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such as dislocations, and the X-ray scatteringfrom such defects is greater than the scatter-ing from bonding electrons. But using anelectron microscope it is possible to image thecrystal, select a perfect region between crystaldefects, and form a diffraction pattern fromthis perfect region. Zuo et al.1 use an electronbeam focused to nanometre dimensions tofind a region of the crystal where the perfect-crystal theory of diffraction applies. Theyalso filtered the electrons transmitted by thespecimen to remove inelastically scatteredelectrons and ease comparison with theory.Using these methods, very accurate charge-density maps can be made which reveal theshape of the electron bonds.

In metal oxides, the metal ions interactmainly with the oxygen atoms. But in manycopper- and silver-oxide compounds themetal ions are found in close-packed crystalstructures, leading to predictions of short-range metal–metal bonding. Such bondingwould be covalent, and therefore requirenon-spherical orbitals, unlike the usual ionicbonding, which involves electrostatic inter-actions between spherical ions. The non-spherical charge density observed by Zuo etal. around Cu atoms in Cu2O reveals unusuald-orbital holes (where the dz2 orbital isunoccupied) and provides strong evidencefor Cu–Cu bonding.

How does this work relate to high-tem-perature superconductivity? We now knowthat in the simple oxide Cu2O there are d-orbital holes located on the Cu atoms. Wealso know that in the copper-oxide super-

conductors, which have CuO2 (rather thanCu2O) conducting planes, the charge carri-ers in the normal state are holes and in thesuperconducting state are hole pairs. In theCuO2 superconductors, the available evi-dence suggests that the holes are on oxygensites rather than on copper sites3,4, whereasthe work of Zuo et al. shows that for Cu2O theholes are on copper sites. It would be of greatinterest to extend this approach to measur-ing charge densities to the more complexCuO2 superconductors. Such an experimentshould give us the following informationabout high-temperature superconductors:first, whether the holes are on copper or oxy-gen sites; second, how many holes there areper CuO2 unit in the conduction planes andhow many holes are elsewhere in the struc-ture. Finally, we would like to know whetherthe distribution of holes in the conductionplanes is actually periodic, as is usuallyassumed, or if there is an irregular two-phasecharge density of holes as recently proposed5.Zuo et al.1 have provided us with a tool toanswer all these questions. ■

Colin J. Humphreys is in the Department ofMaterials Science and Metallurgy, University ofCambridge, Pembroke Street, CambridgeCB2 3QZ, UK.e-mail: cjh1001@hermes.cam.ac.uk

1. Zuo, J. M., Kim, M., O’Keeffe, M. & Spence, C. J. Nature 401,

49–52 (1999).

2. Cottrell, A. Introduction to the Modern Theory of Metals

(Institute of Metals, London, 1988).

3. Temmerman, W. M. et al. J. Phys. C 21, L867–L874 (1988).

4. Nücker, N. et al. Phys. Rev. B 53, 14761–14764 (1996).

5. Humphreys, C. J. Acta Crystallogr. A 55, 228–233 (1999).

help the victims to survive an attack4. Notonly that, but they show that these defencescan be transmitted from an organism to itsoffspring. Induced defence is known to be aform of genotypic plasticity — that is, theability of a given gene sequence (genotype)to produce various traits (phenotypes)depending on environmental conditions.But it has never previously been reported toextend across generations.

To be ready when needed, induced traitsmust develop quickly in the presence of apredator. This might be a real problem.Fortunately, it can be overcome if the targetorganism receives cues of the predatorbefore the actual attack, or if the first attackis unlikely to be lethal. Although plantdefences may be induced simply becauseherbivores are chewing the foliage, manyorganisms have sophisticated early-warningsystems. Some plants, for example, switchon their defence mechanisms as soon as theydetect volatile chemicals released by dam-aged plants close by5. Some of these volatilesalso directly lure predators to attack plant-eating insects or mites6. But the firstencounter with a predator is likely to be fatalfor young water fleas, so they develop longneck spines in response to chemical cuesemitted from their invertebrate predators. Inthe field, this causes water fleas to developspiny, defensive helmets when living in apond also inhabited by predators.

