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Despite widespread concern about declines in pollination services, little is known about the patterns of change in most pollinator assemblages. By studying bee and hoverfly assemblages in Britain and the Netherlands, we found evidence of declines (pre-versus post-1980) in local bee diversity in both countries; however, divergent trends were observed in hoverflies. Depending on the assemblage and location, pollinator declines were most frequent in habitat and flower specialists, in univoltine species, and/or in nonmigrants. In conjunction with this evidence, outcrossing plant species that are reliant on the declining pollinators have themselves declined relative to other plant species. Taken together, these findings strongly suggest a causal connection between local extinctions of functionally linked plant and pollinator species.
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domain substituted by the hydrophobic tail of
H-Ras was not (Fig. 4D). Ra c1 is of parti c ul ar
importance to Fc receptor-mediated phagocytosis
and accumulates at the base of forming phago-
somes, detaching rapidly upon sealing (Fig. 4, E
and F, and fig. S7A) (10). Rac1(Q61L) also de-
tached from sealing phagosomes with kinetics
indistinguishable from those of wild-type Rac1
(Fig. 4, G and H, and movie S7). Because
Rac1(Q61L) is constitutively bound to guanosine
triphosphate (GTP), its dissociation from phago-
somes was not due to nucleotide hydrolysis or
cessation of nucleotide exchange. Instead, release
waslikelymediatedbytermination of its electro-
static association with the plasmalemma. Accord-
ingly, the C-terminal tail of Rac1 containing the
polybasic domain behaved similarly (fig. S7B).
Our data indicate that the surface potential of
the inner leaflet of the membrane decreases locally
during phagosome formation. The change is at-
tributable primarily to depletion of PIP
and PS,
but depletion of phosphatidylinositol 4-phosphate
was also observed (fig. S3 and movie S5). Activa-
tion of inositide lipases, kinases, and phosphatases
occurs during phagocytosis and bacterial invasion
(3), readily accounting for the changes in PIP
could be converted to PE by decarboxylation or
could be externalized during phagocytosis by
scramblases and/or efflux pumps.
Our results also indicate that the anchor-
age of important signaling molecules, includ-
ing K-Ras and Rac1, can be modulated focally
by localized changes in surface potential. Other
proteins anchored electrostatically to the mem-
brane, such as MARCKS, are equally suscepti-
ble to the charge alterations that accompany
lipid remodeling. Indeed, we also obtained
evidence for localized detachment of the
tyrosine kinase c-Src (fig. S5, B and C).
The consequences of altered surface charge in
other important biological phenomena must be
considered. Activation of phosphoinositide metab-
olism, elevation in cytosolic calcium, and PS
flipping occur after stimulation of multiple
receptors and channels as well as during apoptosis.
The effect of such responses on inner surface
potential may be measurable with the use of
approaches like the one described here. Cycles of
membrane dissociation/reassociation may add a
layer of functional control to complement the
traditional biochemical mode of regulation of sig-
naling proteins.
References and Notes
1. M. Olivotto, A. Arcangeli, M. Carla, E. Wanke, Bioessays
18, 495 (1996).
2. S. McLaughlin, A. Aderem, Trends Biochem. Sci. 20, 272
3. R. J. Botelho, C. C. Scott, S. Grinstein, Curr. Top.
Microbiol. Immunol. 282, 1 (2004).
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5. See supporting material on Science Online.
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8298 (2000).
7. J. B. McCabe, L. G. Berthiaume, Mol. Biol. Cell 12, 3601
8. J. F. Hancock, H. Paterson, C. J. Marshall, Cell 63, 133
9. D. Michaelson et al., J. Cell Biol. 152, 111 (2001).
10. A. D. Hoppe, J. A. Swanson, Mol. Biol. Cell 15, 3509
11. We thank E. Pick for providing Rac1 and D. Russell for
providing Nucleosil beads. Supported by the Canadian
Institutes for Health Research and an NIH grant, by a
Canadian Institutes of Health Research studentship (T.Y.),
and by the Pitblado Chair in Cell Biology (S.G.).
Supporting Online Material
Materials and Methods
Figs. S1 to S7
Movies S1 to S7
4 May 2006; accepted 5 June 2006
Parallel Declines in Pollinators and
Insect-Pollinated Plants in
Britain and the Netherlands
J. C. Biesmeijer,
S. P. M. Roberts,
M. Reemer,
R. Ohlemu¨ ller,
M. Edwards,
T. Peeters,
A. P. Schaffers,
S. G. Potts,
R. Kleukers,
C. D. Thomas,
J. Settele,
W. E. Kunin
Despite widespread concern about declines in pollination services, little is known about the
patterns of change in most pollinator assemblages. By studying bee and hoverfly assemblages in
Britain and the Netherlands, we found evidence of declines (pre- versus post-1980) in local bee
diversity in both countries; however, divergent trends were observed in hoverflies. Depending on
the assemblage and location, pollinator declines were most frequent in habitat and flower
specialists, in univoltine species, and/or in nonmigrants. In conjunction with this evidence,
outcrossing plant species that are reliant on the declining pollinators have themselves declined
relative to other plant species. Taken together, these findings strongly suggest a causal connection
between local extinctions of functionally linked plant and pollinator species.
nthropogenic changes in habitats and
climates have resulted in substantial re-
ductions in biodiversity among many
vertebrate taxa (1), and evidence has been ac-
cumulating that insect biodiversity is at risk as
well (2). Of particular concern is the possibility
of community-level cascades of decline and
extinction (3), whereby decline of some ele-
ments of the biota lead to the subsequent loss of
other species that directly or indirectly rely upon
them. Here we examine sets of pollinators and
the plants that they pollinate to test (i) whether
species that are linked to one another within
communities show coincident declines and (ii)
whether species with more links within com-
munities are more robust to change because of
the availability of alternative links, if an inter-
acting species is lost.
