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An indicator of animal intelligence is thought to be the ability to judge ...

An indicator of animal intelligence is thought to be the ability to judge
relationships between members of the same species. This talent,
previously seen only in primates, seems to be evident in a bird.

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Vignal mathevon mottin 2004 nature Vignal mathevon mottin 2004 nature Document Transcript

  • letters to natureand Mars, many features of these planets would be different from ..............................................................those of the Earth. Further studies are necessary to address these andother issues (elasticity and anelasticity, electrical conductivity, Audience drives male songbirdradiative conductivity, energetics of stacking faults, effects ofimpurities on stability and properties of post-perovskite). Finally, response to partner’s voicewe note that the results of a recent, independent, experimental Clementine Vignal1,2, Nicolas Mathevon1 & Stephane Mottin2 ´ ´study26 of the post-perovskite phase transition are consistent withour theoretical and experimental findings. A 1 Equipe ‘Communications Acoustiques’ NAMC CNRS UMR8620, Universite ´ ´ Paris XI-Orsay and LBA Universite Jean Monnet, 42023 Saint-Etienne Cedex 2,Received 24 March; accepted 27 May 2004; doi:10.1038/nature02701. France1. Fiquet, G. Mineral phases of the Earth’s mantle. Z. Krist. 216, 248–271 (2001). 2 ´ TSI CNRS UMR5516 Universite Jean Monnet, 42023 Saint-Etienne Cedex 2,2. Panning, M. & Romanowicz, B. Inferences on flow at the base of Earth’s mantle based on seismic France anisotropy. Science 303, 351–353 (2004). .............................................................................................................................................................................3. Lay, T. & Helmberger, D. V. A shear velocity discontinuity in the lower mantle. Geophys. Res. Lett. 10, 63–66 (1983). According to the social intelligence hypothesis, social context4. Sidorin, I., Gurnis, M., Helmberger, D. V. & Ding, X. Interpreting D 00 seismic structure using synthetic represents an important force driving the selection of animal waveforms computed from dynamic models. Earth Planet. Sci. Lett. 163, 31–41 (1998). cognitive abilities such as the capacity to estimate the nature of5. Sidorin, I., Gurnis, M. & Helmberger, D. V. Evidence for a ubiquitous seismic discontinuity at the base of the mantle. Science 286, 1326–1331 (1999). the social relationships between other individuals1–4. Despite this6. Sidorin, I., Gurnis, M. & Helmberger, D. V. Dynamics of a phase change at the base of the mantle importance, the influence of this force has been assessed only in consistent with seismological observations. J. Geophys. Res. 104, 15005–15023 (1999). primates and never in other animals showing social inter-7. Su, W. J. & Dziewonski, A. M. Simultaneous inversion for 3-D variations in shear and bulk velocity in actions5–7. In this way, avian communication generally takes the mantle. Phys. Earth Planet. Inter. 100, 135–156 (1997). place in a network of signallers and receivers, which represents8. Masters, G. et al. in Earth’s Deep Interior: Mineral Physics and Tomography from the Atomic to the Global Scale (ed. Karato, S.-i.) 63–87 (AGU Geophysical Monograph 117, American Geophysical Union, an audience altering individual signalling behaviours8,9. Indeed, Washington DC, 2000). vocal amplitude10 and repertoire11 are known to be socially9. Saxena, S. K. et al. Stability of perovskite (MgSiO3) in the Earth’s mantle. Science 274, 1357–1359 regulated and the attitude towards the opposite sex may change (1996). depending on the audience8,12,13. This ‘audience effect’8,14–16 pro-10. Fiquet, G., Dewaele, A., Andrault, D., Kunz, M. & Le Bihan, T. Thermoelastic properties and crystal structure of MgSiO3 perovskite at lower mantle pressure and temperature conditions. Geophys. Res. vides support for the reality of social awareness in some bird Lett. 27, 21–24 (2000). species. However no evidence has yet been found to suggest that11. Serghiou, G., Zerr, A. & Boehler, R. (Mg,Fe)SiO3-perovskite stability under lower mantle conditions. birds are able to estimate the characteristics of the social Science 280, 2093–2095 (1998). relationships between group-mates. Here we show that the12. Shim, S. H., Duffy, T. S. & Shen, G. Y. Stability and structure of MgSiO3 perovskite to 2300-kilometer depth in Earth’s mantle. Science 293, 2437–2440 (2001). male of a gregarious songbird species—the