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a ‘noisy’ image. Although a simple task, this
achievement is remarkable because the con-
tinuous conductance changes of memristors
are notoriously noisy and non-symmetric
— that is, increases in conductances often
have different amplitudes from analogous
decreases, which causes problems for learning
algorithms. The authors used two memristors
for each synaptic connection, such that the
strength of a synapse was given by the differ-
ence between two memristor conductances.
This differential implementation of synaptic
strengths has several benefits — for exam-
ple, it reduces the impact of non-symmetric
conductance changes because each synaptic
update involves the change of two conduct-
ances in opposite directions.
Prezioso and co-workers’ result is a proof-
of-concept for hybrid CMOS–memristor
neuromorphic circuits. If this design can be
scaled up to large network sizes, it will affect
the future of computing. Computer scientists
have struggled to design algorithms for jobs
that humans perform easily, such as visual
tasks (distinguishing objects in a scene, for
example), speech recognition and coordi na-
ting muscles and limbs to perform a motor
task. Large neural networks can learn such
tasks from massive data sets
5
. Brain-inspired
hardware would therefore complement the
strengths of conventional computers. In the
future, laptops, mobile phones and robots
could include ultra-low-power neuromorphic
chips that process visual, auditory and other
types of sensory information.
Of course, more research is necessary
to achieve these goals. With an area of
200 × 200 nanometres, the memristive devices
used by Prezioso etal. are still relatively large
compared with other state-of-the-art memris-
tors, and the network described is quite simple.
Much larger networks will need to be created,
with higher numbers of memristors per unit
area, for applications to be realized. Also, the
researchers used a batch-learning set-up, in
which the whole training data set had to be
processed for each update of memristive con-
ductances. This training set-up would there-
fore require many extra circuit components
to provide large amounts of memory outside
the memristive crossbar array. Future research
must explore how efficient learning procedures
for memristive crossbar arrays can be achieved
without the need for external memory. ■
Robert Legenstein is at the Institute
for Theoretical Computer Science, Graz
University of Technology, Graz 8010, Austria.
e-mail: robert.legenstein@igi.tugraz.at
1. Prezioso, M. et al. Nature 521, 61–64 (2015).
2. Backus, J. Commun. ACM 21, 613–641 (1978).
3. McCulloch, W. S. & Pitts, W. H. Bull. Math. Biophys. 5,
115–133 (1943).
4. Rosenblatt, F. Psychol. Rev. 65, 386–408 (1958).
5. Schmidhuber, J. Neural Networks 61, 85–117 (2015).
6. Indiveri, G. et al. Nanotechnology 24, 384010
(2013).
ECOLOGY
Tasteless pesticides
affect bees in the field
Two studies provide evidence that bees cannot taste or avoid neonicotinoid
pesticides, and that exposure to treated crops affects reproduction in solitary bees
as well as bumblebee colony growth and reproduction. S L .74 .77
NIGEL E. RAINE & RICHARD J. GILL
I
nsects such as bees are crucial for the
pollination of agricultural crops and wild
plants1,2, helping to ensure food secu-
rity and maintain biodiversity. Yet a range of
environmental stressors are threatening bee
populations around the world3–6. The impact
of pesticide exposure, particularly from
neonicotinoid insecticides, has received sub-
stantial recent research attention7,8 and has
become a topic of public debate. Studies that
have reported adverse effects of neonicotinoids
on bees have been criticized for several rea-
sons: that exposure tests are carried out under
laboratory or semi-field settings rather than
in the field and use pesticide-treated foods
containing unrealistically high dosages; and
that bees can detect chemical residues on
treated crops and avoid foraging on them. Fur-
ther weight has been added to such criticisms
because the few field studies that have inves-
tigated potential impacts on honeybees and
bumblebees from exposure to neonicotinoid-
treated crops have been interpreted to show
little or no effect9–13, although limitations to
these studies have been highlighted7,14. Two
studies in this issue strike at the heart of these
evidence gaps and improve our understanding
of pesticide exposure risks to bees.
