4
2 APRIL 2004 VOL 304 SCIENCE www.sciencemag.org 46 CREDIT: VIRGINIA INSTITUTE OF MARINE SCIENCE Ongoing Controversy over Pfiesteria READERS OF J. KAISERS ARTICLE “THE Pfiesteria conundrum: More study, less certainty” (News of the Week, 2 Jan., p. 25) may have missed the fact that there is more certainty, not less, about the toxic microbe Pfiesteria. Some Virginia Institute of Marine Science (VIMS) scientists and their collabo- rators had earlier concluded that Pfiesteria as a whole is not toxigenic and only physically attacks fish (1, 2), based on one strain of P. shumwayae, CCMP2089. Yet Pfiesteria has nontoxic as well as toxic strains (3), and expression of toxicity by toxic strains depends on culture conditions (4). Other laboratories have now shown that when cultured and tested appropriately (5, 6), strain CCMP2089 is ichthyotoxic. Kaiser states that I declined to send these VIMS scientists toxic Pfiesteria culture. I had offered to provide them toxic culture and to show them how to grow it to express toxicity, if they would support the cost. Kaiser also describes me as not providing toxic Pfiesteria to the research community in general, although I have provided it to more than 40 scientists. Kaiser does not mention the two recent publications on Pfiesteria effects on fish and mammals: A highly toxic Pfiesteria strain killed shellfish larvae as a toxic effect, without physical contact (7), and Pfiesteria toxin caused hippocampal damage in rats (8). Kaiser mentions only an unpublished study that, logically, found no evidence of health impacts from Pfiesteria because there were no toxic Pfiesteria blooms during the study. Kaiser credits the VIMS scientists (1) for having found that Pfiesteria can kill larval finfish by physical attack, which colleagues and I had earlier published [(4), p. 200], and she asserts that I have attributed fish death from Pfiesteria only to toxin. I have described physical attack and toxin as important interac- tive factors [(9), p. 672]. Kaiser reports only negative findings about Pfiesteria amoebae. She mentions a study by Litaker et al. (10), who did not find amoebae in two P. piscicida strains (cultures 2 to 10 years old, of uncertain toxicity status) and, on that basis, concluded that the species does not form amoebae. She does not mention a peer- reviewed paper (11) with corrective informa- tion: Amoebae are minor to the toxicity issue; toxin is produced mostly by flagellated stages. Cultured toxic strains mostly have formed amoebae within the first few months after field isolation, and nontoxic strains rarely form amoebae. Kaiser describes a workshop presentation by P. Gillevet (VA Common- wealth Univ.), who did not find Pfiesteria amoebae in some estuarine sediments. She does not mention recent research from an international conference presentation: P. Rublee (University of North Carolina) tested estuarine sediments and obtained a positive signal for Pfiesteria by PCR. Amoebae from those sediments were cloned by my labo- ratory, cultured for eight weeks with crypto- phyte prey in the absence of other Pfiesteria stages, and sent to Rublee, who confirmed them as Pfiesteria amoebae with PCR. Rublee then amplified and cloned 18S rDNA fragments, which were sequenced by another laboratory. The amoebae sequence was a perfect match to the sequence for P. piscicida zoo- spores (12). Kaiser consistently fails to include new findings that are actu- ally about toxic Pfiesteria, or does not emphasize their significance. The facts remain: Pfiesteria species have toxic strains. Their toxin adversely affects fish and mammals (5–8, 13). Further study is impor- tant, because it will provide the tools needed by resource managers and public health officials to mitigate impacts when there are more toxic Pfiesteria blooms. JOANN BURKHOLDER Center for Applied Aquatic Ecology, North Carolina State University, 620 Hutton Street, Suite 104, Raleigh, NC 27606, USA. References 1. W. K. Vogelbein et al., Nature 418, 967 (2002). 