13. Lien, M.-C., Procter, R.W., and Ruthruff, E.(2003). Still no evidence for perfect timesharingwith two ideomotor-compatible tasks: A replyto Greenwald (2003). J. Exp. Psychol. Hum.Percept. Perf. 29, 12671272.

14. Luck, S.J. (1998). Sources of dual-taskinterference: Evidence from humanelectrophysiology. Psychol. Sci. 9, 223227.

15. Adcock, R.A., Constable, R.T., Gore, J.C., andGoldman-Rakic, P.S. (2000). Functionalneuroanatomy of executive processes involvedin dual-task performance. Proc. Natl. Acad. Sci.USA 97, 35673572.

16. Jiang, Y., and Kanwisher, N. (2003). Commonneural substrates for response selection across

modalities and mapping paradigms. J. Cogn.Neurosci. 15, 10801094.

17. Schmacher, E.H., Elston, P.A., andDEsposito, M. (2003). Neural evidence forrepresentation-specific response selection.J. Cogn. Neurosci. 15, 11111121.

18. Dux, P.E., Ivanoff, J., Asplund, C.L., andMarois, R. (2006). Isolation of a centralbottleneck in information processing withtime-resolved FMRI. Neuron 52, 11091120.

19. Pashler, H., Luck, S.J., Hillyard, S.A.,Mangun, G.R., OBrien, S., and Gazzaniga, M.S.(1994). Sequential operation of disconnectedcerebral hemispheres in split-brain patients.Neuroreport 5, 23812384.

20. Schumacher, E.H., Seymour, T.L., Glass, J.M.,Fencsik, D.E., Lauber, E.J., Kieras, D.E., andMeyer, D.E. (2001). Virtually perfect timesharing in dual-task performance: Uncorkingthe central cognitive bottleneck. Psychol. Sci.12, 101108.

Crossmodal Research Laboratory,Department of Experimental Psychology,University of Oxford, Oxford OX1 3UD, UK.E-mail: charles.spence@psy.ox.ac.uk

DOI: 10.1016/j.cub.2008.08.039

Pollinator-Dependent Crops:An Increasingly Risky Business

Three-quarters of leading global food crops rely on animal pollination. Withboth managed and wild pollinators declining, is there reason for concern?Researchers are beginning to pin down the possible long-term risks.

Rachael Winfree

Most plants use animals to move theirpollen from the male to the female partsof the flower [1]. In the wild, seedproduction is often pollination-limited([2,3]; but see [4]), suggesting thatpollinators can strongly affect plantfitness. Within the agricultural context,artificial selection for ease of culturehas only partially reduced plantsdependence on pollinators. Pollinationby animals, primarily bees, remainsan essential step in the production ofmany crops, including melons, squash,apples, berries, and almonds [5,6]. Theglobal value of this animal-mediatedpollination is V153 billion [7].Meanwhile, evidence has beenaccumulating that both wild andcommercially managed pollinators arein decline [810]. What does this meanfor the production of animal-pollinatedcrops? In this issue of Current Biology,Aizen et al. [11] provide the first

and in agricultural landscapes wheretheir habitat needs are met, they aresufficient to pollinate crops [12,13].Wild pollinators typically drop to lowlevels, however, in intensivelyagricultural areas [14], where vastmonoculture plantings create aboom-and-bust cycle: un-pollinatedflowers outnumber bees during the fewweeks of crop bloom, while starvingbees outnumber flowers for the restof the year. Furthermore, most wildpollinators nest individually in theground or in twigs and needundisturbed, pesticide-free areas inwhich to do so.

Enter the European honey bee(Figure 1B), a species that nests bythe tens of thousands in convenientlytransportable hives that can be movedinto fields during crop bloom, andwhisked away to safety duringpesticide application. Yet the honeybees success may contain the seedsof its own destruction. It has become

unexplained phenomenon in whichadult bees abandon the hive leavingthe queen and developing broodto starve [1517].

