Contribution of honeybees towards the net environmental benefits of food

Abstract

Beekeeping provides honey, protein-containing drone broods and pollen, and yield-increasing pollination services. This study tested the hypothesis that beekeeping can result in net-positive impacts, if pollination services and protein-containing by-products are utilised. As a case example, Finnish beekeeping practices were used. The study was performed using two different approaches. In both approaches, the evaluated impacts were related to climate change, land use, and freshwater use, and were scaled down to represent one beehive. The first approach considered honey production with pollination services and the replacement of alternative products with co-products. The impacts were normalised to correspond with planetary boundary criteria. The second approach evaluated the impacts of the different products and services of beekeeping separately. In the first approach the honey production system moved towards a safe operational space. Freshwater use was the impact category with the largest shift towards a safe operational space (39% shift). The second approach caused a global warming potential of honey production of 0.65 kg CO2-eq kg −1 , when pollen and drone broods were considered as by-products and the influence of pollination services were not included. When honey, pollen, and drone broods were considered as co-products and pollination services were included, the impacts regarding land use and climate change were net-positive. The impact of freshwater use was relatively small. For honey, the impacts on the climate change, land use, and freshwater use were −0.33 kg CO2-eq kg −1 , −7.89 m 2 kg −1 , and 14.01 kg kg −1 , respectively. The impact allocation with co-products and pollination services was conclusive. A lack of consideration for the impact reduction of pollination led to beekeeping having a negative impact on the environment. Based on these results, beekeeping enhances food security within planetary boundaries, provided that pollination services and protein-containing by-/co-products are utilised.

Full text

Contribution of honeybees towards the net environmental benefits
of food
Jani Sillman
a,
⁎,Ville Uusitalo
a
, Tuire Tapanen
a
,Anneli Salonen
b
,Risto Soukka
a
, Helena Kahiluoto
a
a
LUT University, School of Energy Systems, Sustainability Science, P.O. Box 20, 53851 Lappeenranta, Finland
b
Finnish beekeepers' association, Ullanlinnankatu 1 A 3, 00130 Helsinki, Finland
HIGHLIGHTS
•Shifts in distances to planetary bound-
aries were quantified using LCA.
•Beekeeping reduced environmental im-
pacts of protein and sugar systems.
•Water use was reduced more than land
use and climate change.
•Sugar use and transportation induced
most beekeeping impacts.
•Including pollination revealed the net-
positive impact of beekeeping.
GRAPHICAL ABSTRACT
abstractarticle info
Article history:
Received 3 June 2020
Received in revised form 17 November 2020
Accepted 17 November 2020
Available online 3 December 2020
Editor: Deyi Hou
Keywords:
Life cycle assessment
Planetary boundary
Beekeeping
Food system
Insect
Netpositive
Beekeeping provides honey, protein-containing drone broods and pollen, and yield-increasing pollination ser-
vices. This study tested the hypothesis that beekeeping can result in net-positive impacts, if pollination services
and protein-containing by-products are utilised. As a case example, Finnish beekeeping practices were used. The
study was performed using two different approaches. In both approaches, the evaluated impacts were related to
climate change, land use, and freshwater use, and were scaled downto represent one beehive.The first approach
considered honey production with pollination services and the replacement of alternative products with co-
products. The impacts were normalised to correspond with planetary boundary criteria. The second approach
evaluated the impacts of the different products and services of beekeeping separately. In the first approach the
honey production system moved towards a safe operational space. Freshwater use was the impact category
with the largest shift towards a safe operational space (39% shift). The second approach caused a global warming
potential of honey production of 0.65 kg
CO2-eq
kg
−1
, when pollen and drone broods were considered as by-
products and the influence of pollination services were not included. When honey, pollen, and drone broods
were considered as co-products and pollination services were included, the impacts regarding land use and cli-
mate change were net-positive. The impact of freshwater use was relatively small.For honey, the impacts on the
climate change, land use, and freshwater use were −0.33 kg
CO2-eq
kg
−1
,−7.89 m
2
kg
−1
, and 14.01 kg kg
−1
,re-
spectively. The impact allocation with co-products and pollination services was conclusive. A lack of consider-
ation for the impact reduction of pollination led to beekeeping having a negative impact on the environment.
Based on theseresults, beekeeping enhances foodsecurity within planetary boundaries, providedthat pollination
services and protein-containing by-/co-products are utilised.
© 2020 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://
creativecommons.org/licenses/by/4.0/).
1. Introduction
The phenomenon of declining pollinator populations worldwide has
gained awareness (e.g., Potts et al., 2010;Lebuhn et al., 2013) due to the
key role of pollinators in food production. Klein et al. (2007) estimated
Science of the Total Environment 756 (2021) 143880
⁎Corresponding author at: LUT University, P.O. Box 20, 53851 Lappeenranta, Finland.
E-mail address: jani.sillman@lut.fi(J. Sillman).
https://doi.org/10.1016/j.scitotenv.2020.143880
0048-9697/© 2020 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Contents lists available at ScienceDirect
Science of the Total Environment
journal homepage: www.elsevier.com/locate/scitotenv

that around 35% of global crop production is dependent upon animal pol-
linators, which also maintain the biodiversity of wild plants (Aquilar et al.,
2006). The decline in pollinators is due to land use (LU) change
(Hendrickx et al., 2007;Rader et al., 2014), pesticides (Brittain et al.,
2014), pollution (Rortais et al., 2005), and decreased resource diversity
(Biesmeijer et al., 2006).Thedeclineiscriticalduetotheneedtoprovide
food for a growing population with shrinking resources (FAO, 2017;
Campbell et al., 2017). In addition to the pollination-induced yield in-
crease, pollinators can provide honey and protein sources, such as drone
broods (DBs) (Finke, 2005;Lindström et al., 2016). Alternative protein
sources have gained increasing interest in recent years for numerous rea-
sons, including possible sustainability advantages (e.g., Lindberg, 2016;
van Huis, 2013).