2. J. P. Berry et al., Proc. Natl. Acad. Sci. U.S.A. 99, 10970 (2002). 3. D. D.Turgeon et al., Protocols for Monitoring Pfiesteria and Related Health and Environmental Conditions in U.S. Coastal Waters (National Oceanic & Atmospheric Administration, National Ocean Service, National Center for Coastal Ocean Science and Center for Coastal Monitoring and Assessment, Silver Spring, MD, 2001). 4. J. M. Burkholder, H. B. Glasgow, N. J. Deamer-Melia, Phycologia 40, 186 (2001). 5. P. D. R. Moeller et al., Environ. Health Perspect. 109, 739 (2001). 6. A. S. Gordon, B. J. Dyer, D. Seaborn, H. G. Marshall, Harmful Algae 1, 85 (2002). 7. J. Springer, S. E. Shumway, J. M. Burkholder, H. B. Glasgow, Mar. Ecol. Prog. Ser. 245, 1 (2003). 8. E. D. Levin et al., Neurotoxicol. Teratol. 25, 419 (2003). 9. J. M. Burkholder et al., Environ. Health Perspect. 109, 667 (2001). 10. R. W. Litaker et al., J. Phycol. 38, 442 (2002). 11. J. M. Burkholder, H. B. Glasgow, J. Phycol. 38, 1261 (2002). 12. J. Burkholder, presentation at 10th International Conference on Harmful Algae, St. Petersburg, FL, Oct. 2002. 13. L. M. Grattan et al., Lancet 352, 532 (1998). Response MY REPORT STATED THAT JOANN Burkholder’s lab had declined to share its toxic cultures with “critics.” The fact that more than 40 scientists have received Pfiesteria material from Burkholder, but certain other laboratories have not, was discussed in a previous news story (News Focus, 11 Oct. 2002, p. 346). For example, a request for toxic cultures from researchers at the University of Maryland was turned down because Burkholder decided that the several thousand dollars they offered was not suffi- cient. The VIMS team sent a written request for toxic cultures to Burkholder in August 2002. Burkholder responded that she “cannot” supply cultures without also providing “training to use them properly”; this, she later indicated, would cost $40,000. Burkholder instead suggested a collaboration and sent VIMS a possible research plan in late 2002. According to VIMS scientists, Burkholder did not reply to their response, an e-mail sent 19 December 2002 that called the plan “an appropriate starting point” and suggested next steps. The “recent research” showing that an amoebae sequence matched the sequence for P. piscicida zoospores was presented in October 2002, more than a year before the meeting on which I reported, and has not been published; Burkholder says this culture was lost in a power outage. The fact that the Burkholder lab’s attempts to isolate possible amoeboid Pfiesteira in 2003 yielded only true amoebae species seemed Pfiesteria feeding on fish epidermis. Letters to the Editor Letters (~300 words) discuss material published in Science in the previous 6 months or issues of general interest. They can be submitted through the Web (www.letter2science.org) or by regular mail (1200 New York Ave., NW, Washington, DC 20005, USA). Letters are not acknowledged upon receipt, nor are authors generally consulted before publication. Whether published in full or in part, letters are subject to editing for clarity and space. L ETTERS on September 26, 2012 www.sciencemag.org Downloaded from

