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Some species ring-tailed lemurs andsnow leopards, for example appar-ently thrive in captivity,whereas others,

such as Asian elephants and polar bears, areprone to problems that include poor health,repetitive stereotypic behaviour and breed-ing difficulties. Here we investigate thispreviously unexplained variation in captiveanimals welfare by focusing on caged carni-vores, and show that it stems from con-straints imposed on the natural behaviour ofsusceptible animals, with wide-ranging life-styles in the wild predicting stereotypy andthe extent of infant mortali ty in captivity.Our findings indicate that the keeping ofnaturally wide-ranging carnivores should beeither fundamentally improved or phased out.

Preventing natural behaviour patternsin animals can give rise to stress and frustra-tion1,2,and impair the development of brainregions that are involved in behaviouralsequencing, thereby reducing the animalsabili ty to behave flexibly andappropriately3,4.To investigate whether the observed varia-tion in the welfare of different species couldarise from a differential impact of captivityon their natural behaviour,we calculated themean frequency of stereotypic pacing5 by35 species of caged carnivore. We focusedon pacing because it is the most prevalentstereotypy among carnivores (97% ofreported stereotypies5) and also to avoid

comparability problems raised by poolingdifferent forms of stereotypy (such as sway-ing and head-nodding). We also quanti fiedinfant mortali ty in captivity, which is oftendue to poor maternal care6.

As an animals natural ranging and forag-ing activities are particularly constrainedby captivity7, we obtained all available fielddata on median home-range size,daily traveldistance, time spent i n general acti vity, timespent foraging, and reliance on hunting.We also quantified minimum home-rangesizes and daily travel distances, as these canbe orders of magnitude smaller when food

is abundant

8

. Relationships between wildand captive variables were tested by usingone-tailed regressions.

Body-weight effects were investigated inanalyses involving range size9; phylogeneticeffects were controlled where necessary (andin all analyses involving body mass) bycomparati ve analysis of independent con-trasts10,11.Our inferences about welfare tookinto account natural infant-mortality rates,and the amount of normal activity and totalstereotypy in captivity; we also consideredfeeding regimes,and the size and complexityof enclosures, to check that relationshipsbetween wild and captive variables were

not by-products of vari ation in husbandry.Degrees of freedom varied in subsequentanalyses owing to missing data.

Natural home-range size (HR) predictedcaptive-infant mortality (median HR:F1,216.04,P0.012;minimum HR,see Fig.1a).Control ling for body weight did not alterthis relationship (median HR: F1,204.35,P

0.025; controlling for phylogeny:F1,1620.46, P0.0001; minimum HR:F1,189.29, P0.004; controll ing for phy-logeny: F1,1816.94, P0.001). Minimum,but not median, daily distances travelled(DDT) gave similar results (F1,183.99,P0.03). These effects seem to be specific tocaptive animals: wild and captive infant-mortality rates did not covary (F1,60.08,not significant) and infant mortality inthe wild was unrelated to range size (forexample,minimum HR:F1,70.43,n.s.).

Home-range size also predicted pacing(median HR: F1,225.78, P0.013; mini-mum HR: F1,205.66, P0.014). A positive

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NATURE| VOL 425 | 2 OCTOBER 2003| www.nature.com/nature 473

trend was evident with body weight(F1,333.23, P0.081; controll ing for phy-logeny: F1,314.09, P0.052). With both

terms in a multiple regression, each lost itsindividual effect on pacing, but the overalladjusted r2 value increased to 26.5%, from6.2% (for body weight alone) and 18.2%(for minimum HR alone; Fig.1b). Likewise,median,but not minimum, daily travel dis-tances were positively correlated with pacing(F1,189.80,P0.003).

These results all held when total stereo-typical behaviours (including non-pacing)were analysed5.Naturally wide-ranging ani-mals did not, however, show more normalactivity in captivity (for example,minimumHR:F1,150.17, n.s.; DDT: F1,150.01,n.s.),nor did they move around more overallwithin their enclosures (for example, mini-mum HR:F1,180.61,n.s.; DDT:F1,180.10,n.s.). Home-range size therefore sti ll pre-dicted pacing, even when controlli ng forthe amount of total activity in captivity(for example, minimum HR: F1,142.65,P0.019). The degree of natural foragingand general activity, in contrast, did not pre-dict captive stereotypy or infant mortality5

(for example, the level of natural activit yversus pacing: F1,183.53, n.s.). Variationsin husbandry did not account for any ofthese findings5.

Our results show, to our knowledge for

the first time,that a part icular li festyle in thewild confers vulnerability to welfare prob-lems in captivity. Our study also revealsspecies that are inherently l ikely to fare badlyin zoos and similar establi shments.Amongthe carnivores, naturally wide-rangingspecies show the most evidence of stressand/or psychological dysfunction in capti-vity3,4,12,a finding that is a cause for concern,given the difficulties of conserving suchspecies in situ13. Husbandry of these speciesin captivity is therefore in need of improve-ment, such as provision of extra space (apolar bears typical enclosure size, for exam-

ple, is about one-mil lionth of its minimumhome-range size). Alternatively, zoos couldstop housing wide-ranging carnivores andconcentrate instead on species that respondbetter to being kept i n captivity.Ros Clubb,Georgia MasonAnimal Behaviour Research Group, Department of

Zoology,Uni versity of Oxford, South Parks Road,

Oxford OX1 3PS, UK

e-mai l: georgia.mason@zoology.ox.ac.uk

1. Mason,G.,Cooper, J. & Clarebrough,C.Nature410,

3536 (2001).