Pollination increases crop yields without additional LU and resource
inputs, and honeybee hives can be effectively located for this purpose
(Lindström et al., 2016). The honeybee (Apis mellifera) is a unique pollina-
tor as it provides multiple by-products in addition to pollination services.
Honey can be used as a sweetener to replace sugars from sugarcane or
sugar beet production, which require agricultural land. DBs and pollen
provide protein that can replace animal or plant-based protein sources
(Finke, 2005;Jensen et al., 2016;Lecocq et al., 2018;Komisinska-Vassev
et al., 2015). DBs have previously been regarded as waste or not consid-
ered as a product, thus they were not collected from hives. Recently,
there has been an increase in awareness concerning the potential use of
DBs and pollen as a protein source and healthy food product. However,
honey and DB production have environmental impacts through beekeep-
ing, product processing, packaging, and transporting.
Life cycle assessments (LCAs) of beehives usually focus solely on
honey production (e.g., Kendall et al., 2013;Mujica et al., 2016), despite
the importance of pollination as an ecosystem service being well-
known (Tamburini et al., 2019). There are several studies concerning
the inclusion of pollination services in LCAs, but the focus is mainly on
economic aspects or biodiversity impacts (e.g., Arzoumanidis et al.,
2019;Crenna et al., 2017;Ulmer et al., 2020). Ulmer et al. (2020)
analysed the global warming potential (GWP) of DB production with
honey production. However, pollen was not considered as a by-
product or co-product, and pollination services were considered using
an economic allocation that transfers some of the impactsof beekeeping
to pollination services. Nonetheless, the utilisation of pollination ser-
vices and by-products might cause net-positive environmental impacts
through increasing crop yields and replacing land-based protein pro-
duction. A net-positive environmental impact refers to a situation
where the impact of an activityis not negative towardsthe environment
(e.g., Renger et al., 2014;Grönman et al., 2019;Bjørn and Hauschild,
2012). To our knowledge, the environmental impacts of honey produc-
tion, such as GWP, LU, and freshwater use (FWU), with the inclusion of
pollination services and by-products, such as DB and pollen protein,
have not yet been evaluated.
One method for approaching the evaluation of the environmental
impacts of beekeeping is the planetary boundary (PB) concept
(Rockström et al., 2009;Steffen et al., 2015;Kahiluoto, 2019), to
which LCAs can be integrated (e.g., Uusitalo et al., 2019;Salas et al.,
2016). The combined results can help address several limitations of
LCA studies. For instance, the results of LCA focus on minimizing or mea-
suring the environmental impacts of certain products and services, but
LCA does not set a criterion for sustainable practices (Bjørn et al.,
2015).The results of combined LCAs and PBs indicate the extent to
which a certain system leaves or remains within a safe operation
space. Current challenges associated with the combined approach in-
clude climate change, biogeochemical flows, biosphere integrity, FWU,
and land system change, all of which impact future food security
(Campbell et al., 2017;Hanjra and Qureshi, 2010;Steffen et al., 2015).
There is an urgent need for solutions that help food systems to remain
within or return to a safe operational space.
The aim of this study was to assess the environmental impacts of bee-
keeping while including pollination services and protein-containing by-
products to decipher whether beekeeping can result in net-positive im-
pacts. The assessment consisted of a system-level comparison and
product-based environmental impacts with various allocation options.
The investigated environmental impacts were related to the PBs of cli-
mate change, land system change, and FWU. We hypothesised that
honey production would help to achieve food security within a safe oper-
ational space.
2. Materials and methods
An LCA, which was mainly based on the instructions of ISO 14040
and 14044, was used to analyse the environmental impacts of a honey
production system. All modelling was carried out using GaBi 8.7
software.
2.1. Goal and scope
The function of the LCA is to estimate the environmental impacts of
food products, such as rapeseed and beekeeping beekeeping-related
products. Honey production has numerous side-products, such as DB,
pollen, and wax, as well as providing pollination services for plants.
The aim of this study was to assess the environmental impacts of
honey production systems by providing information on the LU, FWU,
and GWP of different products. These impacts were compared to alter-
native processes that serve the same function. The honey production
system was located in Finland. To answer the research questions, two
different analyses were carried out:
1. A system expansion assessment for a comparison of the LU, GWP,
and FWU of a reference system without honey production and a
new system with honey production. The system expansion was car-
ried out specifically to studythe impacts of pollination and was based
on the instructions of ISO/TR 14049. The functional unit was a one-
year operation related to a hive.
2. The environmental impacts of LU, GWP, and FWU were calculated for
the main products of a honey production system: honey, DB protein,
and pollen protein. The environmental burden was then allocated
between these products. The impact analyses were based on the in-
structions of ISO 14067. The functional unit was the production of
1 kg of the main products.
Honey production systems consist of various life cycle stages, as pre-
sented in Fig. 1. In addition, Fig. 1 shows the system boundaries and
logic for the system expansion. The main assumption for the system ex-
pansion was that the same amounts of products and services(honey, DB
protein, pollen protein, and crops through pollination) were produced
in the honey production and reference systems. The alternative produc-
tion pathways of the reference system consisted of expanded crop pro-
duction without pollination for rapeseed and alternative sugar
production using sugar beet. The comparable protein source for DBs
was poultry, which is relatively sustainable and a widely used animal-
based protein (de Vries and de Boer, 2010), while that for pollen was
rapeseed protein. In addition, rapeseed protein and sugar from sugar
beets are already considered among the examined system of beekeep-
ing. Beeswax is also a by-product of honey production. However, bees-
wax is used for the production of new hives and therefore is assumed to
be utilised inside the system boundaries. The impact categories selected
for the system expansion were GWP (CML methodology), FWU, and
land occupation. The results from the system expansion comparison
are presented as absolute values and normalised using the PBs frame-
work according to the method introduced by Uusitalo et al. (2019).