zebra finch (Taenio-13. Ono, S., Ohishi, Y. & Mibe, K. Phase transition of Ca-perovskite and stability of Al-bearing pygia guttata)—pays attention to the mating status of conspecific Mg-perovskite in the lower mantle. Am. Mineral. (in the press). pairs, and uses this information to control its behaviour towards14. Ono, S., Sata, N. & Ohishi, Y. Phase transformation of perovskite structure in Fe2O3 at high pressures its female partner. and high temperatures. Am. Mineral. (submitted).15. Rodi, F. & Babel, D. Erdalkaliiridium(IV) - oxide: Kristallstruktur von CaIrO3. Z. Anorg. Allg. Chem. Zebra finches are monogamous flock-forming birds that seem to 336, 17–23 (1965). use acoustic recognition for pair-bond maintenance11,17. A number16. Perdew, J. P., Burke, K. & Ernzerhof, M. Generalized gradient approximation made simple. Phys. Rev. of different vocalizations are produced by this species11, distance Lett. 77, 3865–3868 (1996). calls being the most frequently emitted by both males and females.17. Oganov, A. R. & Brodholt, J. P. High-pressure phases in the Al2SiO5 system and the problem of Al- phase in Earth’s lower mantle: ab initio pseudopotential calculations. Phys. Chem. Miner. 27, 430–439 Distance calls are used by the members of a pair to remain in contact (2000). when the flock is foraging or feeding and especially when the birds18. Baroni, S., de Gironcoli, S., Dal Corso, A. & Gianozzi, P. Phonons and related crystal properties from lose visual contact with each other11. As in many gregarious species, density-functional perturbation theory. Rev. Mod. Phys. 73, 515–562 (2001). vocal recognition is thus likely to be a key component of reproduc-19. Urusov, V. S. Theoretical Crystal Chemistry (Moscow State Univ. Press, Moscow, 1987) [in Russian].20. Oganov, A. R., Brodholt, J. P. & Price, G. D. The elastic constants of MgSiO3 perovskite at pressures tive success and it should be supported in both sexes by acoustic and temperatures of the Earth’s mantle. Nature 411, 934–937 (2001). cues of distance calls18–20. Previous laboratory experiments testing21. Oganov, A. R., Brodholt, J. P. & Price, G. D. Ab initio elasticity and thermal equation of state of isolated birds demonstrated that the female zebra finch is able to MgSiO3 perovskite. Earth Planet. Sci. Lett. 184, 555–560 (2001). recognize its mate’s vocalizations from other males’ vocalizations17,22. Ono, S., Hirose, K., Isshiki, M., Mibe, K. & Saito, Y. Equation of state of hexagonal aluminous phase of natural composition to 63 GPa at 300 K. Phys. Chem. Miner. 29, 527–531 (2002). but never succeeded in demonstrating a mutual acoustic recog-23. Jeanloz, R. & Williams, Q. The core-mantle boundary region. Rev. Mineral. 37, 241–259 (1998). nition between mates11. In the natural biological context described24. Wentzcovitch, R. M., Karki, B. B., Karato, S. & da Silva, C. R. S. High pressure elastic anisotropy of above, it is very unlikely that wild male zebra finches do not MgSiO3 perovskite and geophysical implications. Earth Planet. Sci. Lett. 164, 371–378 (1998). recognize their mates’ voices. Two main hypotheses can thus be25. Montagner, J.-P. & Nataf, H.-C. A simple method for inverting the azimuthal anisotropy of surface waves. J. Geophys. Res. 91, 511–520 (1986). envisaged: either captive zebra finches have lost some cognitive26. Murakami, M., Hirose, K., Kawamura, K., Sata, N. & Ohishi, Y. Post-perovskite phase transition in capacities because of domestication (for instance, females’ calls may MgSiO3. Science 304, 855–858 (2004). be less individualized, and/or males may no longer be able to ¨27. Blochl, P. E. Projector augmented-wave method. Phys. Rev. B 50, 17953–17979 (1994). recognize them), or tested males do not show preferential response28. Kresse, G. & Joubert, D. From ultrasoft pseudopotentials to the projector augmented-wave method. Phys. Rev. B 59, 1758–1775 (1999). to their mate’s voice owing to a modification of their natural ¨29. Kresse, G. & Furthmuller, J. Efficiency of ab initio total-energy calculations for metals and behaviour by their socially isolated position during the playback semiconductors using a plane-wave basis set. Comp. Mater. Sci. 6, 15–50 (1996). tests. Indeed social isolation could be a situation of stress in30. Gonze, X. et al. First-principles computation of materials properties: the ABINIT software project. comparison to the natural context where the zebra finch lives in Comp. Mater. Sci. 25, 478–492 (2002). large groups and experiences permanent social interactions thatAcknowledgements Calculations were performed at CSCS (Manno) and ETH Zurich. We