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2 APRIL 2004 VOL 304 SCIENCE www.sciencemag.org46

CR

ED

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IRG

INIA

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ST

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E

Ongoing Controversy

over Pfiesteria

READERS OF J. KAISER’S ARTICLE “THE

Pfiesteria conundrum: More study, lesscertainty” (News of the Week, 2 Jan., p. 25)may have missed the fact that there is morecertainty, not less, about the toxic microbePfiesteria. Some Virginia Institute of MarineScience (VIMS) scientists and their collabo-rators had earlier concluded that Pfiesteria asa whole is not toxigenic and only physicallyattacks fish (1, 2), based on one strain of P.shumwayae, CCMP2089. Yet Pfiesteria hasnontoxic as well as toxic strains (3), andexpression of toxicity by toxic strains dependson culture conditions (4). Other laboratorieshave now shown that when cultured andtested appropriately (5, 6), strain CCMP2089is ichthyotoxic.

Kaiser states that I declined to sendthese VIMS scientists toxic Pfiesteriaculture. I had offered to provide them toxicculture and to show them how to grow it toexpress toxicity, if they would support thecost. Kaiser also describes me as notproviding toxic Pfiesteria to the researchcommunity in general, although I haveprovided it to more than 40 scientists.

Kaiser does not mention the two recentpublications on Pfiesteria effects on fishand mammals: A highly toxic Pfiesteriastrain killed shellfish larvae as a toxiceffect, without physical contact (7), andPfiesteria toxin caused hippocampaldamage in rats (8). Kaiser mentions onlyan unpublished study that, logically, foundno evidence of health impacts fromPfiesteria because there were no toxicPfiesteria blooms during the study.

Kaiser credits the VIMS scientists (1) forhaving found that Pfiesteria can kill larvalfinfish by physical attack, which colleagues

and I had earlier published [(4), p. 200], andshe asserts that I have attributed fish deathfrom Pfiesteria only to toxin. I have describedphysical attack and toxin as important interac-tive factors [(9), p. 672].

Kaiser reports only negative findings aboutPfiesteria amoebae. She mentions a study byLitaker et al. (10), who did not find amoebaein two P. piscicida strains (cultures 2 to 10years old, of uncertain toxicity status) and, onthat basis, concluded that the species does notform amoebae. She does not mention a peer-reviewed paper (11) with corrective informa-tion: Amoebae are minor to the toxicity issue;toxin is produced mostly by flagellated stages.Cultured toxic strains mostly have formedamoebae within the first few months afterfield isolation, and nontoxic strains rarelyform amoebae. Kaiser describes a workshoppresentation by P. Gillevet (VA Common-wealth Univ.), who did not find Pfiesteriaamoebae in some estuarine sediments. Shedoes not mention recent research from aninternational conference presentation: P.Rublee (University of North Carolina) testedestuarine sediments and obtained a positivesignal for Pfiesteria by PCR. Amoebae from those sediments were cloned by my labo-ratory, cultured for eight weeks with crypto-phyte prey in the absence of other Pfiesteria

stages, and sent to Rublee, whoconfirmed them as Pfiesteriaamoebae with PCR. Rublee thenamplified and cloned 18S rDNA fragments, which were sequenced by another laboratory. The amoebaesequence was a perfect match to the sequence for P. piscicida zoo-spores (12).

Kaiser consistently fails toinclude new findings that are actu-ally about toxic Pfiesteria, or doesnot emphasize their significance.The facts remain: Pfiesteria specieshave toxic strains. Their toxinadversely affects fish and mammals(5–8, 13). Further study is impor-

tant, because it will provide the toolsneeded by resource managers and publichealth officials to mitigate impacts whenthere are more toxic Pfiesteria blooms.

JOANN BURKHOLDER

Center for Applied Aquatic Ecology, North Carolina

State University, 620 Hutton Street, Suite 104,

Raleigh, NC 27606, USA.

References

1. W. K. Vogelbein et al., Nature 418, 967 (2002).2. J. P. Berry et al., Proc. Natl. Acad. Sci. U.S.A. 99, 10970

(2002).3. D. D.Turgeon et al., Protocols for Monitoring Pfiesteria and

Related Health and Environmental Conditions in U.S.Coastal Waters (National Oceanic & Atmospheric

Administration, National Ocean Service, National Centerfor Coastal Ocean Science and Center for CoastalMonitoring and Assessment, Silver Spring, MD, 2001).

4. J. M. Burkholder, H. B. Glasgow, N. J. Deamer-Melia,Phycologia 40, 186 (2001).

5. P. D. R. Moeller et al., Environ. Health Perspect. 109,739 (2001).

6. A. S. Gordon, B. J. Dyer, D. Seaborn, H. G. Marshall,Harmful Algae 1, 85 (2002).

7. J. Springer, S. E. Shumway, J. M. Burkholder, H. B.Glasgow, Mar. Ecol. Prog. Ser. 245, 1 (2003).

8. E. D. Levin et al., Neurotoxicol. Teratol. 25, 419 (2003).9. J. M. Burkholder et al., Environ. Health Perspect. 109,

667 (2001).10. R. W. Litaker et al., J. Phycol. 38, 442 (2002).11. J. M. Burkholder, H. B. Glasgow, J. Phycol. 38, 1261

(2002).12. J. Burkholder, presentation at 10th International

Conference on Harmful Algae,St.Petersburg,FL,Oct.2002.13. L. M. Grattan et al., Lancet 352, 532 (1998).