Any loss in biodiversity is a matter of public
concern, but losses of pollinating insects may
be particularly troubling because of the poten-
tial effects on plant reproduction. Many agricul-
tural crops and natural plant populations are
dependent on pollination and often on the ser-
vices provided by wild, unmanaged, pollinator
communities. Substantial concerns have been
raised about the decline or loss of these services
E(4) but see (5)^, culminating in formal rec-
ognition within the Convention on Biological
Diversity (6)intheS,o Paulo Declaration (7)
and the International Initiative for the Conser-
vation and Sustainable Use of Pollinators (8).
However, the evidence for such declines re-
mains scanty (5).
To adequately demonstrate a decline in pol-
linator services, one would need to document
(i) overall declines in pollinator density; and/or
(ii) reductions in species diversity or substantial
shifts in the species composition of pollinator
communities, combined with changes in the
distribution of traits represented in those com-
munities (thus indicating that the loss of some
pollinators has not been compensated by the
rise of functionally equivalent species); and (iii)
declines in either the reproductive success or
abundance of plant species dependent on these
pollinators. No suitable data are available to
address overall pollinator density, but here we
provide evidence for the remaining points,
using data for bees, hoverflies, and plants from
Britain and the Netherlands.
We compiled almost 1 million records for
bee (all native species except the largely
Institute of Integrative and Comparative Biology and Earth
and Biosphere Institute, University of Leeds, Leeds, LS2 9JT,
Centre for Agri-Environmental Research, University of
Reading, Reading, RG6 6AR, UK.
European Invertebrate
Survey–Netherlands/National Museum of Natural History
Naturalis, Postbus 9517, 2300 RA Leiden, Netherlands.
Department of Biology, University of York, York, YO10 5YW,
Lea-side, Carron Lane, Midhurst, GU29 9LB, West
Sussex, UK.
Department of Animal Ecology, Bargerveen
Foundation, Radboud University of Nijmegen, Postbox 9010,
6500 GL Nijmegen, Netherlands.
Nature Conservation and
Plant Ecology Group, Wageningen University and Research
Centre, Bornesteeg 69, 6708 PD Wageningen, Netherlands.
Umweltforschungszentrum–Centre for Environmental Re-
search Leipzig-Halle, Community Ecology (Biozo
schung), Theodor-Lieser-Strasse 4, 06120 Halle, Germany.
*To whom correspondence should be addressed. E-mail: SCIENCE VOL 313 21 JULY 2006
domesticated honeybee Apis mellifera)and
hoverfly observations for both countries from
national entomological databases (9), focusing
on areas with extensive sets of observations
before and after 1980. We then applied
rarefaction methods to compare species rich-
ness of focal areas over each period (10). This
approach allows valid comparisons between
time periods, despite unequal sample sizes and
the incorporation of records collected by many
recorders who used different collecting tech-
niques over long time spans (10).
Bee diversity declined in large fractions
of the 10 km by 10 km cells analyzed in both
countries (Fig. 1). Bee richness was measured
as the number of distinct species; significant de-
creases in richness were observed in 52% and
È67% of British and Dutch cells, respectively, as
compared with richness increases in 10% and 4%
of cells in the two countries (table S1). Shifts in
hoverfly diversity were less consistent (Fig. 1),
with no significant directional change in richness
for the UK (increases in 25% and decreases in
33% of British cells); however, increases in
hoverfly richness were reported in 34%, versus
decreases in 17%, of Dutch cells (table S1).
These shifts in species richness reflect
shifts in the distributions of many species in
both groups. Our data set does not allow di-
rect measurement of population densities of
the species involved; nonetheless, shifts over
time in the relative number of records for dif-
ferent species can be used as an indicator of
their relative frequency and ubiquity (10).
There has been an increase in the domination of
the pollinator communities of both countries by
a smaller number of species. For both taxa in
both countries, about 30% fewer species ac-
count for half of the post-1980 records (percent-
ages of fewer species: British bees, 29%;
British hoverflies, 29%; Netherlands bees,
32%; Netherlands hoverflies, 36%). In Britain,
the species that increased were dispropor-
tionately the ones that were already common
before 1980; however, in the Netherlands, this
The functional diversity of pollination net-
works contributes to the maintenance of diver-
sity in plant communities (12), with different
groups of pollinators being complementary in
their pollination services and different groups
of plants being complementary in their roles as
food plants for pollinators. Consequently, a de-
cline in pollinator diversity might have little
effect on a community if the fluctuating species
were functionally similar. However, the traits
of increasing and declining species of solitary
bees and hoverflies differ in consistent ways
(Table 1). In both countries and in both groups,
species with narrow habitat requirements have
experienced greater relative declines. In solitary
bees, oligolectic species (those using few flower
taxa as food sources) have declined significant-
ly in Britain, and long-tongued taxa have
declined significantly in the Netherlands. Die-
tary specialization is important in hoverflies as
well, with both adult and larval diets being
strongly related to changes in hoverfly occur-
rence. Migratory hoverflies have fared better
than nonmigratory species in both countries. In
Britain, bee and hoverfly declines are greater
among species with only a single generation per
year; however, this pattern is not found in the
Netherlands. The significant trends indicate that
specialized species Ei.e., in habitat and dietary
requirements and, arguably, tongue length
(12, 13)^ and species characterized by slower
development and lower mobility (those having
fewer generations per year and being non-
migratory) tend to decline more than general-
ist, fast developing, and more mobile species.