In their paper, Kessler etal.15 (page74)
present a carefully controlled laboratory study
Non-owering crop
Pesticide exposure: low
Nutrition: scarce
Wild-ower meadows
Pesticide exposure: low
Nutrition: less abundant
but diverse
Field margins
Pesticide exposure: medium
Nutrition: less abundant
but diverse
Solitary-bee
foraging
range
Bumblebee
foraging
range
Honeybee
foraging
range
Flowering crop
Pesticide exposure: high
Nutrition: abundant
but non-diverse
Figure 1 | Bee foraging options and pesticide exposure. Non-flowering crops and pasture cover large
areas of rural land, but typically provide limited food resources for bee populations. Flowering crops can
provide plentiful (although non-diverse) bee food, but are often treated with pesticides, a direct route for
exposure. Flower-rich meadows provide a diverse bee diet, but these are becoming increasingly scarce, and
small areas may support only low bee numbers. Furthermore, wild flowers in field margins may contain
pesticide residues. Rundlöf etal.16 show that the growth rates and reproduction of bumblebee colonies are
lower in neonicotinoid-treated fields than in control fields, and that reproduction of solitary bees can also
be affected. However, the authors found no effect on honeybee colonies. These differences may result from
different ecologies: honeybees can forage many kilometres from their hive, whereas bumblebees roam
over smaller areas, and solitary bees fly less far from their nest. Honeybees also use the waggle dance to
communicate the location of rewarding flower patches to nest-mates. Thus, honeybees may have reduced
pesticide exposure from visiting a greater mixture of foraging sources or through a greater chance of
avoiding treated crops. However, Kessler etal.15 show that neither honeybees nor bumblebees can taste
neonicotinoids, suggesting that such avoidance behaviour is unlikely. (Nest sites, foraging ranges and the
relative proportion of habitat types vary across landscapes — those depicted are representative only.)
38 | NATURE | VOL 521 | 7 MAY 2015
NEWS & VIEWS
RESEARCH
© 2015 Macmillan Publishers Limited. All rights reserved
50 Years Ago
‘The sign of the constant of
gravitation’. By Prof. W. H. McCrea
— A speaker in a recent broadcast
asserted that, were the gravitation-
constant negative instead of
positive, Newton’s apple would have
soared away into the sky instead of
falling on Newton’s head. However,
had that happened, Newton also
would have soared away and there
would have been no legend to
record. In fact, there cannot be a
world for which gravitation is not
attractive … We shall see that the
sign of the gravitation constant is
essentially a matter of convention.
From Nature 8 May 1965
100 Years Ago
It may be remembered that the
Royal Commission on Whisky,
which in 1908–9 gave a lengthy
consideration to the matter, did not
find a very satisfactory answer to
the query “What is whisky?” The
Government of Western Australia
… issued regulations under which
certain chemical standards for “pure
pot-still whisky” were proposed for
adoption. The proposals met with
some criticism. It was alleged, in
fact, that many pot-stills employed
in Great Britain could not produce
whisky which would comply with
the requirements … the proposals,
as now modified … are that, as
regards Scotch whisky, it shall have
been distilled at a strength not more
than 35 degrees above proof and
matured in wood for not less than
two years; and that “standard pot-
still whisky” shall contain at least
45 grams of esters, 3.5 of furfural,
and 180 of higher alcohols per
100litres of absolute alcohol … For
Irish whisky no furfural standard
is proposed at present, but the
proportion of esters is required to be
not less than 35 grams, and of higher
alcohols 200 grams, per 100 litres of
absolute alcohol.
From Nature 6 May 1915
testing the ability of both honeybees (Apis
mellifera) and bumblebees (Bombus terrestris)
to taste the three most commonly used neo-
nicotinoids — clothianidin, imidacloprid and
thiamethoxam. When hungry worker bees
could choose to collect from feeders contain-
ing either a solution of neonicotinoid-treated
sugar water or an untreated solution, neither
species avoided the treated food, which con-
tained neonicotinoid concentrations compa-
rable to those found in the nectar and pollen of
treated crops. Surprisingly, the bees in fact pre-
ferred the treated solution in the imidacloprid
and thiamethoxam tests, which the authors
suggest arises from the pharmacological action
of these insecticides on receptors in the bees’
brains. The authors corroborated their behav-
ioural results with neurophysiological meas-
urements showing that bees are unable to taste
neo nicotinoids in sugar water.
Scaling up from the laboratory, Rundlöf
etal .