thank may influence mate-directed behaviour.P. Ulmer, A.N. Halliday, S. Goes, F. Cammarano, A.B. Thompson and P.J. Tackley for discussions, To determine whether the vocalizations of female zebra finchesand Y. Ohishi and N. Sata for experimental support. Synchrotron radiation experiments were support mate recognition, we analysed the acoustic structure ofperformed at the BL10XU, SPring-8. distance calls, searching for acoustic cues which could encode the emitter’s individual identity. The female distance call is a complexCompeting interests statement The authors declare that they have no competing financial sound with a fundamental frequency associated with severalinterests. harmonics (Fig. 1a). This sound is frequency- and amplitude-Correspondence and requests for materials should be addressed to A.R.O. modulated. With reference to frequency-modulation character-(a.oganov@mat.ethz.ch). istics, the distance call can be divided into three segments of448 ©2004 Nature Publishing Group NATURE | VOL 430 | 22 JULY 2004 | www.nature.com/nature
  • letters to natureFigure 1 Acoustic structure of the distance call of the female zebra finch. a, Spectrogram modulation). The amplitude modulations are represented by a greyscale. b, Acoustic cuesof the call of a female zebra finch. The call can be divided into an initial part (rapid and loud characterizing the fundamental frequency: the beginning frequency (F start), theascending frequency modulation), a long and loud second part with no frequency frequencies at the start and at the end of the second part (F 1, F 2), the frequency at themodulation (the stable part) and a final part (rapid and soft descending frequency end of the third part (F end), and the duration of the second part (d stable).different durations (Fig. 1a): the initial segment defined by a rapid Methods). The discriminant analysis based on the whole set ofand loud ascending frequency modulation, a long and loud second analysed acoustic parameters allows us to discriminate amongsegment with no frequency modulation (the stable part), and a third 100% of the seven females (Fig. 2). According to our analysis, itsegment defined by a rapid and soft descending frequency modu- thus appears that female distance calls contain potential cues tolation. To assess which of these spectral, amplitude and temporal support individual identity coding and thus recognition by males.cues could support individual identity coding and thus vocal To investigate whether mate recognition by males is affected byrecognition by males, we defined a set of 17 parameters describing the current social context, we tested to see whether the vocalthe acoustic structure of the call, and measured the intra-individual response of males to their partner’s calls and to the calls of a familiarand inter-individual variability of each parameter with a non- female changes depending on the composition of the audience. Weparametric analysis of variance. For each measured parameter the performed playback experiments with 15 male zebra finches. Eachdifference between the females is significant (Kruskall–Wallis of these birds was paired for several months with a different femaleANOVA, P , 0.05) and the variation within individuals is smaller and raised at least one brood. The tested male was separated from itsthan that among individuals. In particular, the four spectral mate, put in an experimental cage one night before the test, andparameters (F start, F 1, F 2, F end; Fig. 1b) describing the frequency assigned to one of the following social contexts: (1) the ‘unmatedmodulation of the fundamental frequency are highly individualized males’ context: two single males were placed in a companion cage(potential for individual identity coding values (PIC) .2; see near the experimental cage, (2) the ‘mated pair’ context: a normal male–female pair was placed in the companion cage, and (3) the ‘unmated pair’ context: a male and a female that were not paired were placed in two different companion cages. During playback, the Figure 3 Response of male to female voices as a function of the mating status of the audience. The tested males were placed in different social contexts: (1) ‘unmated males’ (two single males placed in a companion cage), (2) ‘mated pair’ (a normal male–femaleFigure 2 Discriminant analysis on the 17 acoustic parameters of the female call. The calls pair in a companion cage), and (3) ‘unmated pair’ (a male and a female, not paired, in twoof seven individuals are represented according to the two main functions of the analysis. different companion cages). Asterisk, significant difference between the male responsesEach female is represented by one symbol and each point corresponds to one analysed to mate and familiar female in the ‘mated pair’ context. The ‘spontaneous’ activity of thecall. The seven females are discriminated, so the distance calls could support individual male (in the absence of any playback stimulus) is reported. Error bars indicate standardidentity coding. errors.NATURE | VOL 430 | 22 JULY 2004 | www.nature.com/nature ©2004 Nature Publishing Group 449