Such shifts in pollinator traits suggest pos-
sible shifts in pollination services. Indeed,
recent experiments have shown that the func-
tional diversity of pollinators can affect diver-
sity in plant communities (12). We know of no
data that will allow us to assess directly
whether rates of pollinator visitation or pollen
depositiontoflowershave shifted appreciably
in Britain or the Netherlands. We can, however,
examine shifts in plant species distributions
using floral inventories from both countries
(10, 14, 15) to see whether shifts in plants are
consistent with the observed shifts in pollina-
tors. In Britain, obligately outcrossing plants
reliant on insect pollinators were declining on
average; species reliant on abiotic (wind or
water mediated) pollination were increasing;
and self-pollinating plant species showed an in-
termediate response (Table 2). In the Nether-
lands, changes were not significantly different
among these three groups; however, given the
observed decline in bees and increase in hov-
erflies in the Netherlands, divergent trends
between bee-pollinated plants and other insect-
pollinated plants may be expected there. After
reexamining the data on the insect taxa reported
as pollinators of outcrossing plants (15), we
found that, on average in the Netherlands, plants
that were exclusively pollinated by bees were
declining, but plants pollinated by flies and other
insects (including bees) were increasing. If the
changes among bee-pollinated outcrossers, out-
Fig. 1. Bee and hoverfly richness has changed in many of the 10 km by 10 km cells analyzed for
Britain and the Netherlands. Some British cells contained adequate data only on eusocial or only
on solitary bees (10). Changes in species richness were calculated from rarefaction analyses (10).
21 JULY 2006 VOL 313 SCIENCE
crossers with abiotic pollination, and predomi-
nantly self-pollinating plants are compared, the
trends observed in the Netherlands mirror those
for Britain: Bee-dependent plants have declined,
abiotically pollinated plants have increased, and
plants mainly relying on self-pollination have
shown an intermediate response (Table 2).
We cannot tell from these data whether the
decline of the plants precedes the loss of the
associated pollinators, whether the decline of
the pollinators leads to the loss of reproductive
function and then to the decline of the plants, or
indeed whether the plants and their pollinators
are both responding to some other factor. How-
ever, the results clearly show that linked ele-
ments in biological communities (i.e., specialist
pollinators and the obligately outcrossed plants
that they pollinate) are declining in tandem.
Furthermore, the difference between the two
countries implies that there is probably a causal
link, because it is the corresponding groups of
plants and pollinators in both countries that are
changing. The hypothesis that species that rely
on a broader range of other species within a
community are more robust in the face of change
is supported by the following evidence: Polli-
nators that rely on few plants for their resources
have declined the most, whereas generalists
have prospered Ecompare with (16)^. Moreover,
the decline of bees (specialized as pollinators)
relative to hoverflies (having broader feeding
habits) could be interpreted in this light.
Demonstrating that there are shifts in pol-
linator assemblages and associated changes in
wild plant communities in two countries does
not prove the existence of a global pollination
crisis. Britain and the Netherlands are not only
two of the countries with the best available data
but also two of the most densely populated and
anthropogenically modified landscapes on the
planet. Few British habitats can be thought of
as truly natural, and in the Netherlands the
landscape is largely artificial. Nonetheless, it
seems probable that shifts similar to those
documented for these countries will be found
in other parts of northwest Europe and, in-
creasingly, in other regions (17). Documenting
the geographical extent of the declines shown
here is a priority for future research. It is also
important to begin mechanistic studies of the
causes of these declines, with habitat alteration
(18), climate change (19–21), and agricultural
chemical usage (18, 22) being potential key drivers
of observed shifts (23).
1. S. L. Pimm, G. J. Russell, J. L. Gittleman, T. M. Brooks,
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6. Convention on Biological Diversity (
7. International Pollinators Initiative, the Sa
o Paulo Decla-
ration on Pollinators (Brazilian Ministry of the Environ-
ment, 1999); (
8. Agricultural Biodiversity–International Initiative for the
Conservation and Sustainable Use of Pollinators
9. Dutch data on bees are held in the Apidae database of
the European Invertebrate Survey–Netherlands (EIS-NL).
Dutch data on hoverflies are held in the Syrphidae
database of EIS-NL, the Dutch Youth Organisation for
Nature Study, and the Dutch Entomological Society.
British bee data were compiled by S.P.M.R., M.E., and
J.C.B. from data of the UK Bees, Wasps, and Ants
Recording Society. British hoverfly data were obtained
from the National Biodiversity Network
(, largely based on the Hoverfly
Recording Scheme.
10. Materials and methods are available as supporting
material on Science Online.
11. Results of a Mann-Whitney test comparing pre-1980 cell
totals for significantly declining versus significantly
increasing species: British bees, P 0 0.005; British
Table 1. Trait-based patterns in pollinator declines. Proportions are based on species that showed
significant change in the number of cells (n) in which they were reported during the two time
periods (pre- and post-1980). Declining solitary bee and hoverfly species tend to be found more
among the specialists (characterized by narrow habitat ranges, limited dietary choice, slower
development, and greater residency) than among generalist species (characterized by wide habitat
ranges, broader dietary choice, multiple generations per year, and greater tendency toward
migration). Traits were assigned by using methodologies in (25)and(26). Bumblebees and
honeybees were excluded from the analysis (10). Oligo, oligolectic; Poly , polylectic; Uni, univoltine;
Multi, multivoltine; Macro, macroorganisms; Micr o, microorganisms; Res, resident; Mig, migran t.