16
(page77) undertook an ambitious study
to assess the impacts of neonicotinoid exposure
on bees placed near fields of treated oilseed rape
(also known as canola). The experiment — the
largest of its kind so far — involved 16fields
across southern Sweden: 8fields were planted
with seeds treated with the systemic insecti-
cide clothianidin, the pyrethroid insecticide
β-cyfluthrin and the fungicide thiram, and
8 control fields were treated solely with thiram.
Like Kessler etal., these researchers studied
both honeybees and bumble bees, but followed
entire colonies rather than individuals.
Furthermore, they monitored nests of a
species of solitary bee (Osmia bicornis ), as well
as surveying wild bees in field margins.
In treated fields, Rundlöf and colleagues
found fewer wild bees and observed reduced
growth rate and reproduction of bumblebee
colonies (which produced fewer males and
fewer new queens — consistent with previous
semi-field and field studies14,17,18) compared
to control fields. They also found that none
of the solitary bees that emerged from nests
placed next to treated fields came back to their
natal nest to build new brood cells, whereas
emergent females successfully produced brood
cells in six of eight untreated fields. By contrast,
there was no significant difference in honey-
bee colony growth between treated and control
fields. However, the authors’ power analysis
indicated that they would only have been able
to detect a minimum effect size of about 19%
for honeybees.
These studies provide timely data to address
calls for further evidence about the environ-
mental risks of neonicotinoids. The insecti-
cides tested by the authors are currently subject
to a European Union moratorium for use as
seed treatments on crops attractive to bees, but
this usage restriction will be reviewed before
December2015. It is hard to say whether
the preferences observed by Kessler and col-
leagues for nectar containing imidacloprid
and thiamethoxam residues would occur in
a more complex field setting, where many
variables could interfere with foraging deci-
sions. However, their study does imply that
foraging bees are unlikely to avoid seed-treated
crops in the field, and supports previous
reports of honeybees and bumblebees bringing
back nectar and pollen from treated fields
9–12,16
.
If the preference for treated food does apply in
the field, these findings suggest that we could
be underestimating the exposure risk to bees
from treated crops.
Both studies also highlight the fact that
different bee species vary in their responses to
exposure. Current pesticide registrations rely
on ecotoxicological testing of just one spe-
cies, the honeybee, when assessing risks for all
insect pollinators. Yet Rundlöf and colleagues
found negative effects of neonicotinoids on
solitary bees and bumblebees in the field, but
not on honeybees, suggesting that a single
species might not represent the responses of
other pollinators. Potential explanations for
these apparent differences could include a vari-
able affinity of neuronal receptors for binding
neonicotinoids; differences in detoxification
capacities; and divergent foraging behaviours,
which influence levels of exposure (Fig.1).
Differences could also result from variation in
social organization and life-history strategies.
Even the smallest perennial honeybee colonies
contain a queen and several thousand work-
ers that overwinter as a group, whereas annual
bumblebee colonies rarely contain more than
a queen and a few hundred workers. Each
solitary bee is responsible for its own forag-
ing and reproduction during its few weeks of
adult life. The sheer number of workers in the
honeybee colony may better enable buffering
of stress over long periods, whereas the more
severe pinch points that bumblebees and soli-
tary bees experience could render them more
susceptible to environmental pressures19,20.
If field experiments to assess exposure are
deemed so important, why have so few been
carried out? Limiting factors include the
scale of such studies, the levels of replication
required to achieve appropriate statistical
power, and human and budgetary resources.
Even with 16 fields, Rundlöf and colleagues’
study had relatively low statistical power and,
as with other field studies, many environmen-
tal factors probably varied among their sites
and could not be standardized. Such studies
can provide only correlational evidence of
impacts, whereas controlled-exposure studies,
such as that of Kessler etal.15, are better suited
to determining causative relationships through
manipulative experimentation. The comple-
mentarity of these two approaches needs to be
considered by policy-makers and for future
research planning.
Although the two latest studies contribute
to our understanding of the risk neonicoti-
noids pose to bees, knowledge gaps remain.