ResponseMY REPORT STATED THAT JOANN

Burkholder’s lab had declined to share itstoxic cultures with “critics.” The fact thatmore than 40 scientists have receivedPfiesteria material from Burkholder, butcertain other laboratories have not, wasdiscussed in a previous news story (NewsFocus, 11 Oct. 2002, p. 346). For example, arequest for toxic cultures from researchers atthe University of Maryland was turned downbecause Burkholder decided that the severalthousand dollars they offered was not suffi-cient. The VIMS team sent a written requestfor toxic cultures to Burkholder in August2002. Burkholder responded that she“cannot” supply cultures without alsoproviding “training to use them properly”;this, she later indicated, would cost $40,000.Burkholder instead suggested a collaborationand sent VIMS a possible research plan in late2002. According to VIMS scientists,Burkholder did not reply to their response, ane-mail sent 19 December 2002 that called theplan “an appropriate starting point” andsuggested next steps.

The “recent research” showing that anamoebae sequence matched the sequencefor P. piscicida zoospores was presented inOctober 2002, more than a year before themeeting on which I reported, and has notbeen published; Burkholder says thisculture was lost in a power outage. The factthat the Burkholder lab’s attempts to isolatepossible amoeboid Pfiesteira in 2003yielded only true amoebae species seemed

Pfiesteria feeding on fish epidermis.

Letters to the EditorLetters (~300 words) discuss material published

in Science in the previous 6 months or issues

of general interest. They can be submitted

through the Web (www.letter2science.org) or

by regular mail (1200 New York Ave., NW,

Washington, DC 20005, USA). Letters are not

acknowledged upon receipt, nor are authors

generally consulted before publication.

Whether published in full or in part, letters are

subject to editing for clarity and space.

LETTERS

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worth reporting to readers of Science. Manyaspects of Pfiesteria research continue to becontroversial in the field (1, 2).

JOCELYN KAISER

References1. Y. S. Shimizu, Curr. Opin. Microbiol. 6, 236 (2003).2. T. R. Miller, R. Belas, Res. Microbiol. 154, 85 (2003).

Individual Factors in

Suicide Terrorism

IT IS PERPLEXING THAT IN HIS OTHERWISE

compelling Review “Genesis of suicideterrorism” (7 March 2003, p. 1534), S. Atranfails to address the most conspicuous case inrecent memory: the suicidal raids ofSeptember 11, 2001. These events might haveprovided empirical data to corroborate orinvalidate his model. Perhaps because all ofthe direct perpetrators of the attacks perished,it may have seemed wise to avoid any refer-ence to them at all: The data would have beenindirect and anecdotic at best. Nonetheless,the same could be said of most of the exam-ples discussed in the Review: The scantyevidence that Atran presents comes frominterviews with families, acquaintances, andvarious recruiters of a handful of suicidebombers in the Middle East, or from pollssurveying the degree of support that suicidalterrorist acts receive in certain societies.

The paths to martyrdom are diverse. Theyrequire different abilities, talents, andtemperaments, and this also applies tosuicidal attacks. Rejecting individual factorson the basis of a “fundamental attributionerror” (the tendency to explain behavior interms of individual personality traits whensignificant situational factors in the largersociety are at work) can lead to another funda-mental miscalculation: neglecting traitsrobustly related to particular propensities ortemperamental styles. However obvious therelevance of institutional factors to Al Qaedaattacks, it does not obviate the need to analyzewhether the influence of peer pressure under aclosed organization fully explains the excep-tional behaviors under scrutiny. Emotion-driven loyalty in highly indoctrinated smallcells had to be uncompromising during the

preparation and execution of 9/11.Apparently, the model works. Nonetheless,the sheer elaborateness of the plan makesthese attacks very different from a low-costbus ride by a single youth carrying a home-made bomb under his (or, less commonly,her) belt, with the aim of detonating the arti-fact in a crowded marketplace. For the former,you need highly trained and reliable soldiers;for the latter, any indoctrinated believer willdo (hence the wide sociodemographic vari-ability in the studied samples).

