] [CrossRef]
  47. Rucker, R.R.; Thurman, W.N.; Burgett, M. Colony Collapse: The Economic Consequences of Bee Disease; Montana State University, Department of Agricultural Economics and Economics: Bozeman, MT, USA, 2011. [Google Scholar]
  48. Noël, A.; Le Conte, Y.; Mondet, F. Varroa destructor: How does it harm Apis mellifera honey bees and what can be done about it? Emerg. Top. Life Sci. 2020, 4, 45–57. [Google Scholar]
  49. van der Steen, J.; Vejsnæs, F. Varroa Control: A Brief Overview of Available Methods. Bee World 2021, 98, 50–56. [Google Scholar] [CrossRef]
  50. Mancuso, T.; Croce, L.; Vercelli, M. Total Brood Removal and Other Biotechniques for the Sustainable Control of Varroa Mites in Honey Bee Colonies: Economic Impact in Beekeeping Farm Case Studies in Northwestern Italy. Sustainability 2020, 12, 2302. [Google Scholar] [CrossRef] [Green Version]
  51. Vercelli, M.; Croce, L.; Mancuso, T. An Economic Approach to Assess the Annual Stock in Beekeeping Farms: The Honey Bee Colony Inventory Tool. Sustainability 2020, 12, 9258. [Google Scholar] [CrossRef]
  52. Escuredo, O.; Rodríguez-Flores, M.S.; Rojo-Martínez, S.; Seijo, M.C. Contribution to the Chromatic Characterization of Unifloral Honeys from Galicia (NW Spain). Foods 2019, 8, 233. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Rucker, R.R.; Thurman, W.N.; Burgett, M. Colony Collapse and the Consequences of Bee Disease: Market Adaptation to Environmental Change. J. Assoc. Environ. Resour. Econ. 2019, 6, 927–960. [Google Scholar] [CrossRef]
  54. Ministry of Agriculture, Forestry and Water Economy, Yearly Agriculture Report, 2017, Skopje. Available online: http://www.mzsv.gov.mk/cms/Upload/docs/GZI-2017.pdf (accessed on 26 April 2021).
  55. Český Svaz Včelařů, OBĚŽNÍK 3/2016, Praha. Available online: https://www.vcelarstvi.cz/dokumenty-cms/obeznik-3-2016.pdf (accessed on 26 April 2021).
  56. Potts, S.G.; Roberts, S.P.; Dean, R.; Marris, G.; Brown, M.A.; Jones, R.; Neumann, P.; Settele, J. Declines of managed honey bees and beekeepers in Europe. J. Apic. Res. 2010, 49, 15–22. [Google Scholar] [CrossRef]
  57. Steinhauer, N.; van Engelsdorp, D.; Saegerman, C. Prioritizing changes in management practices associated with reduced winter honey bee colony losses for US beekeepers. Sci. Total Environ. 2020, 753, 141629. [Google Scholar] [CrossRef]
  58. Kulhanek, K.; Steinhauer, N.; Wilkes, J.; Wilson, M.; Spivak, M.; Sagili, R.R.; Tarpy, D.R.; McDermott, E.; Garavito, A.; Rennich, K.; et al. Survey-derived best management practices for backyard beekeepers improve colony health and reduce mortality. PLoS ONE 2021, 16, e0245490. [Google Scholar] [CrossRef]
  59. Büchler, R.; Costa, C.; Hatjina, F.; Andonov, S.; Meixner, M.D.; Conte, Y.L.; Uzunov, A.; Berg, S.; Bienkowska, M.; Bouga, M. The influence of genetic origin and its interaction with environmental effects on the survival of Apis mellifera L. colonies in Europe. J. Apic. Res. 2014, 53, 205–214. [Google Scholar] [CrossRef] [Green Version]
  60. Ilyasov, R.A.; Lee, M.L.; Yunusbaev, U.; Nikolenko, A.; Kwon, H.W. Estimation of C-derived introgression into A. m. mellifera colonies in the Russian Urals using microsatellite genotyping. Genes Genom. 2020, 42, 987–996. [Google Scholar] [CrossRef] [PubMed]
  61. Meixner, M.D.; Uzunov, A. Genotype-environment-interactions and the occurrence of honey bee diseases affect the survival of honey bee colonies-summary from a pan-European experiment. Berl. Münch. Tierärztl. 2019, 132, 16–25. [Google Scholar]