For example, we need further evidence about
how neonicotinoid exposure might affect
7 MAY 2015 | VOL 521 | NAT URE | 39
NEWS & VIEWS RESEARCH
© 2015 Macmillan Publishers Limited. All rights reserved
social bee colonies over multiple seasons, how
soil residues might affect ground-nesting bees
and how neonicotinoid exposure interacts with
other environmental stressors. We also need a
greater understanding of how neonicotinoids
affect other pollinators and natural enemies
of crop pests, and of the persistence of these
chemicals in soil and their take-up by untreated
plants growing in or next to treated fields.
Fundamentally, we must move towards
finding the right balance between the risks
of neonicotinoid exposure for insect pollina-
tors and the value these pesticides provide to
ensure crop yield and quality. Selective use of
neonicotinoid seed treatments, on the basis
of a demonstrable need for systemic pest
protection, might help to reduce non-target
exposure and slow the onset of pest resist-
ance. We also need to consider and evaluate
alternative options for pest control. It would
be unfortunate if the recent focus on the risks
from neonicotinoids led unintentionally to
broader use of alternative pesticides that prove
to be even more harmful to insect pollinators
and the essential ecosystem services that they
provide. ■ SEE BOOKS & ARTS P.29
Nigel E. Raine is in the School of
Environmental Sciences, University of Guelph,
Guelph, Ontario N1G 2W1, Canada.
Richard J. Gill is in the Department of Life
Sciences, Silwood Park, Imperial College
London, Ascot SL5 7PY, UK.
e-mails: nraine@uoguelph.ca;
r.gill@imperial.ac.uk
1. Garibaldi, L. A. et al. Science 339, 1608–1611 (2013).
2. Ollerton, J., Winfree, R. & Tarrant, S. Oikos 120,
321–326 (2011).
3. Vanbergen, A. J. et al. Front. Ecol. Environ. 11,
251–259 (2013).
4. Nieto, A. et al. European Red List of Bees (European
Commission, 2014); available at go.nature.com/
c4g8lm
5. Burkle, L. A., Marlin, J. C. & Knight, T. M. Science
339, 1611–1615 (2013).
6. Ollerton, J., Erenler, H., Edwards. M. & Crockett, R.
Science 346, 1360–1362 (2014).
7. Godfray, H. C. J. et al. Proc. R. Soc. B 281,
20140558 (2014).
8. Pisa, L. W. et al. Environ. Sci. Pollut. Res. 22, 68–102
(2015).
9. Cutler, G. C. & Scott-Dupree, C. D. J. Econ. Entomol.
100, 765–772 (2007).
10. Pilling, E., Campbell, P., Coulson, M., Ruddle, N. &
Tornier, I. PLoS ONE 8, e77193 (2013).
11. Cutler, G. C., Scott-Dupree, C. D., Sultan, M.,
Mcfarlane, A. D. & Brewer, L. PeerJ 2, e652 (2014).
12. FERA. Effects of Neonicotinoid Seed Treatments on
Bumble Bee Colonies Under Field Conditions (FERA,
2013); available at go.nature.com/w9jlti
13. Cutler, G. C. & Scott-Dupree, C. D. Ecotoxicology 23,
1755–1763 (2014).
14. Goulson, D. PeerJ 3, e854 (2015).
15. Kessler, S. C. et al. Nature 521, 74–76 (2015).
16. Rundlöf, M. et al. Nature 521, 77–80 (2015).
17. Gill, R. J., Ramos-Rodriguez, O. & Raine, N. E. Nature
491, 105–108 (2012).
18. Whitehorn, P. R., O’Connor, S., Wackers, F. L. &
Goulson, D. Science 336, 351–352 (2012).
19. Bryden, J., Gill, R. J., Mitton, R. A. A., Raine, N. E. &
Jansen, V. A. A. Ecol. Lett. 16, 1463–1469 (2013).
20. Gill, R. J. & Raine, N. E. Funct. Ecol. 28, 1459–1471
(2014).
This article was published online on 22 April 2015.