Agrawal and co-workers3 now report thatin both wild radish, which is a cruciferousplant (its petals are arranged in a crossshape), and the water flea, the risks of ayoung individual’s first encounter withpredators can be reduced by the experiencesof their parents. In the case of the wildradish, the authors allowed butterfly larvae(Pieris rapae; Fig. 1) to attack the leaves in acontrolled manner. The radish plantsresponded by a ten-fold increase in the con-centration of glucosinolate, and they alsodeveloped more numerous hairy trichomeson their leaves. Glucosinolates are bitter-tasting, toxic compounds that reduce insectfeeding; hairy trichomes on leaves have asimilar effect. The authors then exposedseedlings produced by these plants to furtherlarval predation. They found that the off-spring of damaged mothers provided lesssuitable diets for larvae than seedlings fromundamaged, control plants.

A similar thing happened when Agrawalet al. exposed water fleas (Fig. 2) to chemicalcues called kairomones from two inverte-brate predators — the water fleas developedlong helmets. Furthermore, the offspring ofkairomone-treated mothers producedlonger helmets than offspring from controlmothers, irrespective of the environment inwhich the offspring were raised. The authorssaw the same effect in successive broods pro-duced later by the kairomone-treated moth-ers in clean water. This result confirms that

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22 NATURE | VOL 401 | 2 SEPTEMBER 1999 | www.nature.com

Induced defences — which emerge ordevelop to full strength when activated bythe presence of an enemy — are wide-

spread in sedentary or slowly moving prey1.Such induced resistance, as opposed to con-stitutive resistance (which is present allthe time), is profitable when defences aremetabolically expensive, and when attackis unpredictable but recurrent2. Induceddefensive traits are diverse. Water fleas, forexample, form long, helmet-shaped spineson their necks, making it difficult for preda-tors to handle them. Plants, on the otherhand, can produce high levels of toxic com-pounds in their leaves. Much of the literatureon induced plant defences contains reportsof predators having a bad time of it if theytry to target a plant that has already beenattacked. However, these observations donot exclude the possibility that the poorquality of previously damaged plants is afortuitous by-product of recovery from

attack, not a sign of increased defence.This is not the case for the organisms

described by Agrawal et al.3 on page 60 of thisissue. These authors have used radish plants(Raphanus raphanistrum) and water fleas(Daphnia cucullata) to provide the best evi-dence yet that predator-activated responses

Ecology

Bite the mother, fight the daughterErkki Haukioja

Figure1 Radish plant under attack by thebutterfly larva Pieris rapae. The plant’s defenceresponse includes the production of bitter-tasting, toxic compounds, and the developmentof hairy trichomes.

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the development of long helmets in theembryonic stages resulted from maternaleffects, and did not need to be directlyinduced by kairomones. However, offspringproduced by the kairomone-treated mothersin clean water had shorter helmets thanoffspring raised in water that containedthe chemical. This indicates that a recurrentinduction is needed for a maximum-strength defensive response.

At first glance, the observation that cer-tain traits are carried over to the next genera-tion looks like an example of Lamarckianinheritance. This theory, proposed by thenineteenth-century botanist and zoologistJean-Baptiste Pierre Antoine de Lamarck,holds that organisms can pass on to their off-spring traits that they have acquired duringtheir lifetime. Lamarck’s theory is surelywrong if it is interpreted as meaning, say, thatmice with cut tails would have offspring withno tails, or that people with trained muscleswould produce muscly babies. But if the par-ent’s environment affects how the geneticcode in the offspring is translated, then cer-tain acquired traits can be delivered to theoffspring.

Accordingly, the most parsimoniousexplanation of Agrawal and colleagues’ find-ings is that the genes that were switched on inthe parent to generate the defensive responseare also switched on in the offspring. Theinternal milieu of the radish seeds wasindeed different between induced and con-trol mothers, the induced mothers contain-ing higher concentrations of glucosinolate.But this does not need to be the decisive

switch — several alternative mechanisms,passed on from either the mother or thefather, can lead to the inheritance of environ-mentally affected traits7. Because the geneticcode inscribed in the chromosomes does notchange, however, the inter-generationalcarry-over effect is presumably reversible.