  62. Uzunov, A.; Brascamp, E.W.; Büchler, R. The basic concept of honey bee breeding programs. Bee World 2017, 94, 84–87. [Google Scholar] [CrossRef]
  63. Moro, A.; Blacquière, T.; Panziera, D.; Dietemann, V.; Neumann, P. Host-Parasite Co-Evolution in Real-Time: Changes in Honey Bee Resistance Mechanisms and Mite Reproductive Strategies. Insects 2021, 12, 120. [Google Scholar] [CrossRef]
  64. Oddie, M.A.Y.; Dahle, B. Insights from Norway: Using Natural Adaptation to Breed Varroa-Resistant Honey Bees. Bee World 2021, 98, 38–43. [Google Scholar] [CrossRef]
  65. Hawkins, G.P.; Martin, S.J. Elevated recapping behaviour and reduced Varroa destructor reproduction in natural Varroa resistant Apis mellifera honey bees from the UK. Apidologie 2021. [Google Scholar] [CrossRef]
  66. Kovačić, M.; Puškadija, Z.; Dražić, M.M.; Uzunov, A.; Meixner, M.D.; Büchler, R. Effects of selection and local adaptation on resilience and economic suitability in Apis mellifera carnica. Apidologie 2020, 51, 1062–1073. [Google Scholar] [CrossRef]
  67. Büchler, R.; Uzunov, A.; Kovačić, M.; Prešern, J.; Pietropaoli, M.; Hatjina, F.; Pavlov, B.; Charistos, L.; Formato, G.; Galarza, E.; et al. Summer brood interruption as integrated management strategy for effective Varroa control in Europe. J. Apic. Res. 2020, 59, 764–773. [Google Scholar] [CrossRef]
  68. Eurbest. Restructuring of the Honey Bee Chain and Varroa Resistance Breeding & Selection Programme. A Pilot Study Comparing Varroa Resistant Bees under Commercial Beekeeping Conditions. Available online: https://www.eurbest.eu/resources/Leaflet/EurBeST-leaflet-en.pdf (accessed on 23 April 2021).
Table
Table 1. Number of analysed beekeeping operations from the survey according to the number of colonies per operation in Austria (AT), Czechia (CZ), and Macedonia (MK).
Table 1. Number of analysed beekeeping operations from the survey according to the number of colonies per operation in Austria (AT), Czechia (CZ), and Macedonia (MK).
Number of Colonies Per Beekeeping OperationATCZMKTotal
Up to 10 colonies821529331383
(52%)(47%)(11%)(46.3%)
11 to 2038128432697
(24%)(25%)(10%)(23.2%)
21 to 50265224107596
(17%)(20%)(35%)(20.0%)
51 to 100675391211
(4%)(5%)(30%)(7.0%)
101 to 15019172965
(1%)(2%)(10%)(2.1%)
More than 150 colonies17111341
(1%)(1%)(4%)(1.4%)
Total157011183052993
(100%)(100%)(100%)(100%)
Table
Table 2. Values used for calculations according to the number of colonies per beekeeping operation in Austria (AU), Czechia (CZ), and Macedonia (MK) based on the data from the COLOSS survey for 2016/2017.
Table 2. Values used for calculations according to the number of colonies per beekeeping operation in Austria (AU), Czechia (CZ), and Macedonia (MK) based on the data from the COLOSS survey for 2016/2017.
Number of Colonies Per Beekeeping OperationUp to 1011 to 2021 to 5051 to 100101 to 150>150Average
ATAverage no. of lost colonies per beekeeping operation1.233.176.6413.4618.8477.474.18
Average no. of weak colonies per beekeeping operation0.792.464.478.9110.0545.352.76
Average price of one colony in EUR150.00
Average honey yields in kg per colony14.00
Honey price EUR per kg12.00
Number of colonies in country (2016)354,080
Loss rate 2016/2017 (%)21.1
CZAverage no. of lost colonies per beekeeping operation0.541.453.938.4315.0023.822.28
Average no. of weak colonies per beekeeping operation0.421.022.073.665.9413.001.27
Average price of one colony in EUR90.88
Average honey yields in kg per colony15.12