The main aim for the second approach was to calculate the GWP, LU,
and FWU of the main products using allocation methodology. The main
product of apiaries is honey. In addition, pollen and DBs are possible co-
products due to their potential economic value (e.g., Jensen et al., 2016;
Lecocq et al., 2018;Komisinska-Vassev et al., 2015). However, DBs and
pollen were previously not usually utilised nor collected from beehives.
J. Sillman, V. Uusitalo, T. Tapanen et al. Science of the Total Environment 756 (2021) 143880
2

Therefore, there were two options for calculating the environmental im-
pacts of DBs and pollen. The first was to consider them as co-products
with economic value and perform an allocation procedure between
honey, DBs, and pollen. The other option was to consider them as
waste products without economic value and only include processes
that are needed for further processing in the environmental impact as-
sessment. In this case, the impacts from beekeeping were only allocated
to honey. In general, apiaries do not get paid for pollination services in
Finland, and therefore pollination services were not considered a prod-
uct. However, the substituted impacts of pollination services can be al-
located to the different products, which was carried out using
economic allocation due to the different natures of the products. The al-
location was based on the price of the product for the retailer. According
to experts of Finnish honey production, the prices per kg for honey, pol-
len, and DBs were 13€,65€, and 50€, respectively. To evaluate the sus-
tainability of the selected products, the impacts were compared to
those of similar products. Sensitivity analysis was performed by using
one-at-a-time method.
2.2. Life cycle inventory analysis (LCIA)
The modelling of the honey, DB, and pollen production systems were
based on primary data collected from Finnish producers and key infor-
mants. The initial primary data were collected via interviews with ex-
perts of the Finnish honey industry, which was supplemented with
beekeeper interviews. Secondary data, e.g., related to emission factors
and the reference system, were gathered from GaBi and Ecoinvent data-
bases and literature. Finland has a relatively old fleet of vehicles
(LIPASTO, 2020); thus EURO4 type vehicles were used, when transport
processes were modelled. When there was uncertainty with data qual-
ity, conservative estimates were preferred. Data quality assessment
based on the Greenhouse Gas Emissions Protocol (2011) can be found
in the attachment.
2.2.1. Beekeeping
According to the experts and productivity survey (Finnish
beekeeper's association, 2020) of beekeeping, a hive annually produces
an average of 39 kg of honey, 1 kg of DB, and 5 kg of pollen. In addition,
for efficient beekeeping, beehives consume approximately 20 kg of
granulated sugar to feed the honeybees (Luke
a
, 2020). Sugar was
assumed to be produced from sugar beets, which was modelled using
the global average sugar beet sugar production based on the Ecoinvent
database. On average, a beehive annually produces 1 kg of beeswax. It
was assumed that the beeswax was collected and transported to a
centralised separation facility, where it was melted. The melting of the
beeswax occurred in an electric oven, for which the energy consump-
tion was estimated at 0.792 kWh kg
−1
of beeswax.
According to Finnish statistics, the average mobility required for
beekeeping throughout the season is approximately 40 km per hive
(Luke
a
, 2020). However, there can be large variation regarding the mo-
bility. Ifthe hives are located close to the beekeeper's home, the mobility
may be marginal. However, due to long distances to the hives, small-
scale apiary mobility was 375 km per hive. The beekeeper's mobility
was modelled using a EURO 4 class diesel van with a 2-l engine.
Honey, DBs, beeswax, and pollen were then transported an average
of 30 km for centralised separation, production, and packaging. This dis-
tance was estimated using actual apiary locations by using a database of
the locations of hives (Apismap, 2020) in a region of Päijät-Häme in
Finland. In this study, the centralised solution for the environmental im-
pact evaluation was used because thedistributed solution is not seen as
economically feasible when large-scale production is favoured, accord-
ing to the experts. Transportation was modelled based on a EURO 4
class truck with a 2.7-t payload.
2.2.2. Honey processing and packaging
Electricity consumption in honey separation is approximately 0.23
kWh kg
−1
honey
based on energy consumption in an example apiary. Elec-
tricity production is modelled using an average grid mix for Finland.
Honey is packaged into 0.45 kg plastic containers, which is typical in
Finland. Empty plastic containers weight is 0.01 kg. Manufacturing of
plastic containers are modelled using GaBi database process for injec-
tion molding polypropylene part. Transportation distance for packed
honey to retail is approximately 10 km based on the situation in
Päijät-Häme region and it is assumed to be operated by EURO 4 class
truck with 2.7 t payload.
2.2.3. Drone brood processing and packaging
DBs were frozen and separated via screening, for which the electric-
ity consumption was estimated at 0.08 kWh kg
−1
, based on the energy
consumption of the separation device. DBs were packaged into plastic
Fig. 1. System boundaries and logic for the system expansion method.
J. Sillman, V. Uusitalo, T. Tapanen et al. Science of the Total Environment 756 (2021) 143880
3

bags. Plastic bag production was modelled usingthe GaBi database pro-
cess for plastic film production. After separation and packaging, the DBs
were returned to a freezer for health and safety reasons. The electricity
consumption of the cold chain was assumed to be 1.4 kWh kg
−1
,based
on the energy consumption of a freezer. Electricity production was
modelled using an average grid mix for Finland. As with honey, the
transportation distance to retail was 10 km, which was modelled
based on a EURO 4 class truck with a 2.7-t payload. The nutritional con-
tents of DBs are well suited for human consumption. DBs have a rela-
tively high protein content, as well as good quality fatty acids and
carbohydrates. The protein content of 100 g of fresh DBs is approxi-
mately 9.4 g (Finke, 2005). The Finnish beekeeper's association has ap-
plied for DBs to be accepted as a safe food for human consumption
according to the novel food Regulation (EU) 2015/2283.