So where does this leave us? Untilnow, this question has generated moremedia hype than research attention.In this issue, Aizen et al. [11] helpbalance the scales by testing theprediction that pollination shortfalls,if they exist, would decrease globalyields of pollinator-dependent crops.The authors use Food and AgriculturalOrganization (FAO) statistics on yieldper hectare to compare rates ofincrease over the past 45 yearsbetween pollinator-dependent andpollinator-independent crops. Yieldincreased similarly for the two groups,providing no evidence that pollinatordeclines have as yet translated intodecreases in food production. Twoadditional analyses, however, suggestsigns of trouble ahead. First, cropplants that have a high degree ofpollinator dependence showed slowerrates of yield increase than did cropswith low pollinator dependence,although this last pattern was not quitestatistically significant [11]. We wouldexpect yield declines to appear first forthe most pollinator-dependent crops,so this finding may be indicative offuture declines. Second, the global

Current Biology Vol 18 No 20R968comprehensive answer to this questionby comparing trends in global yieldsbetween pollinator-dependent andnon-pollinator-dependent crops.

There are good reasons to expectpollination to limit crop production.Farmers aim to provide pollinationservices, along with many other inputs,in sufficient quantities such that nonebecomes the rate-limiting step in cropproduction. But from the pollinatorspoint of view, the modern agriculturallandscape has become a bit limiting.There are thousands of species ofnative, wild pollinators (Figure 1A),

a virtual monoculture as an agriculturalpollinator, driven to further geneticuniformity by the limited number oflarge breeding facilities that providequeens to bee-keepers [8] thuscreating a resource that pathogensand parasites have been quick toexploit. In North America, for example,the number of managed honey beecolonies shrunk by 59% between1947 and 2005, in part due toinfestations by hemolymph-suckingmites [9]. And since 2006, honey beeshave been threatened by ColonyCollapse Disorder, an as yet

area devoted to pollinator-dependentcrops has been increasingdisproportionately over time, indicatingthat we are increasing the risk offuture pollinator-related declines inour food supply [11].

It follows from Aizen et al.s [11]results that, if the area of pollinator-dependent crops is increasing andthe supply of pollinators decreasing,we will encounter pollination-drivendeclines in food production eventually.What other early-warning signalsmight presage this decline? Onemight be an increase in the price of

References

9. National Research Council (2007). Status ofPollinators in North America (Washington, DC:The National Academies Press).

10. Biesmeijer, J.C., Roberts, S.P.M., Reemer, M.,Oholemuller, R., Edwards, M., Peeters, T.,Schaffers, A.P., Potts, S.G., Kleukers, R.,Thomas, C.D., et al. (2006). Parallel declinesin pollinators and insect-pollinated plants inBritain and the Netherlands. Science 313,351354.

11. Aizen, M.A., Garibaldi, L.A., Cunningham, S.A.,and Klein, A.M. (2008). Long-term global trendsin crop yield and production reveal no currentpollination shortage but increasing pollinatordependency. Curr. Biol. 18, 15721575.

12. Kremen, C., Williams, N.M., and Thorp, R.W.(2002). Crop pollination from native bees atrisk from agricultural intensification. Proc. Natl.Acad. Sci. USA 99, 1681216816.

13. Winfree, R., Williams, N.M., Dushoff, J., andKremen, C. (2007). Native bees provideinsurance against ongoing honey bee losses.Ecol. Lett. 10, 11051113.

ating tomato. (B) European honey bee (Apis: Lisa Mandle.

Dispatchcrops suggests that it may bebeginning to occur. A second keyquestion, and one that is moredifficult to answer, has to do not withcurrent yields but with risk. On this,Aizen et al.s [11] results areunambiguous. Our increasing relianceon pollinator-dependent crops couldact synergistically with our increasingreliance on single pollinator speciesto increase the risk of a future crisisin the global food supply. The timeto act on diversifying our suite ofpollinators and solving honey beehealth problems is now before wesee significant changes in cropproduction.

Purkinje Neurons: Wfor Complex Spikes

Cerebellar Purkinje neurons generate chthese bursts of activity generated by somstudy may have settled this debate by givdoes not fully resolve the question of whdownstream of the Purkinje cells.

Sungho Hong1

and Erik De Schutter1,2

The cerebellar cortex receives twodistinct types of afferent: mossy andpollinator-dependent crops. Therewere no differences in price trends,however, between pollinator-dependent and pollinator-independentcrops in the United States between1966 and 2003 (J. Ghazoul and L.P.Koh, personal communication). Asecond indicator would be an increasein the price farmers pay to rent honeybees for pollination purposes. In fact,the prices paid by North Americanalmond growers have increasedfrom $35 per hive in the early1990s to $150 per hive today [8].