Honey price EUR per kg7.84
Number of colonies in country (2016)693,069
Loss rate 2016/2017 (%)11.2
MKAverage no. of lost colonies per beekeeping operation2.554.5310.0713.7524.4819.5411.54
Average no. of weak colonies per beekeeping operation1.553.006.286.8817.2411.156.85
Average price of one colony in EUR77.1777.6372.3178.4374.9083.5676.16
Average honey yields in kg per colony9.498.398.278.437.0610.958.29
Honey price EUR per kg5.295.615.525.445.264.905.38
Number of colonies in country (2016)101,669
Loss rate 2016/2017 (%)20.3
Table
Table 3. Value of the economic losses. EUR per country stratified by beekeeping operation size, based on the sample data from the COLOSS survey for 2016/2017.
Table 3. Value of the economic losses. EUR per country stratified by beekeeping operation size, based on the sample data from the COLOSS survey for 2016/2017.
Number of Colonies Per Beekeeping OperationAT (EUR)CZ (EUR)MK (EUR)
Up to 10 colonies430,84886,66113,261
11 to 20542,046121,03022,606
21 to 50758,760239,376157,711
51 to 100387,132116,648184,223
101 to 150145,93265,39798,089
More than 150 colonies548,33471,84542,616
Total losses from lost colonies2,085,444533,133422,696
Total losses from weak colonies727,608167,82395,811
Total losses2,813,052700,955518,507
Table
Table 4. Average economic losses per beekeeping operation in EUR per country stratified by beekeeping operation size based on the data from COLOSS survey for 2016/2017.
Table 4. Average economic losses per beekeeping operation in EUR per country stratified by beekeeping operation size based on the data from COLOSS survey for 2016/2017.
Number of Colonies Per Beekeeping OperationsATCZMK
Up to 10 colonies525164402
11 to 201423426706
21 to 50286310691474
51 to 100577822012024
101 to 150768138473382
More than 150 colonies32,25565313278
Average losses per beekeeping operation based on the loss rates for 2016/201717926271700
Table
Table 5. Average economic losses per colony and country and estimated total national economic losses for Austria (AT), Czechia (CZ), and Macedonia (MK) in EUR for 2016/2017.
Table 5. Average economic losses per colony and country and estimated total national economic losses for Austria (AT), Czechia (CZ), and Macedonia (MK) in EUR for 2016/2017.
Type of Economic LossesATCZMK
Losses per one lost colony318209120
Losses per one weak colony16811946
Losses per colony before winter starts903130
Estimated national total economic loss32,031,30521,400,4013,038,741
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Popovska Stojanov, D.; Dimitrov, L.; Danihlík, J.; Uzunov, A.; Golubovski, M.; Andonov, S.; Brodschneider, R. Direct Economic Impact Assessment of Winter Honeybee Colony Losses in Three European Countries. Agriculture 2021, 11, 398. https://doi.org/10.3390/agriculture11050398

AMA Style

Popovska Stojanov D, Dimitrov L, Danihlík J, Uzunov A, Golubovski M, Andonov S, Brodschneider R. Direct Economic Impact Assessment of Winter Honeybee Colony Losses in Three European Countries. Agriculture. 2021; 11(5):398. https://doi.org/10.3390/agriculture11050398

Chicago/Turabian Style

Popovska Stojanov, Despina, Lazo Dimitrov, Jiří Danihlík, Aleksandar Uzunov, Miroljub Golubovski, Sreten Andonov, and Robert Brodschneider. 2021. "Direct Economic Impact Assessment of Winter Honeybee Colony Losses in Three European Countries" Agriculture 11, no. 5: 398. https://doi.org/10.3390/agriculture11050398

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop