University of Nebraska - Lincoln
DigitalCommons@University of Nebraska - Lincoln
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Land-use change reduces habitat suitability for
supporting managed honey bee colonies in the
Northern Great Plains
Clint R. V. O%o
United States Geological Survey%1<164)4)17
Cali L. Roth
United States Geological Survey
Benjamin L. Carlson
United States Geological Survey
Ma%hew D. Smart
United States Geological Survey/4/#3564)4)17
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Land-use change reduces habitat suitability for
supporting managed honey bee colonies in the
Northern Great Plains
Clint R. V. Otto
a,1
, Cali L. Roth
a
, Benjamin L. Carlson
a
, and Matthew D. Smart
a
a
Northern Prairie Wildlife Research Center, United States Geological Survey, Jamestown, ND 58401-7317
Edited by B. L. Turner, Arizo na State University, Tempe, AZ, and approved July 19, 2016 (received for review March 1, 2016)
Human reliance on insect pollination services continues to increase
even as pollinator populations exhibit global declines. Increased
commodity crop prices and federal subsidies for biofuel crops, such
as corn and soybeans, have contributed to rapid land-use change in
the US Northern Great Plains (NGP), changes that may jeopardize
habitat for honey bees in a part of the country that supports >40%
of the US colony stock. We investigated changes in biofuel crop
production and grassland land covers surrounding ∼18,000 regis-
tered commercial apiaries in North and South Dakota from 2006
to 2014. We then developed habitat selection models to identify
remotely sensed land-cover and land-use features that influence
apiary site selection by Dakota beekeepers. Our study demonstrates
a continual increase in biofuel crops, totaling 1.2 Mha, around reg-
istered apiary locations in North and South Dakota. Such crops were
avoided by commercial beekeepers when selecting apiary sites in
this region. Furthermore, our analysis reveals how grasslands that
beekeepers target when selecting commercial apiary locations are
becoming less common in eastern North and South Dakota, changes
that may have lasting impact on pollinator conservation efforts. Our
study highlights how land-use change in the NGP is altering the
landscape in ways that are seemingly less conducive to beekeeping.
Our models can be used to guide future conservation efforts high-
lighted in the US national pollinator health strategy by identifying
areas that support high densities of commercial apiaries and that
have exhibited significant land-use changes.
apiary selection models
|
Apis mellifera
|
land use
|
land-cover trends
|
pollinators
A
nimal pollination service is critical for sustaining ecosystem
health and human well-being (1, 2). In many terrestrial systems,
plant–pollin ator interactions provide the basic framework for all
other trophic interactions. Globally, about one-third of crop pro-
duction depends on animal pollination (3). US agricultural pro-
duction relies heavily on managed and native insects for pollination
services, with an estimated economic value of $15 billion annually
(2). Reliance on insects for pollination services is growing even as
populations of native and managed pollinators exhibit concurrent
declines (4, 5). For example, in 2013−2014, total US honey bee
colony losses were 34%, but beekeepers on average lost 51% of
their colonies (6). Declines in managed honey bees and native bees
put significant pressure on global food supplies, plant–pollinator
networks, agricultural producers, and ecosystem function (7, 8).
Proposed reasons for the declines include parasites, diseases,
agro-chemical use, forage availability, and land-use change (9, 10).
Much of the research investigating anthropogenic disturbance ef-
fects on managed and native pollinators focuses on pesticides and
less so on habitat fragmentation, land-use, and loss of forage. Al-
though a paucity of data exists for most parts of the world, recent
research indicates that land use influences honey bee habitat
availability, forage preferences, nutrition, and colony overwintering
survival (11–15). In response to reported losses of managed honey
bee colonies and declines in native pollinators, a US federal
strategy was developed by the Pollinator Health Task Force to
promote pollinator health (16). One of the three key objectives of
the federal strategy includes the establishment of 7 million acres of
pollinator habitat in the United States by 2020. The strategy also
calls for additional research on the habitat requirements and for-
aging needs of honey bees and other pollinators.
From May to October, the Northern Great Plains (NGP) re-
gion of the United States hosts ∼1 million honey bee colonies,
which represent over 40% of US registered stock (17). Com-
mercial beekeepers transport honey bee colonies to the NGP
each summer to produce a honey crop and bolster colony health.
During the winter, a majority of the commercial colonies that
spend the summer in the NGP are transported throughout the
nation to provide pollination services for crops, such as almonds,
melons, apples, and cherries, or are moved to southern states for
the production of queens and packaged honey bee colonies. In
May to June, commercial beekeepers in the NGP select apiary
locations based on landscape features that will provide abundant
forage for honey bee colonies throughout the growing season.
Beekeepers must obtain permission before establishing apiaries
on private land. Apiary locations selected by beekeepers likely
have a major influence on colony health and honey production
because bees are forced to gather resources from the local
landscape surrounding the predetermined apiary location.