Self-recruitment, for instance, is an indi-vidual factor that characterizes members ofviolent doctrinal groups, although it is not adistinctive feature among their members:fellow devotees, intermediate officers, andcommanders typically share this attribute,which may be connected to biological procliv-ities (1). But there are other constitutionallybased traits (dominance, proneness to risk-taking, fearlessness, aggressiveness, machi-avellianism, narcissism, and obedience) thatmay make a contribution to the different rolesplayed by self-recruited members, which inturn are crucial for the ties they establishwithin their microsocieties as well as thetactics they employ. To put it another way, canthe sole trait of “charisma” explain the excep-tional influence of unique leaders (2)? Somecharismatic leaders commonly succeed inpromoting highly prosocial and nondestruc-tive goals; others are able to push entiregroups of followers into mass suicide withoutinjuring anybody else outside the group; andstill others lead highly cohesive parties tochallenge political power using terror(suicidal or not).

We need to dissect profiles that may char-acterize the different temperamental stylesand goals of terrorism militants. Individual-oriented research seems essential in thisrespect. In addition to the aforementionedtraits, altruistic punishment (3), messianism(4), and religiosity (5, 6) are factors that mayplay important roles in the phenomenon ofsuicidal terrorism. Research efforts directedat disentangling the critical social vectors ofsuicidal terrorism are extremely important.They can, however, become even more valu-able if individuals are taken into account,rather than rejecting the perspective out ofhand just because there is an absence of clearlinks with psychopathology or the lack ofreliable differences between introverts andextroverts (7).

ADOLF TOBEÑA

Unit of Medical Psychology, Institute of

Neurosciences, Department of Psychiatry and

Forensic Medicine, Autonomous University of

Barcelona, Campus of Bellaterra, 08193 Barcelona,

Spain. E-mail: [email protected]

References

1. C. Tudge, New Scientist, 11 May 2002, p. 36.2. J. K. Galbraith, The Anatomy of Power (Houghton

Mifflin, Boston, 1983).3. E. Fher, S. Gächter, Nature 415, 137 (2002).4. A. Tobeña, Anatomia de la Agresividad Humana

(Galaxia Gutenberg, Barcelona, 2001).5. D. S. Wilson, Darwin’s Cathedral: Evolution, Religion

and the Nature of Society (Univ. of Chicago Press,Chicago, 2002).

6. J. Borg et al., Am. J. Psychiatry 160, 1965 (2003).7. A. Merari, paper presented at the Meeting “Mind,

Brain and Violence,” Queen Sophie Center for theStudy of Violence, Valencia, Spain, 7 to 8 Nov. 2002.

ResponseTOBEÑA RAISES TWO CONCERNS ABOUT MY

Review “Genesis of suicide terrorism”(GST): Data stem largely from interviewsand polls, and individual selection factorsmay contribute to understanding, predicting,and countering suicide terrorism.

Such data are almost all that exist,although new material confirms patterns inGST (1). Information from Palestiniannews services on 171 militants killedduring 2000 to 2003 (including 87 suicideattackers) reveals a majority of youngbachelors from multisibling families (bothparents living) having completedsecondary education (most Hamas suicidebombers were college-educated) (2).Terrorist incidents across the world (citedby U.S. Department of State) are unrelatedto per capita income, whereas denial ofcivil liberties (defined by Freedom House)is related (3). U.S. Army DefenseIntelligence (DIA) officials interrogatingSaudi-born Al Qaeda detainees atGuantánamo report that these militants areoften educated above reasonable employ-ment level; a surprising number have grad-uate degrees and come from high-statusfamilies. Motivation and commitment areevident in willingness to sacrifice materialand emotional comforts (families, jobs,physical security), to travel long distances,and to pay their own way (4). For Hamas,Al Qaeda, and allies, religious indoctrina-tion (of recruits who initially express onlymoderate religiosity) appears crucial tocreating intimate cells of fictive kin whosemembers commit to willingly die for oneanother. As with the 9/11 attackers (5), no“personality” defects seem evident.

No doubt, predisposing individualdifferences render some people more

We need to dissectprofiles that may

characterize the differenttemperamental styles and goals

of terrorism militants.Individual-oriented research

seems essential in this respect. ”

–TOBEÑA

Although both personaland contextual factors

affect action, studies ofindividual behavior in group

contexts show situation to bea much better predictor than

personality.”