Britain Netherlands
Solitary bees
Trait Trait category Pn Trait category Pn
(proportion declining) (proportion declining)
Habitat range Narrow Wide Narrow Wide
(0.90) (0.25) 0.0001 32 (0.83) (0.53) 0.090 29
Flower specificity Oligo Poly Oligo Poly
(0.86) (0.41) 0.034 34 (0.55) (0.76) 0.198 36
Tongue length Long Short Long Short
(0.70) (0.41) 0.099 56 (1.00) (0.51) 0.028 49
Generations Uni Multi Uni Multi
(0.60) (0.14) 0.042 44 (0.76) (0.55) 0.433 42
Trait Trait category Pn Trait category Pn
(proportion declining) (proportion declining)
Habitat range Narrow Wide Narrow Wide
(0.96) (0.28) 0.0001 53 (0.52) (0.25) 0.025 67
Adult food Narrow Wide Narrow Wide
(0.63) (0.41) 0.095 60 (0.53) (0.16) 0.0001 86
Larval food Macro Micro Macro Micro
(0.74) (0.43) 0.009 59 (0.59) (0.20) 0.002 79
Generations Uni Multi Uni Multi
(0.80) (0.29) 0.0001 50 (0.43) (0.38) 0.63 88
Migration Res Mig Res Mig
(0.63) (0.20) 0.01 64 (0.46) (0.17) 0.025 88
Table 2. Mean relative change (TSE) in distribution of British (27) and Netherlands (28)plant
species according to their main pollen vector (10). Insect-pollinated outcrossing plants in Britain and
bee-pollinated outcrossing plants in the Netherlands have declined, whereas plants with abiotic
pollination have increased. Plant breeding systems were derived by combining the ECOFL OR (29)and
BIOLFL OR (30) databases (10). British data were tested with an analysis of variance and a post hoc
Tukey test. Netherlands data were tested with a Kruskal-Wallis test and a post hoc multiple comparison
test. Superscripts indicate group differences based on post hoc tests. n, number of plant species; NL,
Obligatory outcrossing,
insect pollinated
Obligatory outcrossing,
wind or water pollinated
self pollinating
Britain –0.22 T 0.06* þ0.18 T 0.14
–0.003 T 0.70*
(n 0 75) (n 0 30) (n 0 116)
Netherlands þ0.10 T 0.08 þ0.18 T 0.08 –0.08 T 0.11 0.091
(n 0 182) (n 0 160) (n 0 143)
NL bee plants –0.12 T 0.13* þ0.18 T 0.08
–0.08 T 0.11*
(n 0 42) (n 0 160) (n 0 143) SCIENCE VOL 313 21 JULY 2006
hoverflies, P G 0.0001; Netherlands bees, P 0 0.07 (the
reverse trend); Netherlands hoverflies, P 0 0.10.
12. C. Fontaine, I. Dajoz, J. Meriguet, M. Loreau, PLoS Biol. 4,
e1 (2006).
13. M. Stang, P. G. L. Klinkhamer, E. Van der Meijden, Oikos
112, 111 (2006).
14. C. D. Preston, D. A. Pearman, T. D. Dines, New Atlas of
the British and Irish Flora: An Atlas of the Vascular Plants
of Britain, Ireland, the Isle of Man, and the Channel
Islands (Oxford Univ. Press, Oxford, 2002).
15. Biobase 2003, Centraal Bureau voor de Statistiek,
Voorburg/Heerlen, The Netherlands (2003).
16. J. Memmott, N. M. Waser, M. V. Price, Proc. R. Soc.
London Ser. B 271, 2605 (2004).
17. J. Banaszak, Ed. Changes in Fauna of Wild Bees in
Europe (Pedagogical University, Bydgoszcz, Poland,
18. J. A. Foley et al., Science 309, 570 (2005).
19. C. D. Thomas et al., Nature 427, 145 (2004).
20. M. S. Warren et al., Nature 414, 65 (2001).
21. C. Parmesan, G. Hoyle, Nature 421, 37 (2003).
22. P. G. Kevan, Biol. Conserv. 7 , 301 (1975).
23. A Europe-wide assessment of the risks associated with
pollinator loss and its drivers is currently being under-
taken within the 6th European Union Framework
Programme–Assessing Large-scale Environmental Risks
for Biodiversity with Tested Methods project [GOCE-CT-
2003-506675 (], of which this
study is a core element (24).
24. J. Settele et al., GAIA 14, 69 (2005).
25. S.P.M.R. compiled trait data of European bees from
published sources (see
26. M. Speight, E. Castella, J.-P. Sarthou, C. Monteil, Eds.,
Syrph the Net on CD, Issue 2. The Database of European
Syrphidae (Syrph the Net Publications, Dublin, 2004).
27. Change indices from (14) were calculated from occu-
pancy data in surveys conducted from 1930 to 1969 and
from 1987 to 1999.
28. Comparison of the number of 5 km by 5 km cells
occupied in 1940 and 1990. Data from Biobase (15)
were organized into frequency classes by A.P.S. (10).
29. The Ecological Flora of the British Isles at the University
of York (
30. S. Klotz, I. Ku
hn, W. Durka, Eds. BIOLFLOR: A Database
on Biological and Ecological Traits of the German Flora
(Bundesamt fu
r Naturschutz, Bonn, 2002).
Supporting Online Material
Materials and Methods
Figs. S1 and S2
Tables S1 and S2
24 March 2006; accepted 6 June 2006
Crystal Structure of a Divalent
Metal Ion Transporter CorA at
2.9 Angstrom Resolution
Said Eshaghi,
Damian Niegowski,
Andreas Kohl,
Daniel Martinez Molina,
Scott A. Lesley,
r Nordlund
CorA family members are ubiquitously distributed transporters of divalent metal cations and are
considered to be the primary Mg
transporter of Bacteria and Archaea. We have determined a
2.9 angstrom resolution structure of CorA from Thermotoga maritima that reveals a pentameric cone–
shaped protein. Two potential regulatory metal binding sites are found in the N-terminal domain that
bind both Mg
and Co
. The structure of CorA supports an efflux system involving dehydration and
rehydration of divalent metal ions potentially mediated by a ring of conserved aspartate residues at
the cytoplasmic entrance and a carbonyl funnel at the periplasmic side of the pore.
ivalent metal cations are essential co-
factors in many proteins. To provide
cells with appropriate concentrations
of divalent metal cations, highly regulated
transporters and channels have evolved to
translocate these ions across the hydrophobic
membranes. CorA is one of the best studied
families of divalent cation transporters (1–9).
It is considered to be the primary Mg
porter of both Bacteria and Archaea and is
ubiquitously distributed (8). Sequence homolo-
gies between members of this family are most
pronounced at the C termini; sequence conser-
vation in the N termini is less significant (fig.
S1). The overall sequence similarity between
eukaryotes and prokaryotes is weak, except for
the highly conserved Gly-Met-Asn (GMN)
motif close to the C termini (10, 11). Never-
theless, some eukaryotic CorA family members
show overlapping activities with the prokary-
otic members that suggests functional, as well
as structural, conservation (4, 10, 12, 13).