The NGP has served as an unofficial refuge for commercial
beekeepers because of the abundance of uncultivated pasture
and rangelands and cultivated agricultural crops, such as alfalfa,
sunflower, and canola, that provided forage for bees throughout
the growing season. Over the past 100 y, the major agricultural
crops in this region have included small grains, flaxseed, hay,
sunflower, canola, and dry beans, all with varying forage value to
Significance
Insect pollinators are critically important for maintaining global
food production and ecosystem function. Our research in-
vestigated how land-use changes occurring in the US Northern
Great Plains (NGP) is affecting habitat for managed honey bee
colonies in a region supporting >40% of the US commercial
colony stock. Our study reveals that land-cover features used
by beekeepers when selecting apiary locations are decreasing
in the NGP and that corn and soybeans, crops actively avoided
by beekeepers, are becoming more common in areas with
higher apiary density. These findings suggest that the NGP is
rapidly changing to a landscape that is less conducive to com-
mercial beekeeping. Our models identified areas within the
NGP that can be targeted for pollinator habitat improvements.
Author co ntributions: C.R.V.O. and M.D.S. designed resear ch; C.R.V.O. and C.L.R. per-
formed research; C.L.R. and B.L.C. contributed new reagents/analytic tools; C.R.V.O.
analyzed data; and C.R.V.O., C.L.R., and M.D.S. w rote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
1
To whom correspondence should be addressed. Email: cotto@usgs.gov.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
1073/pnas.1603481113/-/DCSupplemental
.
10430–10435
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PNAS
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September 13, 2016
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vol. 113
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no. 37 www.pnas.org/cgi/doi/10.1073/pnas.1603481113
This document is a U.S. government work and
is not subject to copyright in the United States.
pollinators. Rising commodity crop prices, increased subsidies
for biofuels, such as corn-based ethanol and soy-based biodiesel,
and reduction in US Farm Bill conservation programs have fa-
cilitated rapid land-use changes in the NGP (18–20). The US
Energy and Security Act of 2007 calls for an annual production
of 36 billion gallons of liquid biofuels by 2022 (21). Long-term
land-cover trends in the region reveal a gradual shift toward
increased corn and soybean cultivation and reduction in grass-
lands and wetlands that have historically dominated much of the
NGP (22). For example, in North Dakota, there has been loss of
∼647,500 ha (1.6 million acres) of land enrolled in the US De-
partment of Agriculture (USDA) Conservation Reserve Pro-
gram (CRP) from 2006 to 201 4 (23). Additional research is
needed to understand how changes in government-managed
conservation lands and programs affect ecosystem service de-
livery and wildlife habitat in the NGP (24, 25). Although re-
newable biofuels are touted as a mechanism for increasing
energy security and potentially reducing greenhouse gas emis-
sions (but see ref. 26), little is known about how rapid expansion
of biofuel crops will impact pollinator habitat, health, and pol-
lination services. Farming practices associated with biofuel crops
in the NGP often include prophylactic use of pesticides, in-
cluding neonicotinoids, that may pose health risks to bees via
direct and indirect exposure (27, 28) and herbicide use that in-
hibits growth of noncrop plants that provide a forage base for
bees. Recent field studies conducted in the NGP have shown that
apiaries surrounded by larger scale agricultural land covers, in-
cluding biofuels, have lower honey bee colony overwintering
survival rates and increased physiological stress (14, 15).
We quantified changes in biofuel crop production and grassland
land covers around ∼18,000 registered apiary locations in North
Dakota (ND) and South Dakota (SD) from 2006 to 2014 (Fig. 1).
We then developed habitat selection models to identify remotely
sensed land-cover and land-use features that influence apiary site
selection by commercial beekeepers residing in areas of significant
land-use change within the Dakotas. Specifically, our questions
were as follows: (i) How has land cover, including biofuel crops
and grassland, surrounding registered commercial apiary locations
changed in ND and SD from 2006 to 2014? (ii)Whatareaswithin
the Dakotas exhibit substantial rates of land-cover change and also
support a large number of commercial apiaries? (iii)Whatland-
use and land-cover features do beekeepers target when selecting
commercial apiary sites? (iv) Do government conservation lands,
such as those in the CRP, influence beekeeper apiary selection
choices? By identifying land-use trends surrounding commercial
apiaries and building beekeeper habitat selection models, we
quantified how recent land-use changes, including biofuel crops,
are altering habitat for managed pollinators in the NGP.
Results
Apiary Trends: Land-Use Change and Landscape Stress. In 2006, biofuel
crops surrounding commercial apiary locations were generally
confined to far eastern portions of ND and SD (Fig. 2A). In 2014,
biofuel crop area surrounding apiaries generally expanded west
and northward across the study region, with continued intensifi-
cation in eastern ND and SD and southern SD (Fig. 2B). Our trend
analysis revealed significant annual gains in biofuel crop area around
registered apiary locations from 2006 to 2014 [
^
β
YEAR
= 9.1 ha an-
nually, 95% credible interval (CI) 8.9–9.3]. Across ND and SD,
between 2006 and 2014, there were an additional 1.2 Mha of biofuel
crops surrounding registered apiary locations. Much of the increase
inbiofuelcropareaaroundapiarieswasfocusedinthePrairie
Pothole Region (PPR) of the Dakotas, a region extending east and
north of the Missouri River in ND and SD (Fig. 3A). Average an-
nual gains in biofuel cropping area were four times greater among
registered apiaries in the PPR [
x = 10.3 ha ± 11.3 (1 SD)] than in
apiaries west or south of the Missouri River, a region also known as
the Badlands and Plains Region (BPR) (
x = 2.5 ha ± 5.7). There
were 13,038 and 5,325 registered apiary locations in the PPR and
BPR, respectively. Of the 432 apiary locations exhibiting an annual
increase in biofuel crops of >30 ha, 98% were located east or north
of the Missouri River, in the PPR. In general, counties with greater
gains in biofuel crop area tended to have higher densities of regis-
tered apiary locations, suggesting that recent expansion of corn and
soybean plantings may be encroaching into the core area of Dakota
beekeepe rs (Fig. 3A).