2.2.4. Pollen processing and packaging
Pollen was collected separately. For transporting, the same vehicle as
that used for maintenance driving was used. According to an example
beekeeper, the mobility required for 1 kg of pollen was approximately
5 km. There are several ways of drying pollen, e.g., electric-oven and
air-drying. In this study, to represent a conservative estimation, it was
assumed that light fuel oil was used for drying. Based on the average
drying process in GaBi and applied moisture contents, drying consumes
approximately 0.5 MJ of thermal energy for 1 kg of pollen. The pollen
was cooled and frozen, which consumes 1.4 kWh kg
−1
of electricity
from the Finnish grid. Then, the pollen was packed into 0.25 kg plastic
packages. The plastic package production was modelled similarly to
that for honey. The transportation distance to retail was 10 km, which
was modelled based on a EURO 4 class truck with a 2.7-t payload. Bee-
collected pollen is high in nutrients and contains an average of 22.7%
protein, among other nutrients (Komisinska-Vassev et al., 2015).
2.2.5. Pollination services and crop production system
Honeybees impact crop yields through pollination. The impacts of
pollination on rapeseed yields have been chosen as a case example.
The effects of pollination were calculated based on the results of
Lindström et al. (2016), in which it was shown that rapeseed yields in
the presence of approximately two hives per hectare increased by 11%
compared to the control fields with no added hives. A similar crop in-
crease (11–15%) was presented by Korpela (1988).Inthisstudy,it
was assumed that there was the same number of beehives per hectare,
and rapeseed production increased by 11%. The protein content of rape-
seed varies between 17 and 26% (Day, 2013), with an average of 21.5%.
Rapeseed production was modelled based on the average in Finland
between 2016 and 2017, which was 1400 kg ha
−1
(The Finnish Cereal
Committee, 2019). According to Farmit (2017), the average fertiliser
use per hectare for oil crops in Finland is 111 kg of nitrogen, 11 kg of
phosphorous, and 23 kg of potassium. Fertilising was modelled using
the GaBi database processes for N-P-K, ammonium nitrate, and potas-
sium chloride fertilisers. It was assumed that 1% of the nitrogen from
fertilisers reacted to form N
2
O(Brandao et al., 2011). For the rapeseed
cultivation, the agricultural machinery was assumed to utilise 90 l of
diesel per hectare (Uusitalo et al., 2014). Cultivation was modelled
using universal tractor operations from the GaBi database. In Finland,
rapeseed is not typically irrigated, thus the direct FWU was assumed
to be zero.
2.2.6. Alternative sugar production system
In the system expansion approach, sugar was replaced with honey.
For this, sugar was assumed to be produced from sugar beets and
modelled using the global average sugar beet production based on the
Ecoinvent database. Typically, honey is regarded as sweeter than
sugar, with honey sweetness estimates varying from 1.0 to 1.5 times
the sweetness of sugar (National Honey Board, 2011). In the model, it
was assumed that 1 kg of honey can replace 1.25 kg of sugar.
2.2.7. Alternative protein production systems
DB and pollen proteins were compared to existing animal- and
plant-based proteins. There is a relatively high uncertainty concerning
the protein sources that are actually replaced, but for this study it was
assumed that DB replaces poultry protein and pollen replaces rapeseed
protein. In addition, we compared the environmental impacts of single
products from honey production systems to possible alternatives. Poul-
try is a widely used animal-based protein source and is relatively sus-
tainable compared to other common protein sources (Nijdam et al.,
2012;Mekonnen and Hoekstra, 2012). As for insects, there are several
possibilities that could be used for comparison. Mealworms are rela-
tively well studied and an efficient protein source. Thus, mealworms
were used as an insect-based protein source for comparison
(e.g., Siemianowska et al., 2013;Miglietta et al., 2015). Due to a lack of
studies concerning the environmental impacts of the selected products,
the impacts do not necessarily represent those caused by production in
Finland. Thus, all impacts should be considered as estimates. The im-
pacts of different protein sources are presented as the impact per kg of
protein. The protein content of poultry and mealworms are 20% and
18.6%, respectively (Nijdam et al., 2012;Miglietta et al., 2015). The
water use was measured as the FWU per kg of protein and LU as the
land occupation value per kg of protein. The averages and ranges of
the impacts of the selected comparable products are listed in Table 1.
2.3. Normalising LCA results to correspond to the PB criteria
Steffen et al. (2015) defined PBs for several human impacts usingab-
solute values. Concerning LCA studies, at least some of the results from
can be modified to represent the criteria used to quantify PBs
(e.g., Uusitalo et al., 2019;Salas et al., 2016). This method has also
been proposed for integrating LCA and PB by Ryberg et al. (2016).
These values can be normalised in relation to the safe operation zone
of PBs. Uusitalo et al. (2019) used the following normalisation equation:
ni¼
ri
zi
where:
n is the normalised results,
r is the modified results from the life cycle assessment,
z is the safe operational zone as an absolute value (Steffen et al.,
2015), and
i is the PB category.
In this study, we focused on three PB categories, including climate
change, FWU, and land system change. Regarding PBs, climate change
is defined according to the CO
2
concentration in the atmosphere. The
PB has been assessed to be 350 ppm (Steffen et al., 2015). Uusitalo
et al. (2019) roughly calculated that one GtCO
2
increases the atmo-
spheric concentration by 0.0796 ppm. The uncertainty related to this
enables the modification of CO
2
emissions from an LCA to ppm in the
atmosphere.
Table 1
Global warming potential, LU and freshwater consumption of poultry and mealworm
proteins.
GWP
kgCO
2-eq
/kg
protein
LU
m
2
/kg
protein
FWU
kg/kg
protein
Poultry 15 (10–30)
a
31.5 (23–40)
a
742 (596–887)
b
Mealworm 9,7 (5,3–14)
c,d,e
13,3 (8,6–18)
c,d
2780
f
a
Nijdam et al. (2012).
b
Mekonnen and Hoekstra (2012).
c
Thévenot et al. (2018).
d
Oonincx and de Boer (2012).
e
Joensuu and Silvenius (2017).
f
Miglietta et al. (2015).
