POLLINATORS POLLINATION AND FOOD PRODUCTION

THE ASSESSMENT REPORT ON POLLINATORS, POLLINATION AND FOOD PRODUCTION
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3. THE STATUS AND TRENDS IN POLLINATORS
AND POLLINATION
land use in that area, Bartomeus et al. (2013) found that
aggregate native species richness declines were modest
outside of the genus Bombus; the number of rarefied non-
Bombus bee species per time period has declined by 15%,
but the trend is not statistically significant (p = 0.07).
A third example of re-sampling of bees, in Colorado, USA,
used a century-old record of bee fauna that had found 116
species in grassland habitats (Kearns and Oliveras, 2009a).
The re-sampling, a five-year effort, recorded 110 species,
two genera of which were not present in the original 1907
collection. Their comparison was hampered by the lack of
information about the sampling techniques of the original
study, and taxonomic changes, but the authors concluded
that the conservation of most of the original species had
been facilitated by the large amount of preserved habitat in
the study area (Kearns and Oliveras, 2009b). An even longer
re-sampling period of 120 years in Illinois, in temperate
forest understory, found a degradation of interaction network
structure and function, with extirpation of 50% of the original
bee species (Burkle et al., 2013). The authors attributed
much of this loss to shifts in both plant and bee phenologies
that resulted in temporal mismatches, nonrandom species
extinctions, and loss of spatial co-occurrences between
species in the highly modified landscape. Thus negative
changes in the degree and quality of pollination seem to be
ameliorated by habitat conservation.
Examination of museum specimens has also been shown
to provide insights into reasons for bee population declines.
Pollen analysis from 57 generalist bee species caught before
1950 showed that loss of preferred host plants was strongly
related to bee declines, with large-bodied bees (which
require more pollen) showing greater declines than small
bees (Scheper et al., 2014).
In a meta-analysis of long-term observations across Europe
and North America over 110 years, Kerr et al. (2015) looked
for climate change–related range shifts in bumble bee
species across the full extents of their historic latitudinal and
thermal limits, and changes along elevation gradients. They
found consistent trends from both continents with bumble
bees failing to track warming through time at their northern
range limits, range losses from southern range limits, and
shifts to higher elevations among southern species. These
effects were not associated with changing land uses or
pesticide applications.
A monitoring program for butterflies in the Flanders region
of Belgium (Maes and Van Dyck, 2001) provides evidence
for that region having the highest number of butterfly
extinctions in Europe, with 19 of the original 64 indigenous
species having gone extinct. Half of the remaining species
are now threatened with extinction. The authors attribute
these losses to more intensive agricultural practices and the
expansion of building and road construction (urbanization),
which increased the extinction rate more than eight-fold in
the second half of the 20 th century.
In the absence of population trend data, studies of species
diversity can also provide some information about the status
of pollinators. Studies such as those of Keil et al. (2011) for
Syrphidae, and another study of species of bees, hoverflies
(Syrphidae) and butterflies (Carvalheiro et al., 2013) are
examples of this. Carvalheiro et al. (2013) looked at these
three groups of pollinators in Great Britain, Netherlands,
and Belgium for four consecutive 20-year periods (1930-
2009). They found evidence of extensive species richness
loss and biotic homogenization before 1990, but those
negative trends became substantially less accentuated
during recent decades, even being partially reversed for
some taxa (e.g., bees in Great Britain and Netherlands). They
attributed these recoveries to the cessation of large-scale
land-use intensification and natural habitat loss in the past
few decades. Most vulnerable species had been lost by the
1980s from the bee communities in the intensively farmed
northwestern European agricultural landscapes, with only
the most robust species remaining (Becher, 2013; Heikkinen
et al., 2010, Casner et al., 2014; Holzschuh, 2008). New
species are continuously colonizing north-western Europe
from the much richer Central and South European regions.
This may also contribute to increases of insect pollinator
richness. Bartomeus et al. (2013) found that bee species
with lower latitudinal range boundaries were increasing in
relative abundance in the northeastern USA, and Pyke et
al. (2016) compared altitudinal distributions of bumble bees
in the Colorado Rocky Mountains from 1973 and 2007 and
found that queens had moved up in altitude by an average of
80m. Also, uphill shifts in bumble bee altitudinal distributions
have been recorded in the Cantabrian Cordillera of northern
Spain during the last 20 years leading to local extinctions
and bee fauna homogenization where previously there were
distinct community differences (Ploquin et al., 2013).
Temperature increases can directly affect bee metabolism
but there have also been significant temperature-related
changes in the phenology of floral resources important for
pollinators, including earlier flowering of most species, and
changes in the seasonal availability of flowers that may also
affect pollinator survivorship (Aldridge et al., 2011). Forrest
(2015) reviewed research on plant–pollinator mismatches,
and concluded that although certain pairs of interacting
species are showing independent shifts in phenology (a
mismatch), only in a few cases have these independent
shifts been shown to affect population vital rates (seed
production by plants) but this largely reflects a lack of
research. Bartomeus et al. (2011) combined 46 years of
data on apple flowering phenology with historical records
of bee pollinators over the same period, and found that for
the key pollinators there was extensive synchrony between
bee activity and apple peak bloom due to complementarity
between the bees’ activity periods. Differential sensitivity