The grassland trend analysis revealed a systematic decrease in
grassland land cover surrounding registered apiary locations from
2006 to 2014 (
^
β
YEAR
= −0.8 ha annually, 95% CI −0.59 to −0.97).
Our interpolation model of grassland change showed that apiaries
with larger gains in biofuel cropping area also lost more grassland
(Fig. 3B). Of the 3,105 apiary locations exhibiting a >10-ha annual
decrease in grassland, 81% were located east or north of the
Missouri River, in the PPR. Areas that exhibited high levels of
grassland loss and high apiary density were generally confined to
central and southern ND and the eastern half of SD (Fig. 3B).
Apiary Selection Models. Relationships among our land-cover
and land-use covariates were highly varied, with Grassland and
Biofuels exhibiting the strongest negative correlation (
Fig. S2). All
Registered Apiary
0240120 km
Fig. 1. Location of 18,363 registered apiaries (red dots) in North and South
Dakota. Gray counties are in the Prairie Pothole Region, and white counties
are in the Badlands and Plains Region. The Missouri River, which separates
the two regions, is in blue. An apiary density map can be found in
Fig. S1.
AB
Fig. 2. Heat maps representing the spatial distribution of corn and soybean
fields in (A) 2006 and (B) 2014. Maps were created using interpolation and
data from 18,363 registered apiary locations in North and South Dakota.
Color ranges from green to yellow to red, with red representing the areas of
more corn and soybean production.
Otto et al. PNAS
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SUSTAINABILITY
SCIENCE
covariates included in the same model had correlation coeffi-
cients <0.3. Grassland was the most common land cover sur-
rounding apiaries in this region, followed by biofuel crops, small
grains, and open water (
Fig. S3). Our COMMODITY crop
model revealed that the probability of a site being used as a
commercial apiary was negatively related to our commodity crop
covariates (Fig. 4A). In general, Biofuels (−0.64; 95% CI −0.77 to
−0.50) exhibited a stronger negative correlation with site use
than Sm_Grains (−0.43; CI −0.58 to −0.28), suggesting a slightly
stronger avoidance of biofuel crops than small grain fields by
commercial beekeepers. Our HABITAT model estimated a
strong positive relationship between apiary site use probability
and grassland area (Grassland, 0.70; CI 0.56 to 0.83), alfalfa
(Alfalfa, 0.25; CI 0.13 to 0.28), and open water (Water, 0.29; CI
0.17 and 0.42) (Fig. 4B). The model revealed equivocal results
for associations between apiary site use and woodlands (Forest,
−0.016; CI −0.45 to 0.13) and sunflower fields (Sunflower, −0.04;
CI −0.18 to 0.11), with both parameters having credible intervals
that overlapped zero. Results from our CONSERVATION
model show that commercial beekeepers were more likely to use
sites with larger areas of CRP land (CRP, 0.19; CI 0.08 to 0.31)
(Fig. 4C). This model also demonstrated a weak positive re-
lationship between other state and federal lands and apiary site
selection probability (Fed_State, 0.08; CI −0.03 to 0.20); how-
ever, the credible intervals overlapped zero.
Model validation showed that all models performed better than
random in predicting use of 196 sites (
Fig. S4). Our HABITAT
and COMMODITY models yielded similar discriminatory results,
with both models having comparable area under the curve (AUC)
values and correctly discerned a higher number of validation sites
than our CONSERVATION model.
Discussion
Our study provides an empirical investigation of land-use and land-
cover change surrounding apiary locations in a region of critical
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Decrease
Increase
Increase
Decrease
A
B
Fig. 3. Heat maps representing the annual rate of change in (A) corn and
soybean or (B) grassland area from 2006 to 2014. Maps were created using
interpolation and data from 18,363 registered apiary locations in North and
South Dakota. ( A) Red represents regions with the greatest annual increase
of corn and soybean area surrounding commercial apiaries. (B) Red repre-
sents regions with the greatest annual loss of grassland area surrounding
commercial apiaries. Values within county boundaries represent the average
number of registered apiaries per 10,000 ha.
0 200 400 600
0.0
0.2
0.4
0.6
0.8
1.0
Biofuel
Grain
A
0 200 400 600 800
0.0
0.2
0.4
0.6
0.8
1.0
Use Probability