J. Sillman, V. Uusitalo, T. Tapanen et al. Science of the Total Environment 756 (2021) 143880
4

Land-use change was defined by Steffen et al. (2015) as an area of
forested land as a percentage of the original forest, and for boreal, tem-
perate, and tropical forests, as a percentage of the potential forest. The
current state of global forests is 62%. The boundary for boreal forests is
85% (Steffen et al., 2015). According to the Global Forest Atlas (2018),
boreal forests span approximately 16,600,000 km
2
.
Finally,the PB for FWU was set at 4000 km
3
a
−1
(Steffen et al., 2015).
3. Results
3.1. Honey production system, reference system, and normalised PB values
The honey production system had a lower GWP, LU (occupation),
and FWU than the reference system without honey production
(Table 2). From the perspective of PBs,applying a honey production sys-
tem can assist in returning an area to a safe operational zone.
The GWP of the reference system was almost three times higher
than that of the honey production system. The maintenance driving
for apiaries (10 kgCO
2eq
), sugar production (8 kgCO
2eq
) and honey/
wax production (6 kgCO
2eq
) contributed to a major portion (77%) of
the GWP impacts of honey production. In the reference system, most
of the GWP impacts were caused by rapeseed cultivation (53 kgCO
2eq
)
and sugar production (24 kgCO
2eq
). The GWP of honey production
would be significantly higher if longer maintenance driving distances
were required. This could occur for various reasons, including small-
scale production when the beekeeper does not live close to the hives.
From the LU (occupation) perspective, honey production systems re-
quire significantly less land area. The majority of the honey production
related LU was caused by sugar production (11 m
2
). In the reference
system, rapeseed cultivation (551 m
2
), sugar production (27 m
2
), and
rapeseed production for proteins (39 m
2
) caused the majority of the
LU. The FWU of the reference system was approximately 2.4 times
higher than that of the honey production system. The FWU during
sugar production (890 kg) was the dominant factor in the honey pro-
duction system. In the reference system, the main life cycle stage that
uses freshwater was sugar production (2170 kg) (Appendix Table 1).
According to Table 2 and Fig. 2, both the honey production and ref-
erence systems impact the climate change, FWU, and land system
change. From the perspective of PBs, freshwater consumption appears
to be the most important aspect, followed by land-system change. Com-
pared to the reference system, the honey production system seems to
support the return of an area to a safe operational zone, as it causes
net-positive impacts.
3.2. Environmental impacts of beekeeping products
Table 3 presents the GWP, LU, and FWU of honey, pollen, and DBs.
For the first method, all impacts of the shared processes, such as bee-
keeping, sugar use, and pollination, were allocated to honey. For this,
we assume that DBs were previously discarded as waste. In addition,
pollen collection has just recently started, and honey production sys-
tems do not focus on theirproduction. For the second method, the emis-
sions from the shared processes were allocated between the products
based on their economic value. The impacts of pollination were pre-
sented as negative through the increased crop production of rapeseed.
The impact depends upon the allocation method. When the impact
reduction via the inclusion of pollination services was not considered
in the calculations and the pollen and DBs were considered as by-
Table 2
Environmental impactsof the system expansionapproach and normalised values to corre-
spond with PB criteria.
Honey
production
system (hive)
Reference
system
a
LCA results
GWP (kgCO
2
eq) 32 83
LU (occupation) (m
2
) 13 619
FWU (kg) 937 2239
Results modified for PB normalisation
Climate change (ppm) 2.6 × 10
−9
6.6 × 10
−9
Land system change (km
2
) 1.3 × 10
−5
6.2 × 10
−4
FWU (km
3
) 9.4 × 10
−7
2.2 × 10
−6
PB normalisation factors
Normalisation factor for climate change (ppm) 350 350
Normalisation factor for land system change
(km
2
)
10,054,000 10,054,000
Normalisation factor for fresh water use (km
3
) 4000 4000
Normalised results
Climate change 7.4 × 10
−12
1.9 × 10
−11
Land system change 1.3 × 10
−12
6.2 × 10
−11
FWU 2.4 × 10
−10
5.6 × 10
−10
a
Incorporates the environmental impacts of rapeseed, poultry protein, and sugar beet
production without beekeeping.
Fig. 2. Normalised impacts in the PB framework for honey production and reference systems.
J. Sillman, V. Uusitalo, T. Tapanen et al. Science of the Total Environment 756 (2021) 143880
5

products, the GWP of 1 kg of honey production wasapproximately 0.65
kgCO
2eq
. However, when DBs and pollen were considered as co-
products, the GWP reduced by 32%. Furthermore, the inclusion of polli-
nation services caused a further reduction in the GWP. For these cases,
the impacts became net-positive. Therefore, honey production can
help an area to stay within the PBs. Compared to by-products, the
GWP was reduced by approximately 50% for pollen and 75% for DBs
when allocated as co-products. When pollination services were in-
cluded in thecalculations, the impact becamenet-positive. Similar shifts
occur for other impact categories of different products when different
methods of impact distribution are performed.
When the sustainability was evaluated via environmental impacts
without pollination services, by-products containing protein compared
well with the alternative products (Tables 1 and 3;Appendix Table 1).
The impacts of DBs on the GWP, LU, and FWU were minimal compared
to those of poultry production. When the impacts were allocated to DBs,
the difference becomes moderate. However, the DBs are still the most
sustainable alternative in all studied impact categories. Notably, the dif-
ference between the FWUs was significant. When comparing the
sustainability of DBs and mealworms, DBs were favoured when consid-
ered a by-product. When DBs were considered a co-product, the GWP
and LU impacts were very similar. However, the impact of DBs on the
FWU was significantly lower than that of mealworms. When the impact
reduction of pollination services was included, the impact of DBs was
net-positive, making DBs superior compared to poultry or mealworms
regarding sustainability.