Studies of CorA from Salmonella typhimurium,
Escherichia coli, and the Archaeon Methano-
coccus jannaschii demonstrate that ions can be
transported in both directions (1–3, 5, 8, 9).
Kehres and Maguire recently reported two
classes of CorAs among Bacteria and Archaea
(8). The second class, CorA-II, which differs
from the extensively studied S. typhimurium
and E. coli CorAs, was suggested to contain
two transmembrane helices, with both termini
in the cytosol. In the same report, the CorA-II
proteins were suggested to be efflux systems.
Moreover, a novel CorA-related protein, ZntB,
was recently identified in S. typhimurium (14).
ZntB was shown to be a Zn
efflux system
with two predicted transmembrane helices and
both termini facing the cytosol (15). This is in
contrast with the predicted topology of S.
typhimurium and E. coli CorA, with three trans-
membrane helices and the N terminus facing
the periplasm.
Here, we report the crystal structure of a
full-length CorA homolog from Thermotoga
maritima,at2.9) resolution. The recently
reported structure of a pentameric full-length
CorA at 3.9 ) was used for molecular
replacement, revealing two pentamers in
the asymmetric unit (16). The structure has
been refined to an R of 27.6% and an R
29.5% with good stereochemistry (table S1).
The CorA structure reveals a pentamer with
the shape of a cone (Fig. 1). The tip of the cone
is formed by two transmembrane (TM) helical
segments from each monomer and the large
opening of the cone by the N-terminal region
of CorA. The fold of the CorA monomer is
composed of an N-terminal a/b domainwitha
central seven-stranded mixed b sheet lined by
three small helices. Two long a helices cover
one face of the a/b domain and form a bundle
together with a giant a helix 7 constituted by
È70 residues. The C-terminal end of helix 7
constitutes the first transmembrane segments
(residues 291 to 312). Following the large helix
7 is helix 8 (residues 327 to 349), which forms
the second TM helix and packs in a ring around
the TM segment of helix 7 (Fig. 1).
Thermotoga maritima CorA is most closely
related to the class II CorA with both N- and
C-terminal ends facing the cytosol and, there-
fore, is likely to be primarily involved in ion
efflux. The localization of the N termini in the
cytoplasm is also supported by the positive-
inside rule (17)andtheN
topology of
Bhelical hairpin[ structures (18). Sequence
alignment of close homologs of T. maritima
CorA and those of S. typhimurium CorA sup-
port the proposal for two distinct classes of
CorA (fig. S1).
Our structure agrees in all general features
with the structure determined by Lunin et al.
(16) that was used for phasing. However, be-
cause of the higher resolution of 2.9 ), our
structure provides more details of functionally
important regions, including potential regulato-
ry metal binding sites beyond the metal in site 1
(M1) identified in the 3.9 ) structure. Two
putative metal-binding sites are found at each
interface between the N-terminal domains in
the pentamer (Fig. 2). An anomalous difference
map of Co
-soaked crystals shows that Co
Division of Biophysics, Department of Medical Bio-
chemistry and Biophysics, Karolinska Institute, SE-171 77
Stockholm, Sweden.
Department of Biochemistry and
Biophysics, Stockholm University, S-106 91 Stockholm,
Joint Center for Structural Genomics and
Genomics Institute of the Novartis Research Foundation,
San Diego, CA 92121, USA.
*These authors contributed equally to this work.
†To whom correspondence should be addressed. E-mail: (P.N.); (S.E.)
21 JULY 2006 VOL 313 SCIENCE
... Bees (Hymenoptera: Apoidea) are considered the most effective pollinator insects, thus guaranteeing one of the most valuable ecosystem services (Porto et al. 2020) by allowing plant reproduction (Ollerton et al. 2011), maintaining food security (Montoya et al. 2021) and ultimately having a high relevance for global Sustainable Development Goals (Patel et al. 2021;Díaz et al. 2015). It is thus especially worrying the recently documented decline of wild bees (all bee species except the domesticated honeybee) in different countries (Biesmeijer et al. 2006), though the magnitude of such decline is still debated given that the conservation status of most wild bee species remains unknown to date (see Nieto et al. 2014 for Europe). Land-use change, including the expansion of cities (urbanization), seems however to be particularly detrimental (Goulson et al. 2015). ...
... Insects are among the organisms with the largest diversity in urbanized environments (Corcos et al. 2019) and provide several ecosystem services (Hall et al. 2017). However, bees (Biesmeijer et al. 2006) and other non-hymenopteran flower visitors (Deguines et al. 2012) have been reported to decline as a 1 3 46 Page 2 of 23 consequence of increasing urbanization (but see Hall et al. 2017 andBaldock et al. 2019), with potential impacts on pollination service. The expansion of cities causes natural habitats to be reduced, fragmented and substituted mostly by impervious surfaces (i.e. ...
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Land-use change, including urbanization, is known to affect wild bee (Hymenoptera: Apoidea) diversity. However, while previous studies have focused on differences across local urbanization gradients, to the best of our knowledge, none focused on differences among cities at a wide geographical scale. We here used published data for wild bee communities in 55 cities across the globe, in order to explore how city traits (popula-tion density, city size, climate and land-use parameters) affect both taxonomic (diversity, distinctness, dominance) and functional (body size, nesting strategy, sociality, plant host specialization) profile of urban bee communities. By controlling for sample size and sampling effort, we found that bigger cities host few parasitic and oligolectic species, along with more above-ground-nesting bees. Cities with highly fragmented green areas present a lower proportion of oligolectic species and a higher proportion of both social species and large-bodied bees. Cities with more impervious surfaces seem to host a lower proportion of below-ground-nesting bees. Hotter cities present both a lower richness and diversity, with functional diversity highest at intermediate precipitation values. Overall, it seems that high levels of urbanization-through habitat modification and the "heat island" effect-lead to a strong simplification of the functional diversity of wild bee communities in cities. Our results may help explain the previously observed variable response of some bee community traits across local urbanization gradients.