–ATRAN

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susceptible to social factors that leadersuse to get people to die for their cause. Butindividual differences often singled out ascausally important—personal instability,hopelessness, and poverty (6)—are notdependable predictors (1). Tobeñaproposes additional personality traits aspossible factors (aggressiveness, narcis-sism, and obedience). But a U.S.Interagency report (used by the CIA)concludes: “there is no particular psycho-logical attribute… or any ‘personality’ thatis distinctive of terrorists” (7, p. 40).Months—sometimes years—of intenseindoctrination can lead to “blind obedi-ence” no matter who the individual, asindicated in studies of torturers (8).

Traits conceived as cross-situationaldispositions are somewhat circular inscientific reasoning. How do we knowsomeone is aggressive? Because the personattacks when provoked. Why does heattack? Because he is aggressive. Incontrast to personality traits, cognitiveattributions and appraisals (of how an indi-vidual construes the situation he findshimself in) may have explanatory value:One can present the same event and manip-ulate the attribution/appraisal of the eventto get different reactions.

Although both personal and contextualfactors affect action, studies of individualbehavior in group contexts show situationto be a much better predictor than person-ality (9). One situational factor, accordingto a U.S. Defense Science Board, is polit-ical context: “Historical data show a strongcorrelation between U.S. involvement ininternational situations and an increase interrorist attacks against the United States”[(10), p. 8]. In any event, we cannot domuch about personality traits, whetherbiologically influenced or not. We presum-ably can think of ways to make terroristgroups less attractive and to underminetheir effectiveness with recruits.

GST sought to encourage new researchinto what causes suicide terrorism so thatknowledge of causes could be used to stop thekilling and devastation. The final U.S.Interagency report on combating terrorismoverseas shows funding increasing 133% from2001 (apart from $165 billion voted for theIraq war, which was primarily billed asdepriving terrorists of weapons of massdestruction) (11). Incidence of suicideterrorism has not decreased. Despite detailedreview of actions related to tens of billionsspent by dozens of federal civilian and militaryagencies, there is scant mention of funding, orefforts to understand or prevent people frombecoming terrorists in the first place.

SCOTT ATRAN

CNRS–Institut Jean Nicod, 1 bis Avenue Lowendal,

75007 Paris, France, and Institute for Social

Research, University of Michigan, Ann Arbor, MI

48106–1248, USA. E-mail: [email protected]

References and Notes1. See supplementary online material available on

Science Online at www.sciencemag.org/cgi/content/full/304/5667/47/DC1.

2. B. Saleh, paper presented to the Graduate ResearchForum, Kansas State University, 4 April 2003.

3. A. Krueger, J. Maleková, Chron. Higher Educ., 6 June2003; available at http://chronicle.com/free/v49/i39/39b01001.htm.

4. S. Atran, N.Y. Times, 5 May 2003, p. A27.5. A. Karatnycky, National Review, 5 Nov. 2001; available

at www.freedomhouse.org/media/0501nr.htm.6. “September 11 one year later” (U.S. Department of

State, Washington, DC, September 2002), p. 14; avail-able at usinfo.state.gov/journals/itgic/0902/ijge/ijge0902.htm.

7. “The Sociology and Psychology of Terrorism” (FederalResearch Division, Library of Congress, Washington, DC,September 1999); released 14 December 2001;available atwww.loc.gov/rr/frd/pdf-files/Soc_Psych_of_ Terrorism.pdf.

8. M. Haritkos-Fatouros, J. Appl. Social Psychol. 18, 1107(1988).

9. L. Ross, R. Nisbett, The Person and the Situation(McGraw-Hill, New York, 1991).

10. “DoD Responses to Transnational Threats, Vol. 2: DSBForce Protection Panel Report to DSB,” December1997; available at www.acq.osd.mil/dsb/trans2.pdf.

11. “Combating terrorism: Interagency framework andagency programs to address the overseas threat” (U.S.General Accounting Office, Washington, DC, 23 May2003); available at www.gao.gov/highlights/d03165high.pdf.

12. Thanks to B. Saleh, T. Stewart, R. Nisbett, R. Gonzalez,R. Axelrod, N. Chomsky, G. Hammel, D. Medin, I.Pitchford, H. Gintis, and D. Sperber for arguments andsuggestions, and G. Origgi for organizing a CNRS-sponsored internet debate targeted on GST (availableat www.interdisciplines.org/terrorism).