3.3. Sensitivity analysis
Maintenance driving and sugar consumption cause significant
shares of emissions for different beekeeping products. In addition,
both factors have a relatively large range of values, of which the average
estimate was used in the GaBi model. Hence, the sensitivities of these
variables were investigated. Maintenance driving and the amount of
sugar have both good data quality (attachment).
Sugar for feeding bees is responsible for 32% of GWP, 83% of LU and
95% of FWU of beekeeping, when 20 kg sugar is needed per hive. This
leads to 10.4 kg kgCO
2eq
,11.2m
2
LU and 890 kg FWU. If varying sugar
use from 15 to 25 kg per hive the results would vary for GWP
7.8–13.0 kgCO
2eq
,forLU8.4–14.0 m
2
and for FWU 667.5–1112.5 kg.
Maintenance drivingis one of the key factors in GWP but it does not
have a significant impact on LU or FWU. The basic assumption was that
total maintenance driving is 40 km per hive whichleads to 8.6 kgCO
2eq
.
If hives are close to the farmer's home and the required driving is only
5 km then GWP is only 1.1 kgCO
2eq
. With some of the small-scale apiar-
ies that are located far from farmers' home drivingcan be 375 km which
would lead to 80.6 kgCO
2eq
. However, this can be considered not as a
typical case.
4. Discussion
4.1. Sustainability and validity of the findings
The results show clear environmental benefits from the perspectives
of GWP, LU, and FWU, when comparing food production with beekeep-
ing to food production without beekeeping. When only the impacts of
beekeeping were considered, the GWP, LU, and FWU were impacted.
However, when considering systemic benefits, e.g., pollinating services
or product replacement, the impact reductions were significant. In
fact, beekeeping can havea net-positive impact on the system. Including
the impact reduction of pollination services with beekeeping causes less
land occupation and greenhouse gas emissions than the beekeeping
alone. Regarding water use, the studied system caused FWUimpacts de-
spite the inclusion of pollination services. However, rapeseed farming
does not typically require irrigation in Finland, thus an increase in the
rapeseed yield was not apparent in the FWU value. If the studied system
requires irrigation, the FWU can also become net-positive.
To decipher the validity of the impact evaluation, the results of this
study were compared to those of other studies. Provided that the im-
pacts of shared processes were solely allocated to honey and the bene-
fits of pollination were not considered, the carbon footprint of honey
was 0.65 kgCO
2eq
kg
−1
.Kendall et al. (2013) calculated that the carbon
footprint of honey produced in the U.S. was 0.67–0.92 kgCO
2eq
kg
−1
,for
which the main contributor was the transportation of beehives. Mujica
et al. (2016) calculated the carbon footprint of honey production in
Argentina. According to their study, the carbon footprint of honey pro-
duction was approximately 2.5 kgCO
2eq
kg
−1
, of which honey extrac-
tion was responsible for 90.7%. In our study, unlike in the U.S.,
honeybees and hives were not transported. In addition, the honey
extraction emissions in this study were significantly lower than those
presented by Mujica et al. (2016) due to the significantly lower electric-
ity consumption duringthe extraction process. The demand for electric-
ity as well as the amount of sugar consumed per hive as assumed in this
study, was similar to that presented by Ulmer et al. (2020) for two ex-
ample cases in Germany.
Table 3
Global warming potential (kgCO
2eq
), LU (m
2
a), and FWU (kg) for honey, pollen, and DBs
with different allocation factors for the beekeeping processes.
1 kg of honey
Allocation of beekeeping
processes
100% 57%
GWP LU FWU GWP LU FWU
Maintenance driving by a
farmer, hives, and wax
0.23 0.02 0.00 0.13 0.01 0.00
Sugar production 0.27 0.29 22.82 0.15 0.16 13.01
Honey transportation for
processing
0.01 0.00 0.00 0.01 0.00 0.00
Honey processing 0.15 0.02 1.00 0.15 0.02 1.00
Honey transportation for retail 0.00 0.00 0.00 0.00 0.00 0.00
Total without pollination 0.65 0.32 23.82 0.44 0.19 14.01
Pollination −1.35 −14.13 0.00 −0.77 −8.06 0.00
Total −0.70 −13.81 23.82 −0.33 −7.86 14.01
1 kg of pollen protein
Allocation of beekeeping
processes
0% 37%
GWP LU FWU GWP LU FWU
Maintenance driving by a
farmer, hives, and wax
0.00 0.00 0.00 2.87 0.23 0.00
Sugar production 0.00 0.00 0.00 3.40 3.66 290.13
Pollen collecting and
transportation for processing
3.93 0.30 0.00 3.93 0.30 0.00
Pollen processing 1.99 0.37 6.51 1.99 0.37 6.51
Pollen transportation for retail 0.01 0.00 0.00 0.01 0.00 0.00
Total without pollination 5.93 0.67 6.51 12.20 4.56 296.64
Pollination 0.00 0.00 0.00 −17.21 −179.70 0.00
Total 5.93 0.67 6.51 −5.01 −175.14 296.64
1 kg of drone brood protein
Allocation of beekeeping
processes
0% 6%
GWP LU FWU GWP LU FWU
Maintenance driving by a
farmer, hives, and wax
0.00 0.00 0.00 5.62 0.45 0.00
Sugar production 0.00 0.00 0.00 6.65 7.17 568.09
Drone brood transportation for
processing
0.09 0.01 0.00 0.09 0.01 0.00
Drone brood processing 3.35 1.15 0.00 3.35 1.15 0.00
Drone brood transportation for
retail
0.02 0.00 0.00 0.02 0.00 0.00
Total without pollination 3.46 1.16 0.00 15.73 8.78 568.09
Pollination 0.00 0.00 0.00 −33.70 −351.86 0.00
Total 3.46 1.16 0.00 −17.97 −343.08 568.09
J. Sillman, V. Uusitalo, T. Tapanen et al. Science of the Total Environment 756 (2021) 143880
6

The impact evaluation of the comparison between the honey pro-
duction and reference systems includes high uncertainty related to the
products that were replaced with pollen and DB. In addition, it is possi-
ble that because pollen and DBs are new products, there are no appro-
priate direct replacements. This uncertainty was also raised by Ulmer
et al. (2020). However, our results show that the replacement of poultry
and rapeseed proteins has a marginal impact on the results compared to
sugar replacement and the advantages of pollination services. There-
fore, changes in the assumptionsrelated to crop productivity with rape-
seed pollination, sugar required for beekeeping, and sugar replacement
by honey may have considerable impacts on the results. In addition,