PALAEONTOLOGY
Dinosaur up in the air
A new feathered dinosaur from China, belonging to an obscure and strange
carnivorous group, bears a seemingly bony wrist structure that may have
had a role in flight. S L .70
KEVIN PADIAN
W
hen the first dinosaurs with feathers
or feather-like structures were
brought to light by Chinese
scientists in the mid-1990s, they cemented the
hypothesis of the dinosaurian origin of birds
and provided spectacular evidence about the
origin of flight and the primordial functions of
feathers
1,2
. In the ensuing two decades, the pic-
ture of the evolution of feathers and flight has
become richer and more complicated as other
feathered dinosaurs have been discovered,
seemingly on a monthly basis
3
. But things have
just gone from the strange to the bizarre. On
page70 of this issue, Xu etal.4 present a feath-
ered dinosaur from a completely un expected
branch of the dinosaur tree — and it sports a
never-before-seen skeletal element that the
authors think may be related to flight.
The dinosaur, named Yi qi, is a member of
the unusual group of theropod (carnivorous)
dinosaurs called Scansoriopterygidae
5
(Fig.1).
Although scansoriopterygids are not well
known — there are only three kinds, and only
incomplete remains of these — they seem to
be small (the skull of Yi qi is about 4centime-
tres long), with smaller and fewer teeth than
other theropods, and with long hands. Unusu-
ally for theropod dinosaurs, the third finger is
longer than the second. It is especially long in
Yiqi, and its forelimb is further distinguished
by a long ‘styliform element’ coming off the
wrist. The authors are refreshingly agnostic
about the exact function of this new struc-
ture, partly because it is so different from any-
thing previously known. However, their find
opens two cans of worms: about interpreting
unique structures in fossils and about what it
means to fly.
The styliform element, which may be a
hypertrophied wrist bone or a neomorphic
calcified structure, is longer than any of the
animal’s fingers and is curved at both ends. It
is probably not a true finger, such as the fourth
finger that forms the main outboard spar of
the wing in pterosaurs — flying reptiles that
were related to their dinosaur contemporaries,
but that evolved flight independently of birds.
Instead, the styliform element of Yiqi has no
joints and comes directly off the carpal bones
without the intermediary of a meta carpal
(palm bone), so it is probably not a finger (the
authors confusingly label the three fingers of
the dinosaur-bird hand as II–III–IV instead
of the standard I–II–III, which corresponds
to our thumb, index and middle fingers6).
How the structure is attached to the wrist is
not clear, because its proximal end seems quite
squared off; this means that we also do not
know if or how it could move. Superficially, it
looks the same as the animal’s other bones, a
conclusion supported by the authors’ energy
dispersive spectrometry analysis. It would be
interesting to see if it has true bone cells, to
confirm that it is indeed bone and not calcified
cartilage or other calcified tissue.
What could this element be except a
support for some kind of aerofoil? The authors
infer this on the basis of its position and the
presence of membranous tissue in the wrist
area. But although they consider a variety of
analogous structures in living and extinct fly-
ing and gliding animals, none is exactly like
the styliform element in Yi qi. Furthermore,
Yi qi ’s body is not preserved below the ribcage,
so reconstructions of the pelvis, hindlimbs and
tail must be conjectured from what is known of
other scansoriopterygids (Fig.1). Further ana-
tomical analysis of this structure and how the
rest of the body related to it — such as whether
the tail created lift or drag — will require other
discoveries.
In the meantime, the authors do not
commit themselves to whether this animal
could flap or glide, or both, or neither. That
is a good position to take
7
, but we can parse it
further. To fly actively, an animal must be able
to execute a flight stroke that can generate a
vortex wake that propels it forward
8
. No evi-
dence presented so far suggests that Yi qi had
this ability. Furthermore, in flapping animals
the outboard skeletal elements (wrist, hand
and so on) are primarily responsible for thrust,
the essential component of powered flight8,9,
but these are not particularly long in Yi qi. So,
at present we can shelve the possibility that this
dinosaur flapped.
As for gliding, if Yi qi’s styliform element
helped to support a membranous aerofoil, it
can be used to reconstruct the planform of the
wing, as Xu and colleagues have done. But in a
gliding animal, the centre of lift of the aerofoil
should be fairly congruent with the centre of
gravity of the body — if the bulk of the animal’s
weight falls too far behind the centre of lift,
the back end will sag and the animal will stall
9
.
That is clearly the case in the authors’ recon
-
struction of Yi qi , but an aerofoil that was swept
back more, if anatomically possible, might
40 | NATURE | VOL 521 | 7 MAY 2015
NEWS & VIEWS
RESEARCH
© 2015 Macmillan Publishers Limited. All rights reserved