  • letters to naturemale, accompanied by its audience, was presented with two sets of analysis, followed by a discriminant analysis. To describe the intra-individual and inter- individual variations of each parameter we used the coefficient of variation (CV)24. Forstimuli: a series of calls of its mate and a series of calls of a familiar each parameter we calculated CVi (within individual CV) and CVb (between individualfemale. The male’s response was assessed by counting the number of CV) according to the formula for weak samples: CV ¼ {100(SD/X mean)[1 þ 1/(4n)]}calls emitted during the stimulus broadcasting. The audience where SD is standard deviation, X mean is the mean of the sample and n is the populationbehaviour in response to stimuli was also monitored. Before the sample25. To assess the potential of individual coding (PIC) for each parameter, weplayback, the ‘spontaneous’ activity of the male was always very low calculated the ratio CVb/CVi, mean (CVi, mean being the mean value of the CVi of all individuals). For a given parameter, a PIC value greater than one suggests that this(Fig. 3) and not dependent on the audience (Kruskall–Wallis parameter may be used for individual recognition because its intra-individual variability isANOVA, P ¼ 0.069). Whereas the audience behaviour seems to smaller than its inter-individual variability.be fully independent of which female’s calls were being presented A synthetic copy of three distance calls of each female was created with Avisoft-SAS Lab(Wilcoxon matched-pairs test: ‘unmated males’, P ¼ 0.892; ‘mated Pro software (version 4.16, 2002) in order to have experimental signals with neither any background noise nor sound degradation. These synthetic calls were used for playbackpair’, P ¼ 0.419; ‘unmated pair’, P ¼ 0.715), the sex and the mating tests. For playback tests, each tested male bird (n ¼ 15) was separated from its mate andstatus of the accompanying birds modified the response of tested placed in an experimental cage (240 £ 50 £ 50 cm, equipped with roosts) one night beforemales to the playback of the calls of their mate (Kruskall–Wallis the start of stimulus presentation. The experimental cage was in a soundproof chamberANOVA, P , 0.04) (Fig. 3). When the male was in the presence of with a 12 h light/12 h dark photoperiod. Another cage was placed near the experimental cage in the chamber: this companion cage contained the two birds defining the socialan established male–female pair, its vocal response was significantly context. This audience was composed of different individuals during each trial. Thestronger to its partner’s calls than to the familiar female’s calls playback equipment was constituted by two high-fidelity speakers (JBLTLX 12) connected(Wilcoxon matched-pairs test, P , 0.05). Alternatively, when the to a DAT recorder (Sony DTC-ZE 700) placed at either end of the cage. During each testmale was in the presence of unmated conspecifics, that is, two single only one randomly chosen speaker emitted the playback stimuli (sound level, 70 dB at 1 m). The tested male was presented with two sets of stimuli: a series of distance calls of itsmales or one single female and one single male, its response did not mate and a series of distance calls of a familiar female (series were broadcast at random;differ significantly between the two stimuli sets (Wilcoxon series duration, 5.0 s, one call per second; interval between series, 30 s). As all the birdsmatched-pairs test, P ¼ 0.593 and 0.138, respectively), showing (audience birds, tested males and their mates, familiar females) had been bred in the sameno preference to the calls of its own mate. Finally, the audience did aviary, all acoustic stimuli can be considered as perceptually equivalent for the audiencenot seem to influence the male’s response to the calls of a familiar birds. The vocal and locomotor activity of the bird was recorded with a video recorder (Sony DCR-TRV24E) and the number of distance calls emitted during the broadcasting offemale (Kruskall–Wallis ANOVA, P ¼ 0.348). These experiments the stimuli