when investigating the impact reduction of pollination services, the re-
duction differs greatly depending upon the crop, fruit, or berries that are
used. Therefore, when using the approach presented in this study to in-
vestigate the possible net-positive impacts of otherfood production sys-
tems with beekeeping, impact reduction should be evaluated case by
case depending upon the target of the pollination services. In addition,
the focus of this study was beekeeping in Finland. Different locations
have specific climatic conditions that influence crop yields and beekeep-
ing. For these reasons, the results cannot be used to estimate theimpact
of beekeeping in countries with different climatic and ecological condi-
tions. To estimate the exact environmental impacts of beekeeping in
other countries, the effects of pollination services and other factors
should be estimated according to those countries. Despite these uncer-
tainties, the results show clear environmental benefits. Thus, it can be
argued that beekeeping should be maintained or improved in areas
with crops requiring pollination, which could result in net-positive en-
vironmental impacts.
The impacts of the different products became more case dependent
after system expansion, when using different allocation methods, and
after product replacement. By using different allocation methods, the
assessment can be modified to achieve the wanted values. Thus, the al-
location method should be standardised for LCAs considering beekeep-
ing. For instance, the variation in the environmental values of DBs is
greatly dependent upon how the impacts are allocated and whether
the DBs are considered by-products or co-products (Table 3). When
the impact reduction of the pollination services was included in the cal-
culations, the results provided a more systematic evaluation of the im-
pacts of beekeeping. Without beekeeping, no benefits can be gained
from pollination services. With this in mind, the situation for bee-
keepers is unfavourable, if the impact reduction of pollination services
is given to crop farmers or not considered at all.
In Finland, the most important product from beekeeping is honey.
However, DBs and pollen have higher economic values per kg of the prod-
uct. The amount of DBs and pollen produced is over ten times less than
that of honey and their use is still marginal. Considering the bulk prices
of the products in Finland, honey accounts for over 57% of the economic
value of the products from beekeeping, if DBs and pollen are utilised.
However, life cycle cost analysis was not performed in this study. Thus,
more detailed research is required to investigate whether it is economi-
cally feasible to produce DBs and pollen as protein sources along with
honey. Considering how the impacts are divided among different prod-
ucts of beekeeping, the situation becomes different for honey production
in other countries where pollination services account for a major portion
of the economic value (e.g., Ulmer et al., 2020). In these cases, the eco-
nomic allocation should be conducted differently (e.g., Arzoumanidis
et al., 2019). Furthermore, future variation in the prices of pollen and
DBs due to changes in the supply and demand will have an influence on
how the impacts are distributed among the products.
4.2. Limitations of the LCA PB approach
The conversion of the LCA results to the absolute values of PBs pro-
duces some shortcomings (e.g., Bjørn et al., 2019;Ryberg et al., 2016).
For instance, this study did not consider local water scarcity issues and
the LU was estimated based on the occupied area. In this study, it was
assumed that the unused land area was boreal forest, which is not nec-
essarily the case. In addition, the occupied boreal forest does not influ-
ence the climate change values in this study. Another limitation of the
method used in this study is how companies, organisations, or institu-
tions understand their roles in comparison to others, especially others
operating in the same market segments, when considering safe opera-
tional space. Despite these uncertainties, this study shows that it is pos-
sible to use the methodology developed by Uusitalo et al. (2019) to
other kinds of systems than their example in a flexible manner. This
study integrated LCA and PB to a system with different kinds of products
and services and compared them with other similar systems. However,
further research is required to overcome the shortcomings related to
the methodology of combined LCAs and PBs.
Biodiversity is a PB that has exceeded the safe operation space
(Campbell et al., 2017;Steffen et al., 2015). However, this impact category
was not modelled in this study. The impacts on biodiversity are complex
and there are several influencing factors regarding pollinators, such as cli-
mate change, LU, pesticides, pollination services, and local conditions
(Biesmeijer et al., 2006;Brittain et al., 2014;Hendrickx et al., 2007;
Rader et al., 2014;Rortais et al., 2005). Methods incorporating LCAs to
evaluate the biodiversity impacts of pollinators are still being developed
(Crenna et al., 2017), which is why the impacts on biodiversity were
not included in this study. However, the results of decreased greenhouse
gas emissions and LU indicates that honey production can have a positive
influence on biodiversity. In addition, beekeeping can be seen to have
positive impacts on biodiversity, for instance by increasing the pollination
services for wild plants (Potts et al., 2010).
4.3. Honey production can enhance food security withoutthe additional use
of resources
Regarding the DB and pollen production capacity, the production is
relatively minor, with approximately 1 kg of DBs and 5 kg of pollen
per hive per year. According to the Finnish beekeeper's association
(2020), there are approximately 70,000 active hives in Finland. There-
fore, theoretically, the maximum production capacities of DBs and pol-
len are 70 and 350 tons, respectively. This corresponds to 6.6 tons of
protein from DBs and 79.5 tons of protein from pollen. Regarding
honey, the annual production is approximately 2730 tons per year.