Nonetheless, the demonstration thatchemically mediated defensive traits can becarried over between generations in twototally unrelated species hints that suchphenomena might be widespread. Interest isgrowing in the idea that certain environmen-tal effects can be inherited in many types oforganism, from bacteria to plants, insectsand mammals7. Although it is not yet clearto what extent these inter-generationalresponses are adaptive (that is, tailored toequip an organism for a particular situa-tion), they have been reported in cases whenparents and offspring meet similar environ-mental challenges. For example, parentalcrowding alters the physiology, behaviour,coloration and structures of the offspring insome species of locust8 and lepidopteran9.This helps them to manage at high or low

population densities — situations that oftenoccur over several successive generations.Such observations indicate that if we do nottake into account the environmental fates ofthe parents of experimental organisms, wemay find unexplained variance in the resultsof ecological experiments. This is particular-ly true for research on induced defences, andAgrawal and colleagues’ study indicates thatecologists have much to do to uncoversources of variation, such as how dynamic orlong-lasting the effects of induced defencescan be. ■

Erkki Haukioja is in the Department of Biology,University of Turku, FIN-20014 Turku, Finland.e-mail: haukioja@utu.fi1. Harvell, C. D. Q. Rev. Biol. 65, 323–340 (1990).2. Baldwin, I. T. Proc. Natl Acad. Sci. USA 95, 8113–8118 (1998).3. Agrawal, A. A., Laforsch, C. & Tollrian, R. Nature 401, 60–63

(1999).4. Agrawal, A. A. Science 279, 1201–1202 (1998).5. Karban, R. & Baldwin, I. T. Induced Responses to Herbivory

(Univ. Chicago Press, 1997).6. Dicke, M. et al. J. Chem. Ecol. 19, 581–599 (1993).7. Rossiter, M. C. Annu. Rev. Ecol. Syst. 27, 451–476 (1996).8. Applebaum, S. W. & Heifetz, Y. Annu. Rev. Entomol. 44,

317–341 (1999).9. Rose, D. J. W., Dewhurst, C. F. & Page, W. W. Integr. Pest

Manage. Rev. 1, 49–64 (1995).

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Figure 2 Mother knows best. Agrawal et al.3 haveshown that defence responses induced inresponse to predators in female water fleas(pictured carrying eggs) can be passed on totheir offspring.

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Random noise, and its effect on physicalsystems, has always been an interdisci-plinary subject. Using the study of

fluctuations as a unifying theme can lead tointeresting scientific conferences, such as therecent UPoN’99 meeting in Adelaide, Aus-tralia*.

Over the years, noise has attracted someof the best scientists: in 1828 the botanistRobert Brown1 discovered the random fluc-tuations of tiny particles in a fluid, whichremained a mystery until Einstein’s epoch-making paper2 on Brownian motion in 1905.But it was not until later that the ubiquitouspresence of noise began to be appreciated. Amilestone was Johnson’s 1927 paper3 inwhich he identified noise in electrical cir-cuits as being of thermal origin. In the mid-dle of the twentieth century, noise seemedmerely a nuisance — to be eliminated orminimized wherever possible. It spoiledradio reception and musical recordings, andlimited the precision of physical measure-ments. Later, it was found to wash out thefine structure of beautiful fractal patternsgenerated by nonlinear systems.

But noise is much more than just a nui-sance. By the 1970s it became apparent thatnoise can play a creative role too. One of the

first examples was the observation of noise-induced transitions4, whereby the state of anonlinear system can be utterly changed bythe introduction of noise above a criticalintensity. Another was stochastic resonance,in which a weak periodic signal in a nonlin-ear system can be amplified by added noise.Stochastic resonance was introduced5,6 to tryto explain the Earth’s ice-age cycle, but it isnow recognized to be far more common,occurring for example in lasers, electroniccircuits and sensory neurons. Yet anothercreative effect of noise is seen in Brownianratchets7 where a net current of particles canbe driven by noise, providing that there is anappropriate asymmetry in the system: thisparticular phenomenon may underlie thetransport of macromolecules within biolog-ical cells. And, of course, it is noise in thesense of thermal fluctuations that driveschemical reactions, including those respon-sible for life itself.

The negative aspects of noise are still withus and, given its Janus-like character, how isnoise to be perceived, pursued and investi-gated? A proper appreciation of noise mustinvolve studies of both the mechanisms thatproduce it, for example in semiconductordevices, and the effect that it has on systemssubject to it. Both these aspects were wellrepresented at UPoN’99.

Of the several kinds of Brownian ratchet

Random fluctuations

Unsolved problems of noisePeter V. E. McClintock

*Second International Conference on Unsolved Problems of Noise and

Fluctuations (UPoN’99), Adelaide, Australia, 11–15 July 1999.

Proceedings to be published by the American Institute of Physics.