was counted. The audience behaviour was similarly assessed. Before theclearly show that male zebra finches have the ability to recognize playback broadcasting, the male ‘spontaneous’ activity (call rate per 5.0 s) was alsotheir mate’s voice, but that partner acoustic recognition is expressed measured. The effects of the mating status of the accompanying birds on the ‘spontaneous’differently according to the social relationships between accompa- activity of males and on the response of males to the playback of the calls of their mate or of a familiar female were analysed with Kruskall–Wallis ANOVAs (P ¼ 0.05).nying birds. This effect of social context on acoustic communication Complementary tests (Wilcoxon matched-pairs test24, P ¼ 0.05) were performed toin songbirds is in accordance with neurophysiological data: birds compare the responses to both stimuli in each social context. We also tested whether therecorded in isolation or in visual and auditory contact with a female audience behaviour was independent of which female’s calls were being presentedshow different levels of electrophysiological activity21 and ZENK (Wilcoxon matched-pairs test, P ¼ 0.05).gene expression22 within auditory brain nuclei. Received 31 March; accepted 11 May 2004; doi:10.1038/nature02645. The present results support the idea that songbirds are capable of 1. Barton, R. A. & Dunbar, R. I. M. in Machiavellian Intelligence II: Extensions and Evaluations (edsbehaviours that are not just “incidentally communicative”12,13. In Whiten, A. & Byrne, R. W.) 240–263 (Cambridge Univ. Press, Cambridge, 1997).spite of the fact that recognizing one’s partner is often crucial to 2. Byrne, R. W. & Whiten, A. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes and Humans (Clarendon, Oxford, 1988).reproductive success, the vocal response to one’s mate does not seem 3. Dunbar, R. I. M. The social brain hypothesis. Evol. Anthropol. 6, 178–190 (1998).to be reflexive but can be modulated by the presence of companions. 4. Adolphs, R. Cognitive neuroscience of human social behaviour. Nature Rev. Neurosci. 4, 165–178Moreover, this precise regulation of signalling behaviour with (2003). 5. Perry, S., Barrett, C. & Manson, J. H. White-faced capuchin monkeys show triadic awareness in theirregard to the mating status of conspecifics provides evidence that choice of allies. Anim. Behav. 67, 165–170 (2004).songbirds experiencing gregarious life can show awareness of social 6. Jolly, A. Lemur social behaviour and primate intelligence. Science 153, 501–506 (1966).relationships comparable to those demonstrated by social mammals 7. Tomasello, M. & Call, J. Primate Cognition (Oxford Univ. Press, Oxford, 1997).such as primates7. This ability might be linked to the cognitive 8. Baltz, A. P. & Clark, A. B. Extra-pair courtship behaviour of male budgerigars and the effect of an audience. Anim. Behav. 53, 1017–1024 (1997).demands of social living3,4, which are potentially an important force 9. McGregor, P. K., Otter, K. & Peake, T. M. in Animal Signals: Signalling and Signal Design in Animaldriving the evolution of intelligence. Indeed, one possible ultimate Communication (eds Espmark, Y., Amundsen, T. & Rosenqvist, G.) 329–340 (Tapir Academic,explanation of why male songbirds may respond to their partner’s Trondheim, Norway, 2000).voice in the presence of a paired audience might be that the presence 10. Cynx, J. & Gell, C. Social mediation of vocal amplitude in a songbird, Taeniopygia guttata. Anim. Behav. 67, 451–455 (2004).of a mated male expressing female-guarding behaviour could 11. Zann, R. The Zebra Finch: a Synthesis of Field and Laboratory Studies 196–213 (Oxford Univ. Press,stimulate similar mate-guarding signalling by the tested male. Oxford, 1996).Finally, our work emphasizes that playback results can be influenced 12. Evans, C. S. & Evans, L. Chicken food calls are functionally referential. Anim. Behav. 58, 307–319 (1999).by the presence of a particular audience, stressing the importance of 13. Evans, C. S. & Marler, P. Food calling and audience effects in male chickens, Gallus gallus: theirconsidering the social environment during experiments. A relationships to food availability, courtship and social facilitation. Anim. Behav. 47, 1159–1170 (1994). 14. Marler, P., Dufty, A. & Pickert, R. Vocal communication in the domestic chicken: II. Is a sender sensitive to the presence and nature of a receiver? Anim. Behav. 34, 194–198 (1986).Methods 15. Striedter, G. F., Freibott, L., Hile, A. G. & Burley, N. T. For whom the male calls: an effect of audienceAdult zebra finches (Taeniopygia guttata) served as the subjects for this study and were on contact call rate and repertoire in budgerigars, Melopsittacus undulatus. Anim. Behav. 