2. Dawkins,M . S.Appl.Anim. Behav. Sci.20,209225 (1988).

3. Robbins, T.W., Jones, G.H. & Wilkinson, L.S.

J.Psychopharmacol.10,3947 (1996).

4. Lewis, M. H., Gluck, J. P.,Bodfish,J.W., Beauchamp,A. J. &

Captivity effects on wide-ranging carnivoresAnim als that roam over a large territory in the w ild do not take kindly to be ing confined .

L

L

AF

AF

AM

AM

70

60

50

40

30

20

10

0

1

1 0 1 32 4 5234

0 1 2 3

Minimum homerange size (log km2)

Minimum homerange size (log km2;

accounting for body weight)

Captive-infantmort

ality

(%b

irths)

P B

P B

b

a

60

50

40

30

20

10

0Stereo

typyfrequency

(%

observation)

Figure 1 Natural ranging behaviour and welfare of species

from the order Carnivora in captivity. a, Carnivores minimum

home-range sizes in the wild predict captive infant mortality

(F1,1912.60, P0.001). b, Together with body weight (see text),

minimum home-range size also predicts stereotypic pacing in

captivity (F2,194.79, P0.011; controlling for phylogeny:

F2,173.11, P0.036). On these cross-species plots, a few

species from a range of families and with varying relation to the

regression line are highlighted: AF, Arctic fox (Alopex lagopus); PB,polar bear (Ursus maritimus); AM, American mink (Mustela vison);

L , l ion (Panthera leo). Values on the x-axes differ because fitted

values are used in b that incorporate body weight; the y-axis in b

shows data back-transformed from an arc-sine transformation.

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*Oak Ridge Nat ional Laboratory, Oak Ridge,

Tennessee 37831, USA

Department of Physics, University of Tennessee,Knoxvi lle, Tennessee 37996, USA

Transportati on Securit y Admini stration,

US Department of Homeland Securi ty,

Atlanti c City, New Jersey 08405, USA

Department of Mechanical Engineeri ng and the

Nevada Ventures Nanoscience Program, University

of Nevada, Reno, Nevada 89557,USA

e-mail : jdadams@unr.edu

1. Furton, K.G.& Myers, L.J.Talanta54,487500 (2001).

2. Colton, R.J. & Russell, J. N.Science299,13241325 (2003).

3. Czarnik,A.W.Nature394,417418 (1998).

4. Thundat, T., Chen, G.Y.,Warmack, R.J.,Alli son,D. P. &

Wachter,E.A. Anal. Chem. 67,519521 (1995).

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6. Muralidharan, G.et al.Ultramicroscopy97,433439 (2003).

7. Minne,S. C., Manalis,S. R.& Quate, C.F.Appl. Phys. Lett. 67,39183920 (1995).

8. Rogers, B.et al. Rev.Sci. Instruments(in the press).

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327333 (2003).

Competingfinancial interests: declared none.

Mailman, R.B.in Stereotyped Movements(eds Sprague,R. L.

& Newell, K. M.) 3767 (Am. Psychol. Assoc.,

Washington DC, 1996).

5. Clubb, R. E.The Roles ofForaging N iche,Rearing Condit ions and

Current Husbandry on the Development of Stereotypies in

Carnivores(Thesis,Univ.Oxford, 2001).

6. Meier,J. in Zoo and Wild Animal Medicine(ed.Fowler, M. E.)

842851 (Saunders,Phi ladelphia, 1986).

7. Shepherdson,D. J.,Mellen, J. D.& Hutchins, M. (eds) Second

Natur e: Environmental Enri chment for Capti ve Animal s

(Smithsonian Inst. Press,Washington DC,1998).

8. Gittleman, J. L. & Harvey,P. H. Behav.Ecol. Sociobiol. 10,

5763 (1982).

9. Gittleman,J.L. J. Mamm. 67,2336 (1986).

10.Purvis,A. & Rambaut, A.Comp.Appl. Biosci.11,247251 (1995).

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74,143175 (1999).

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Behav. 64,429437 (1998).

13.Woodroffe,R. & Ginsberg, J. R.Science280,21262128 (1998).