... Managed honey bees (Apis mellifera) in particular have received a great deal of attention, with an estimated 59% reduction in the number of colonies in North America alone [38]. Wild native pollinators, including bumble bees, solitary bees, butterflies, and moths, have also experienced substantial population losses [39][40][41]. In 2017, the rusty-patched bumble bee (Bombus affinis) became the first federally listed endangered bee under the U.S. Endangered Species Act (U.S. Fish & Wildlife Service, Federal Register 82 FR 3186). ...
... More than 80% the world's flowering plants depend on animal pollination [45]. Of these, outcrossing and rare plants are particularly susceptible to pollinator declines [46,47], and may themselves decline as a result [40]. Crop production is also vulnerable to the loss of insect pollinators. ...
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Globally, grasslands have been heavily degraded, more so than any other biome. Grasslands of the eastern U.S. are no exception to this trend and, consequently, native biota associated with the region’s >20 million ha of agricultural grasslands are under considerable stress. For example, grassland associated breeding bird populations have declined precipitously in recent decades as have numerous species of pollinators. Although there is increasing awareness of the role grasslands can play in global carbon cycles and in providing high quality dietary proteins needed by an increasing global population, there is a lack of awareness of the alarming trends in the sustainability of the native biota of these ecosystems. Here, we present the status of this conservation challenge and offer prospective solutions through a working lands conservation approach. Such a strategy entails maintaining appropriate disturbances (i.e., grazing, fire, and their combination), improved grazing management, an increased reliance on native grasses and forbs, and improved plant diversity within pastures. Furthermore, we note some examples of opportunities to achieve these goals, offer suggestions for agricultural and conservation policy, and provide a framework for evaluating tradeoffs that are inevitably required when pursuing a multi-purpose grassland management framework.
... Hoverflies have also recently been recognised for their roles in pollination, pest control and in decomposing organic material (Bugg et al. 2008, Pineda & Marcos-García 2008, Ssymank et al. 2008, Rotheray & Gilbert 2011, Martínez-Falcón et al. 2012, Inouye et al. 2015, Klecka et al. 2018, Dunn et al. 2020, Moerkens et al. 2021. The large amount of biological data available for the family (e.g., Speight 2020, van Steenis et al. 2020, combined with the known relationship between declines of pollinators and plant communities (Biesmeijer et al. 2006), has led the IUCN to develop a European Red List for Syrphidae (IUCN 2018). The need for this Red List is even more urgent given the recent insights into massive losses of insects and specifically hoverflies over the last 50 years (Seibold et al. 2019, Hallmann et al. 2021, Wagner et al. 2021. ...
The hoverfly species Platycheirus torei Barkalov, 2013 is recorded from Europe for the first time. It was collected in a palsa mire in Seitajaure, northern Sweden, representing a westward extension of its potential range by 3,500 km. The properties of the palsa mire at Seitajaure are described and a list of additional hoverfly species recorded there is provided. A differential diagnosis of Platycheirus torei is provided, with all cited characters illustrated in the accompanying illustrations. An extensive discussion is given on palsa mires, with special attention to their predicted loss due to climate change, and the potential risk that represents for hoverfly species that depend on palsa mires for their survival in Europe.
... As pollinators, bees are of indisputable economic and ecological value [101,102]. This is also true for orchid bees, key pollinators of plants from approximately 30 families, including valuable crops and many species of orchids. ...
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To accommodate an ever-increasing human population, agriculture is rapidly intensifying at the expense of natural habitat, with negative and widely reported effects on biodiversity in general and on wild bee abundance and diversity in particular. Cities are similarly increasing in area, though the impact of urbanisation on wild bees is more equivocal and potentially positive in northern temperate regions. Yet agriculture and urbanisation both lead to the loss and alteration of natural habitat, its fragmentation, a potential reduction in floral availability, and warmer temperatures, factors thought to be drivers of wild bee decline. They have also been shown to be factors to which wild bee populations respond through morphological change. Body size is one such trait that, because of its relation to individual fitness, has received growing attention as a morphological feature that responds to human induced modification in land use. Here, we investigated the change in body size of two sympatric orchid bee species on the Yucatan Peninsula of Mexico in response to urbanization and agricultural intensification. By measuring 540 male individuals sampled from overall 24 sites, we found that Euglossa dilemma and Euglossa viridissima were on average smaller in urban and agricultural habitats than in natural ones. We discuss the potential role of reduced availability of resources in driving the observed body size shifts. Agricultural and urban land management in tropical regions might benefit wild bees if it encompassed the planting of flowering herbs and trees to enhance their conservation.
Accurate identification of flower position and orientation is an essential prerequisite for robotic pollinators to accomplish precise targeted pollination and improve the pollen utilisation rate. To accurately identify the pollination position and orientation of kiwifruit flowers, this study presents a vision-based information perception approach for automatically detecting flowers and accurately identifying their positions and orientations. After using YOLO v4 to identify the kiwifruit flower, the contour detection algorithm was used to detect the contour boundary of the flower pistil area and the contour boundary of the minimum circumscribed circle of the petals, and fit the centres of gravity of the pistil contour and the petal contour according to the two contours respectively. The line connecting the two centre points was used as the central axis representing the growth direction of the flowers, achieving precise identification of the flower position and orientation. After building a robotic pollinator, an experiment was conducted to identify kiwifruit flower targets and a performance test experiment was performed to target pollinated kiwifruit flowers in a kiwifruit orchard with a mechanical arm based on flower position and orientation. The experimental results showed that the precision of the identification of kiwifruit flowers was 95.27%, the success rate of the mechanical arm for target pollination based on flower position and orientation identification was 89.59%, the average pollination time was 6 s⋅per flower, and the pollination efficiency was 20 h⋅ha⁻¹. The identification algorithm of flower position and orientation proposed in this study can improve the precision and success rate of robotic pollination.