65, 875–882naive to all testing procedures. Birds were bred in an aviary (12 h light/12 h dark (2003).photoperiod with adapted wavelengths); food and water were provided ad libitum and 16. Johnstone, A. R. Eavesdropping and animal conflict. Proc. Natl Acad. Sci. USA 98, 9177–9180 (2001).temperature was maintained between 23 and 25 8C. All birds were paired for several 17. Miller, D. B. The acoustic basis of mate recognition by female zebra finches (Taeniopygia guttata).months and raised at least one brood. All experiments occurred between 9 a.m. and noon. Anim. Behav. 27, 376–380 (1979).During testing periods, temperature, food and water conditions were the same as in the 18. Charrier, I., Mathevon, N. & Jouventin, P. Mother’s voice recognition by seal pups. Nature 412, 873aviary. The experimental protocols were approved by the Jean Monnet University’s animal (2001).care committee. ´ 19. Belin, P., Fecteau, S. & Bedard, C. Thinking the voice: neural correlates of voice perception. Trends Seven female zebra finches were recorded for analysis of female distance calls. Each Cogn. Sci. 8, 129–135 (2004).female was isolated from its mate and seven to ten distance calls were recorded with a 20. Insley, S. J. Long-term recognition in the northern fur seal. Nature 406, 404–405 (2000).Sennheiser MD42 microphone, placed 0.3 m above the cage, connected to a Marantz 21. Hessler, N. A. & Doupe, A. J. Social context modulates singing-related neural activity in the songbirdPMD690/W1B recorder with 22,050-Hz sampling rate. We analysed a total of 65 female forebrain. Nature Neurosci. 2, 209–211 (1999).distance calls using Syntana software23 and Praat version 4.0.19. We defined seventeen 22. Jarvis, E. D., Scharff, C. & Grossman, M. R. For whom the bird sings: context-dependent genespectral, temporal and amplitude acoustic cues to describe the calls’ acoustic structure. expression. Neuron 21, 775–788 (1998).These measured parameters allowed statistical analysis of the cues potentially supporting 23. Aubin, T. Syntana: a software for the synthesis and analysis of animal sounds. Bioacoustics 6, 80–81individual identity coding and thus recognition by males. We performed a non-parametric (1994).analysis of variance (Kruskall–Wallis ANOVA, P ¼ 0.05) and a principal components 24. Sokal, R. R. & Rohlf, F. J. Biometry 57–58 & 443 (Freeman, New York, 1995).450 ©2004 Nature Publishing Group NATURE | VOL 430 | 22 JULY 2004 | www.nature.com/nature
  • letters to nature ´25. Robinson, P., Aubin, T. & Bremond, J. C. Individuality in the voice of emperor penguin Aptenodytes study implicated Ebola virus as the cause of a more than 50% forsteri: adaptation to a noisy environment. Ethology 94, 279–290 (1993). reduction in the number of chimpanzees and gorillas in large areasAcknowledgements This research was supported by the Interdisciplinary Program “Cognition of Central Africa9. Ebola was also shown as the main cause of deathand Information Processing” of the Centre National de la Recherche Scientifique (CNRS). C.V. is in two epidemics in 1992 and 1994 that reduced the size of asupported by the French Ministry of National Education. We thank C. Bouchut, M. Rabearinaivo ¨ monitored community of chimpanzees in the Taı National Parkand S. Tisseur for their help during the work, L. Bloomfield for improving the English, andI. Charrier for her advice on previous drafts of the manuscript. from 51 to 31 individuals10,11. The behaviour and apparent health of chimpanzees in the Taı ¨Competing interests statement The authors declare that they have no competing financial National Park have been closely monitored since 1984, and threeinterests. communities (North, Middle and South) are currently under observation11. In October 2001, four apparently healthy individualsCorrespondence and requests for materials should be addressed to N.M.