Competingfinancial interests: declared (see online version) .

in Fig.1.During event 1,before loading withTNT, a reference voltage pulse (25 volts) isapplied to the piezoresistive heater, causing atemporary upward spike in circuit outputthat is due to heating.TNT loading (event 2)causes a gradual upward shift in sensor out-put,which then gradually decreases when theTNT begins to desorb from the cantilever(event 3). The second pulse (5 volts) during

desorption does not raise the cantilevertemperature sufficiently for deflagration(event 4). The third pulse (25 volts) causesdeflagration, as shown by a visible smokeplume,and a dramatic mass decrease,whichis verified by a reduction in circuit output(event 5) that overwhelms the upward ther-mal signal evident in event 1.Post-deflagra-tion reference pulses of 25 volts resulted inspikes similar to the one seen in event 1.

The occurrence of deflagration wasinferred from three consistent observations.First, the canti lever returns to i ts pre-testresonance frequency after deflagration, sug-gesti ng that all of the adsorbed material hasbeen lost. Second, a specific voltage (corre-sponding to a threshold, or deflagration-point, temperature) is necessary to causedeflagration. Third, the measurement ofheat added to the cantilever during deflagra-tion shows that the reaction is exothermic,ruling out other possible reactions such asmelt ing,vaporization or decomposit ion.

Our method currently detects the defla-gration of as li ttl e as 70 picograms (1.91011

molecules) of TNT (calculated from the shiftin canti lever resonance). This limit of detec-ti on is the same as that of an improved ver-sion9of the ion-mobili ty mass-spectrometry

technology now used for airport security.Calculations show that the detection limitcould be improved by up to three orders ofmagnitude by using optimized cantilevers.

An explosive-detection technique basedon deflagrati on i s advantageous, becausedeflagration is a characteristic property ofthese substances.Other potentially interfer-ing but non-explosive substances tested including water, acetone, ethyl alcohol andgasoline all desorbed in our system beforethe voltage pulse was applied. In the absenceof a voltage pulse, desorption of nanogramquantities of deposited TNT takes tens ofminutes; comparable amounts of water oralcohol desorb in seconds.

Other explosive molecules can be detect-ed by this method and differentiated by theircompound-specific deflagration points anddesorption t imes (results not shown). Ourtechnique could also be used in conjunctionwith coated-cantilever chemical-sensingarrays5, in which the arrays serve as an initialindicator, and positi ve readings are verifiedby deflagration on an uncoated cantilever.L.A.Pinnaduwage*,A.Gehl*,D.L.Hedden*,G.Muralidharan*,T.Thundat*,R.T.Lareau,T.Sulchek,L.Manning,B.Rogers,M.Jones,J.D.Adams

Explosives

A microsensor fortrinitrotoluene vapour

Sensing devices designed to detectexplosive vapours are bulky, expensiveand in need of technological improve-

ment dogs remain the most effectivedetectors1 in the fight against terrorismand in the removal of land-mines2,3. Herewe demonstrate the deflagration of tr i-nitrotoluene (TNT) in a small localizedexplosion on an uncoated piezoresistivemicrocantilever. This explosive-vapour sen-sor, which has a detection capabil it y that i scomparable to that of a dog, should enableextremely sensitive, miniature detectiondevices to be used on a large scale.

Microcantilevers with specific coatingscan be used for chemical detection4,5, butTNT molecules, which are intrinsicallysticky,readily adhere to uncoated cantileversurfaces6. When the source of TNT isremoved, the TNT molecules slowly desorb.We found that applying a voltage pulse toan integrated piezoresistor during this de-sorption process causes the cantilever tem-perature to rise beyond the deflagrationpoint of TNT,resulting in a miniature defla-gration. Our canti levers did not degradeafter hundreds of pulses (1025 volts) anddeflagrations.

We monitored deflagration by captur ingmagnified high-speed video images,by mea-suring the deflection due to released heatusing an optical beam-bounce techniquethat i s used in atomic-force microscopy,andby measuring resonance-frequency shiftsand heat added with a piezoelectric/piezo-resistive cantilever7 operated in self-sensingmode by means of an a.c.bridge circuit8.Thecircuits output increases with mass loadingof adsorbed TNT and increasing tempera-ture; it decreases with mass desorption anddecreasing temperature.

A five-event TNT-detection test,using theself-sensing platform described, is illustrated

474 NATURE | VOL 425| 2 OCTOBER 2003 | www.nature.com/nature

Figure 1 Deflagration and detection of trinitrotoluene (TNT). a,

Sensor output plotted against time. During event 1 (numbered

arrow) of the test, a 25- volt reference pulse is sent to the piezo-

resistor before TNT loading begins; sensor output returns quickly

to almost its pre-pulse value. In event 2, TNT is gradually loaded

onto the cantilever and the resonance frequency decreases, causing

the sensor output to increase. After loading, the TNT begins to

desorb (event 3) and a 5-volt pulse (event 4) is insufficient to heat

the explosive on the cantilever to its deflagration point. However, a

25- volt pulse is sufficient to cause deflagration (event 5). b, Left,

diagram of the m icrocantilever, showing the integrated piezoelec-

tric sensor, piezoresistive heater, and TNT loaded on the cantilever

surface. Scale bar, 100 m. Right, deflagration is confirmed in

magnified high-speed video images; the smoke plume is visible,

particularly when illuminated by red laser light.

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