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Wild bees form diverse communities that pollinate plants in both native and agricultural ecosystems making them both ecologically and economically important. The growing evidence of bee declines has sparked increased interest in monitoring bee community and population dynamics using standardized methods. Here, we studied the dynamics of bee biodiversity within and across years by monitoring wild bees adjacent to four apple orchard locations in Southern Pennsylvania, USA. We collected bees using passive Blue Vane traps continuously from April to October for 6 years (2014–2019) amassing over 26,000 bees representing 144 species. We quantified total abundance, richness, diversity, composition, and phylogenetic structure. There were large seasonal changes in all measures of biodiversity with month explaining an average of 72% of the variation in our models. Changes over time were less dramatic with years explaining an average of 44% of the variation in biodiversity metrics. We found declines in all measures of biodiversity especially in the last 3 years, though additional years of sampling are needed to say if changes over time are part of a larger trend. Analyses of population dynamics over time for the 40 most abundant species indicate that about one third of species showed at least some evidence for declines in abundance. Bee family explained variation in species‐level seasonal patterns but we found no consistent family‐level patterns in declines, though bumble bees and sweat bees were groups that declined the most. Overall, our results show that season‐wide standardized sampling across multiple years can reveal nuanced patterns in bee biodiversity, phenological patterns of bees, and population trends over time of many co‐occurring species. These datasets could be used to quantify the relative effects that different aspects of environmental change have on bee communities and to help identify species of conservation concern. Six years of bee monitoring shows that bee biodiversity is highly dynamic from month to month and across years. Looking across 40 species, 1/3 show evidence of declining abundance over time.
Black queen cell virus (BQCV) is a severe threat to the honeybee ( Apis mellifera ) worldwide. Although several BQCV strains have been reported in China, the molecular basis for BQCV pathogenicity has not been well understood. Thus, a reverse genetic system of BQCV is required for studying viral replication and its pathogenic mechanism. Here, the complete genome sequence of BQCV was obtained from honeybees using reverse transcription PCR (RT-PCR), namely a BQCV China-GS1 strain (KY741959). Then, a phylogenetic tree was built to analyse the genetic relationships among BQCV strains from different regions. Our results showed that the BQCV China-GS1 contained two ORFs, consistent with the known reference strains, except for the BQCV China-JL1 strain (KP119603). Furthermore, the infectious clone of BQCV was constructed based on BQCV China-GS1 using a low copy vector pACYC177 and gene recombination. Due to the lack of culture cells for bee viruses, we infected the healthy bees with infectious clone of BQCV, and the rescued BQCV resulted in the recovery of recombinant virus, which induced higher mortality than those of the control group. Immune response after inoculated with BQCV further confirmed that the infectious clone of BQCV caused the cellular and humoral immune response of honeybee ( A. mellifera ). In conclusion, the full nucleotide sequence of BQCV China-GS1 strain was determined, and the infectious clone of BQCV was constructed in this study. These data will improve the understanding of pathogenesis and the host immune responses to viral infection.
Several management practices have been suggested to mitigate the global pollinator decline in agro‐ecosystems, including wildflower strips and Farming with Alternative Pollinators (FAP). FAP proposes to dedicate 25% of the field area to seed Marketable Habitat Enhancement Plants (MHEP) around the main crop, occupying 75% of the field. However, wild pollinators may not rely fully on the resources that fields provide due to differences in flying period and host‐plant preferences, and need additional resources from wild flowering plant communities. Here we aim to compare wild pollinator communities between FAP fields, monoculture of pollinator dependent crops and the nearby wild flowering plants. We developed two experimental trials with two main crops (faba bean and eggplant) in 16 fields in North‐West Morocco and we compared wild pollinator richness and wild pollinator specialization between FAP fields, control fields and the nearby wild flowering plants. We recorded a significantly higher pollinator richness in FAP fields compared to wild flowering plants and monoculture. Pollinator specialization index (i.e. degree of interaction specialization at the species level) did not differ significantly between the three treatments in faba bean trial (i.e. FAP, control and wild plants), whilst in eggplant trial, wild plants harboured significantly more specialist species than FAP fields. Yet, no significant differences in pollinator specialization index were reported between the other treatments in eggplant trial (i.e. FAP vs. control and control vs. wild plants). Moreover, 28% of the pollinator species collected, were only observed on wild plants, particularly thistles. These results highlight the potential of FAP approach as a tool for pollinator conservation in farmlands. However, the FAP approach alone is not sufficient to cater the diverse pollinators present in the agro‐ecosystem, and hence, the maintenance of the surrounding wild flowering plants is necessary to support pollinators in farmlands.
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Eryngium maritimum L. (Apiaceae) is a geophyte that inhabits in the dunes of the Mediterranean and Atlantic. Although it is a highly entomophilous species, there is little literature on its pollinator assemblage. The aim of this study is to analyze the role played by E. maritimum in the dune pollination network of the Balearic Islands, where there is an intense anthropogenic impact in its habitat. For this purpose, two populations located in the North and South of Mallorca were chosen, in which diurnal transects were carried out to observe and capture pollinators on 15 plant species during the anthesis period of E. maritimum. The flowering period of 10 plant species flowering at the same period than E. maritimum was analyzed to identify periods of competition. A total of 71 pollinator species were found, belonging to 30 different families. Eryngium maritimum is a strongly generalist species, with a total of 45 pollinator species. Two new species, Odice blandula and Leucospis gigas, were found for the first time in Mallorca. In terms of pollinators, Teucrium dunense and Helichrysum stoechas are the most similar species to E. maritimum. However, analysis of phenology suggests that these three species have been able to decouple their blooms to avoid competition. The present study shows that E. maritimum plays an important role in the dune pollination network, being its anthesis located at the end of the dune flowering season, when there are no functionally similar species in flower. Eryngium maritimum (L.) plays a key role in the dune pollination network of the Balearic islands. It behaves as an opportunistic species and is visited by more than 80 different species. Its conservation is vital to maintain the complex ecological network of this coastal habitat.