A key question for those concernedwith pollinator decline is whetherchanges in pollinator abundancetranslate into changes in cropproduction [1820]. Determining this isnot as easy as it would seem becausea multitude of inputs can limit cropproduction, including soil fertility, pestcontrol, irrigation, and weather, thusrequiring large-scale experimentalmanipulations to determine how oftenpollination is a limiting factor at thefield scale. Aizen et al.s [11] findings,although non-experimental, suggestthat such limitation has not yetoccurred globally, though the loweryield of the most pollinator-dependent

Figure 1. Pollinating bees.

(A) Native, wild bee (Augochlora pura) pollinmellifera) pollinating watermelon. Photo credit

R9691. Linder, H.P. (1998). Morphology and theevolution of wind pollination. In ReproductiveBiology, S.J. Owens and P.J. Rudall, eds.(Richmond, UK: Royal Botanic Gardens, Kew),pp. 123135.

2. Ashman, T., Knight, T.M., Steets, J.A.,Amarasekare, P., Burd, M., Campbell, D.R.,Dudash, M.R., Jongston, M.O., Mazer, S.J.,Mitchell, R.J., et al. (2004). Pollen limitation ofplant reproduction: ecological and evolutionarycauses and consequences. Ecology 85,24082421.

3. Burd, M. (1994). Batemans principle and plantreproduction: the role of pollen limitation in fruitand seed set. Botanical Rev. 60, 83139.

4. Knight, T.M., Steets, J.A., and Ashman, T.L.(2006). A quantitative synthesis of pollensupplementation experiments highlights thecontribution of resource reallocation toestimates of pollen limitation. Am. J. Botany 93,271277.

5. Klein, A.-M., Vaissie`re, B.E., Cane, J.H.,Steffan-Dewenter, I., Cunningham, S.A.,Kremen, C., and Tscharntke, T. (2007).Importance of pollinators in changinglandscapes for world crops. Proc. R. Soc.Lond. B 274, 303313.

6. Free, J.B. (1993). Insect Pollination of Crops,2nd Edition (London: Academic Press).

7. Gallai, N., Salles, J.-M., Settele, J., andVaissie`re, B.E. (2008). Economic valuationof the vulnerability of world agricultureconfronted with pollinator decline. Ecolog.Econ., in press.

8. Johnson, R. (2007). Recent Honey Bee Declines(Washington, DC: Congressional ResearchService), 14 pages.14. Ricketts, T.H., Regetz, J., Steffan-Dewenter, I.,Cunningham, S.A., Kremen, C., Bogdanski, A.,Gemmill-Herren, B., Greenleaf, S.S.,Klein, A.M., Mayfield, M.M., et al. (2008).Landscape effects on crop pollination services:Are there general patterns? Ecol. Lett. 11,499515.

15. Williams, N. (2008). Bee fears heighten. Curr.Biol. 18, R682R683.

16. Stokstad, E. (2007). The case of the emptyhives. Science 316, 970972.

17. Cox-Foster, D.L., Conlan, S., Holmes, E.C.,Palacios, G., Evans, J.D., Moran, N.A.,Quan, P.-L., Briese, T., Hornig, M., Geiser, D.M.,et al. (2007). A metagenomic survey ofmicrobes in honey bee colony collapsedisorder. Science 318, 283286.

18. Ghazoul, J. (2005). Buzziness as usual?Questioning the global pollination crisis. TrendsEcol. Evol. 20, 367373.

19. Ghazoul, J. (2007). Challenges to the uptake ofthe ecosystem service rationale forconservation. Cons. Biol. 21, 16511652.

20. Kremen, C., Daily, G.C., Klein, A.-M., andScofield, D. (2008). Inadequate assessmentof the ecosystem service rationale forconservation: A reply to Ghazoul. Cons. Biol.22, 795798.

Department of Entomology, RutgersUniversity, New Brunswick, New Jersey08901, USA.E-mail: rwinfree@rci.rutgers.edu

DOI: 10.1016/j.cub.2008.09.010

hat Is the Signal?

aracteristic complex spikes; but areatic or dendritic excitability? A recenting the soma the dominant role, but itat information is transmitted

climbing fibers. While mossy fiberscarry inputs from many differentregions of the central nervous system,climbing fibers originate only from theinferior olive and contact only one cell

Pollinator-Dependent Crops: An Increasingly Risky BusinessReferences