(mathevon@univ-st-etienne.fr). ` (Dorry, Gargantua, Gisele and Goma) of the North community left the main group and were not followed by observers. Three days later, the one- to two-day-old remains of three of the chimpanzees were found within 50 metres of each other. Six weeks later, a skeleton attributed to Goma was found about 200 metres away. A new cluster of unexpected deaths occurred in the Middle.............................................................. community in February 2002. The body of Noah, a juvenile male who exhibited no previous signs of illness, was found the morningAnthrax kills wild chimpanzees of 13 February near his sleeping nest, and was estimated to have ´in a tropical rainforest been dead for approximately five hours. The next day, Leo, the top- ranking male of the same community, showed sudden signs of weakness, vomited several times and died within two hours of theFabian H. Leendertz1,2,3, Heinz Ellerbrok2, Christophe Boesch1, onset of symptoms. Another community member, Koulo, was lastEmmanuel Couacy-Hymann4, Kerstin Matz-Rensing5, ¨Regine Hakenbeck6, Carina Bergmann6, Pola Abaza1,2, observed on that day and never seen again despite intensiveSandra Junglen1,2, Yasmin Moebius1, Linda Vigilant1, Pierre Formenty7 searching, and hence is presumed dead. Finally, in June 2002,& Georg Pauli2 Olduvai, a subadult male of the South community, was found near to death less than three hours after he had been last observed in1 Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, normal condition.D-04103 Leipzig, Germany In total, eight sudden deaths were recorded in the three chim-2 ¨ Zentrum fur biologische Sicherheit, Robert Koch-Institut, Nordufer 20, panzee communities between October 2001 and June 2002, and allD-13353 Berlin, Germany of the individuals were in apparent good health shortly before,3 Institute for Parasitology and International Animal Health, Free University of suggesting an acute infectious agent as the cause. Samples from all ¨Berlin, Konigsweg 67, D-14163 Berlin, Germany4 six available dead individuals tested negative for the filo- and Lanada/Lcpa, Bingerville, Ivory Coast5 ¨ German Primate Center, Kellnerweg 4, D-37077 Gottingen, Germany arenaviruses Ebola, Marburg and Lassa. Pathological and histologi-6 Department of Microbiology, University of Kaiserslautern, Paul-Ehrlich-Straße, ´ cal examination of the remains of Leo and Noah revealed haemor-D-67663 Kaiserslautern, Germany rhages presenting as small ecchymoses in nearly all inner organs,7 ¨ Ebola Taı Forest Project, World Health Organisation, WHO Office, Abidjan, particularly in the intestines and lungs, and the lungs wereIvory Coast also characterized by oedema and emphysema. Microscopic exami-............................................................................................................................................................................. nation revealed Gram-positive, rod-shaped bacteria located intra-Infectious disease has joined habitat loss and hunting as threats and extravascularly in all tissues examined—spleen, liver, lung,to the survival of the remaining wild populations of great apes.Nevertheless, relatively little is known about the causativeagents1–3. We investigated an unusually high number of suddendeaths observed over nine months in three communities of wild ¨chimpanzees (Pan troglodytes verus) in the Taı National Park,Ivory Coast. Here we report combined pathological, cytologicaland molecular investigations that identified Bacillus anthracis asthe cause of death for at least six individuals. We show thatanthrax can be found in wild non-human primates living in atropical rainforest, a habitat not previously known to harbourB. anthracis. Anthrax is an acute disease that infects ruminants4,5,but other mammals, including humans, can be infected throughcontacting or inhaling high doses of spores or by consumingmeat from infected animals6. Respiratory and gastrointestinalanthrax are characterized by rapid onset, fever, septicaemia and ahigh fatality rate without early antibiotic treatment6,7. Ourresults suggest that epidemic diseases represent substantialthreats to wild ape populations, and through bushmeat con-sumption also pose a hazard to human health. Long-term studies of wild chimpanzees habituated to humanobservation have revealed that mortality rates of adult animals arehigh and several times in excess of those reported for human hunter-gatherer communities8. Unfortunately, although direct observationof ill animals has suggested infectious disease as the cause of many ´ Figure 1 Histological section of lung tissues of the chimpanzee Leo. Thin sections ofdeaths and disappearances, practical difficulties concerning acqui- altered tissues were stained with haematoxylin and eosin. Under a light microscope, longsition and testing of diagnostic samples have usually precluded rod-shaped bacteria (arrows) were visible. Left panel, section of the lung parenchyma withidentification of the disease-causing agent(s). However, one recent oedema and emphysema. Right panel, intravascular bacteria. Scale bars, 20 mm.NATURE | VOL 430 | 22 JULY 2004 | www.nature.com/nature ©2004 Nature Publishing Group 451