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Fenitrothion, an organophosphorus insecticide, has been used as a larvicidal spray against spruce budworm (Choristoneura fumiferana (Clem.) Lepidoptera: Tortricidae) over wide areas of forest in New Brunswick, Canada, since 1969. The important pollinators of lowbush blueberries in the region are native wild bees. Populations of these insects appear to have been severely reduced on fields within areas adjacent to where Fenitrothion has been used and residues have been found in carcasses of both honey bees and native bees. From that evidence, together with high toxicity of Fenitrothion to bees, and the area covered by their foraging ranges, it is concluded that blueberry fields and their immediate surrounds received doses of the pesticide. Because blueberries require outcrossing by bees, it is believed that crop failures have, in part, been caused by drifts or indiscriminate applications, or both, of the pesticide.
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The number of interactions with flower visitor species differs considerably among insect pollinated plants. Knowing the causes for this variation is central to the conservation of single species as well as whole plant–flower visitor communities. Species specific constraints on flower visitor numbers are seldom investigated at the community level. In this study we tested whether flower size parameters set constraints on the morphology of the potential nectar feeding visitors and thus determine the number of visitor species. We studied three possible constraints: the depth and width of tubular structures hiding the nectar (nectar holder depth and width) and the size of flower parts that visitors can land on (size of the alighting place). In addition we assess the role of flower abundance on this relationship. We hypothesized that the stronger size constraints and the smaller flower abundance, the smaller the number of visitor species will be. Our study of a Mediterranean plant–flower visitor community revealed that nectar holder depth, nectar holder width and number of flowers explained 71% of the variation in the number of visitor species. The size of the alighting place did not restrict the body length of the visitors and was not related to visitor species number. In a second step of the analyses we calculated for each plant species the potential number of visitors by determining for each insect species of the local visitor pool whether it passed the morphological limits set by the plant. These potential numbers were highly correlated with the observed numbers (r2=0.5, p<0.001). For each plant species we tested whether the observed visitors were a random selection out of these potential visitors by comparing the mean of the observed and expected proboscis length distributions. For most plant species the observed mean was not significantly different from the random means. Our findings shed light on the way plant–flower visitor networks are structured. Knowing the constraints on interaction patterns will be an important prerequisite to formulate realistic null models and understand patterns of resource partitioning as well as coevolutionary processes.
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Habitat degradation and climate change are thought to be altering the distributions and abundances of animals and plants throughout the world, but their combined impacts have not been assessed for any species assemblage. Here we evaluated changes in the distribution sizes and abundances of 46 species of butterflies that approach their northern climatic range margins in Britain-where changes in climate and habitat are opposing forces. These insects might be expected to have responded positively to climate warming over the past 30 years, yet three-quarters of them declined: negative responses to habitat loss have outweighed positive responses to climate warming. Half of the species that were mobile and habitat generalists increased their distribution sites over this period (consistent with a climate explanation), whereas the other generalists and 89% of the habitat specialists declined in distribution size (consistent with habitat limitation). Changes in population abundances closely matched changes in distributions. The dual forces of habitat modification and climate change are likely to cause specialists to decline, leaving biological communities with reduced numbers of species and dominated by mobile and widespread habitat generalists.
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Causal attribution of recent biological trends to climate change is complicated because non-climatic influences dominate local, short-term biological changes. Any underlying signal from climate change is likely to be revealed by analyses that seek systematic trends across diverse species and geographic regions; however, debates within the Intergovernmental Panel on Climate Change (IPCC) reveal several definitions of a 'systematic trend'. Here, we explore these differences, apply diverse analyses to more than 1,700 species, and show that recent biological trends match climate change predictions. Global meta-analyses documented significant range shifts averaging 6.1 km per decade towards the poles (or metres per decade upward), and significant mean advancement of spring events by 2.3 days per decade. We define a diagnostic fingerprint of temporal and spatial 'sign-switching' responses uniquely predicted by twentieth century climate trends. Among appropriate long-term/large-scale/multi-species data sets, this diagnostic fingerprint was found for 279 species. This suite of analyses generates 'very high confidence' (as laid down by the IPCC) that climate change is already affecting living systems.
A general binomial mixture model is proposed for the species accumulation function based on presence-absence (incidence) of species in a sample of quadrats or other sampling units. The model covers interpolation between zero and the observed number of samples, as well as extrapolation beyond the observed sample set. For interpolation (sample-based rarefaction), easily calculated, closed-form expressions for both expected richness and its confidence limits are developed (using the method of moments) that completely eliminate the need for resampling methods and permit direct statistical comparison of richness between sample sets. An incidence-based form of the Coleman (random-placement) model is developed and compared with the moment-based interpolation method. For extrapolation beyond the empirical sample set (and simultaneously, as an alternative method of interpolation), a likelihood-based estimator with a bootstrap confidence interval is described that relies on a sequential, AIC-guided algorithm to fit the mixture model parameters. Both the moment-based and likelihood-based estimators are illustrated with data sets for temperate birds and tropical seeds, ants, and trees. The moment-based estimator is confidently recommended for interpolation (sample-based rarefaction). For extrapolation, the likelihood-based estimator performs well for doubling or tripling the number of empirical samples, but it is not reliable for estimating the richness asymptote. The sensitivity of individual-based and sample-based rarefaction to spatial (or temporal) patchiness is discussed.
The EU-funded research project ALARM will develop and test methods and protocols for the assessment of large-scale environmental risks in order to minimise negative human impacts. Research focuses on the assessment and forecast of changes in biodiversity and in the structure, function, and dynamics of ecosystems. This includes the relationships between society, the economy and biodiversity.
Changes in the abundance of species—especially those that influence water and nutrient dynamics, trophic interactions, or disturbance regime—affect the structure and functioning of ecosystems. Diversity is also functionally important, both because it increases the probability of including species that have strong ecosystem effects and because it can increase the efficiency of resource use. Differences in environmental sensitivity among functionally similar species give stability to ecosystem processes, whereas differences in sensitivity among functionally different species make ecosystems more vulnerable to change. Current global environmental changes that affect species composition and diversity are therefore profoundly altering the functioning of the biosphere.