However, the annual increase in the yields of crops, fruits, and berries
due to pollination services might be more significant than the honey
production itself, as is shown in the case of rapeseed production. For in-
stance, the production capacity of rape and rapeseed in Finland was ap-
proximately 71 thousand tons in 2018 (Luke
b
, 2020). If all cultivation
areas of rape and rapeseed have at least two bee hives per hectare,
which increases the yield by 11%, this would mean that approximately
7036 tons of rapeseed are annually produced due to bee farming. As-
suming that the average protein content is 21.5%, this corresponds to
a production of 1512 tons of plant-based protein per year. Based on
these assumptions, beekeeping can have a positive impact onfood secu-
rity through increased protein and sweetener production with reduced
environmental impacts. However, these values are based on assump-
tions. Therefore, more research is required concerning the influence of
honeybees on the pollination of crop yields in large-scale.
Given that similar net-positive impacts are possible for other food
systems, the phenomenon of de creasing pollinator populations is severe
in the context of sustainability goals and food security issues, as approx-
imately 35% of cultivated crops are dependent upon pollinators. In an
economical manner pollination has a huge impact on agriculture. For in-
stance, it has been estimated that pollination has a direct economic ben-
efit of approximately 585€per hectare for oilseed rape farming in
Ireland (Stanley et al., 2013;Breeze et al., 2016). Globally, the value of
pollination has been evaluated at 153 €billion in 2005 (Gallai et al.,
2009). If the phenomenon of decreasing populations is not halted, anal-
ternative method for influencing food production is required.
Otherwise, food security is in danger of being compromised due to
J. Sillman, V. Uusitalo, T. Tapanen et al. Science of the Total Environment 756 (2021) 143880
7

decreased crop yields and the loss of products from honey production.
However, the results of this study show that it is possible to increase
food production without the additional use of resources in areas with-
out proper beekeeping practices. To create the possibility of net-
positive impacts and increase food security by increasing the yields of
some crops and co-products of beekeeping, beekeeping with crops re-
quiring pollination services should be maintained and possibly even im-
proved. For instance, the balance between a suitable amount of
pesticides and beehives in different crop production areas should be in-
vestigated, as the use of pesticides contributes towards the declining
pollinator populations (Brittain et al., 2014).
5. Conclusions
In this study, a novel approach was used to estimate environmental
impacts of beekeeping. The results of LCA were converted to represent
PB criteria and consider the impact of pollination services, which has
previously not been done. The results show that beekeeping can help
the food sector to remain within safe operation spaces concerning
three impact categories. The impact categories were GWP, LU, and
FWU. From the perspective of PBs, the biggest impact reduction was
FWU. When the impacts were considered as product-based, the GWP
and LU impacts were net-positive, given that pollination services were
included in the calculations. Based on the impact values of the assess-
ment, it is strongly recommended that beekeeping is increased in
areas where possible, as there are clear benefits regarding sustainability
and food security. The knowledge can help decision makers plan more
sustainable food systems and aid beekeepers in estimating theirpositive
influence on food systems and marketing their pollination services.
However, more research is required concerning different systems with
different crops to show how beekeeping affects overall food systems
and their environmental impacts.
CRediT authorship contribution statement
Conceptualization Ideas; formulation or evolution of overarching research goals
and aims
Methodology Development or design of methodology; creation of models
Software Programming, software development; designing computer
programs; implementation of the computer code and
supporting algorithms; testing of existing code components
Validation Verification, whether as a part of the activity or separate, of
the overall replication/reproducibility of results/experiments
and other research outputs
Formal analysis Application of statistical, mathematical, computational, or
other formal techniques to analyse or synthesize study data
Investigation Conducting a research and investigation process, specifically
performing the experiments, or data/evidence collection
Resources Provision of study materials, reagents, materials, patients,
laboratory samples, animals, instrumentation, computing
resources, or other analysis tools
Data curation Management activities to annotate (produce metadata),
scrub data and maintain research data (including software
code, where it is necessary for interpreting the data itself) for
initial use and later reuse
Writing - Original
draft
Preparation, creation and/or presentation of the published
work, specifically writing the initial draft (including
substantive translation)
Writing - Review &
editing
Preparation, creation and/or presentation of the published
work by those from the original research group, specifically
critical review, commentary or revision –including pre-or
postpublication stages
Visualization Preparation, creation and/or presentation of the published
work, specifically visualization/data presentation
Supervision Oversight and leadership responsibility for the research
activity planning and execution, including mentorship
external to the core team
Project
administration
Management and coordination responsibility for the research
activity planning and execution
Funding
acquisition
Acquisition of the financial support for the project leading to
this publication
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
This paper is a part of the SIRKKA (A74136) and the REISKA
(A70561) projects funded by the European Regional Development
Fund.
Appendix A
Appendix Table 1
Environmental impacts of the system expansion approach.
Honey production system
GWP LU (occupation) FWU
kgCO
2
eq m
2
kg
Maintenance driving by a farmer and hives 8.6 0.6 0.0
Sugar production 10.4 11.2 890.0
Transportation for processing 0.4 0.0 0.0
Honey and wax processing 6.0 0.7 39.2
Pollen processing 2.3 0.4 7.4
Drone brood processing 0.3 0.1 0.0
Pollen collecting 4.4 0.3 0.0
Transportation for retail 0.1 0.0 0.0
Total 32.6 13.5 936.5
Reference system
GPW LU (occupation) FWU
kgCO
2
eq m
2
kg
Rapeseed cultivation 52.8 551.2 0.0
Poultry protein production 1.4 3.0 69.7
Sugar production 24.3 27.4 2169.4
Rapeseed protein production 3.6 37.8 0.0
Transportation 0.4 0.0 0.0
Total 82.5 619.4 2239.1
Appendix B. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.scitotenv.2020.143880.
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