“Fictive Kin” and Suicide

Terrorism

IN HIS REVIEW “GENESIS OF SUICIDE

terrorism” (7 March 2003, p. 1534), S. Atranwrites that institutional reinforcement ofevolved psychological dispositions may playa role in the training of suicide terrorists.These dispositions “may have emerged undernatural selection’s influence to refine or over-ride short-term rational calculations thatwould otherwise preclude achieving goalsagainst long odds.” In Atran’s view, commit-ment to apparently irrational behavior is asignal that convinces others of one’s sincerewillingness to act. Organizations that recruitand train suicide terrorists purposefullymanipulate dispositions to such commitmentin order to engender or reinforce a willingnessto engage in suicidal sacrifice. However, it isdifficult to see how individuals could beinduced to commit acts so personally costlythat they preclude the fitness benefits thatsignaling is presumably evolved to provide.Only if commitment to suicide occurs in thecontext of kin and psychological dispositionsrelated to kin-related altruism is successfulmanipulation plausible.

I have developed a model to explore therelationship between nonkin altruism and

institutional practices related to kin recog-nition. Its logic is straightforward: Kinrecognition is a necessary component ofinclusive fitness calculations related toaltruistic behavior in many species, and kinare often identified by means of evolvedcues that are open to manipulation (1, 2).As recognizing kin has been an importantproblem in hominid evolution (3), cognitiveadaptations to address that problem haveevolved (4, 5). Relevant literature suggeststhat cues most applicable to humanbehavior are close physical association(particularly during development), pheno-typic similarity, and the use of kin termsand other symbolic kin referents (6–8).Thus, institutions desiring to maintain andreinforce nonkin altruistic behavior amongtheir members should attempt to manipulatepredispositions associated with these cues (9,10). It is predicted that they will tend to“cloister” recruits with each other and theirtrainers, provide them with false phenotypicmatches such as uniforms and distinctive hair-styles, and encourage use of linguistic andother symbolic kin referents. Additionally,because youth and separation from kin areconditions likely to facilitate manipulation,institutions should prefer young, impression-able recruits and discourage their associationwith actual kin.

As suicide terrorism is an example ofdramatically self-sacrificial behavior oftenexhibited in institutional contexts, themodel should apply to this behavior aswell, and a preliminary review of availabledata suggests that it does. Atran describestwo of the five predicted practices: Suicideterrorists are typically young (early twen-ties), and they are recruited and trainedeven younger. Parental and sibling kinterms are often used among recruits,trainers, and leaders. In addition, recruitsare typically separated from kin andcommunity to train in secret, isolatedcamps where uniforms and other markersof phenotypic similarity are common. Forexample, among the “Children of theIman” in 1980s Iran, young boys and girlswere selected for martyrdom and sent toisolated camps for training. They “nolonger belong[ed] to their respective fami-lies,” were assigned uniforms and redheadbands, and were referred to as brothersand sisters, and children of the Ayatollah[(11), p. 91]. The same pattern can be seenamong recruits to Al Qaeda, where kinshipimagery is particularly pronounced: Osamabin Laden is known as the “elder brother,”and recruits are placed in “families” duringtraining and deployment (12).

It is no accident that suicide terroristsare often compared to monks (13) ormembers of religious cults (14), or that theorganizational structure of suicide terrorist

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camps mirrors that of military organiza-tions (15). Costly sacrifice in nonkincontexts is the key to understandingcommitment and behavior in all of theseinstitutions. And while what motivatesparticular individuals to commit suicideterrorism may be impossible to ascertain,how institutions maintain and reinforce awillingness to do so can be more clearlyunderstood. Atran is to be commended forhis exploration of this question in evolu-tionary psychological terms. One hopesthat work on kin-cue manipulative institu-tional practices will contribute to furtherunderstanding in this area.

HECTOR N. QIRKO

Department of Anthropology, University of

Tennessee, South Stadium Hall 250, Knoxville, TN

37996–0720, USA. E-mail: [email protected]

References1. R. Trivers, Social Evolution (Benjamin/Cummings,

Menlo Park, CA, 1985).2. D. Fletcher, C. Michener, Kin Recognition in Animals

(Wiley, New York, 1987).3. M. Daly, C. Salmon, M. Wilson, in Evolutionary Social

Psychology, J. Simpson, D. Kenrick, Eds. (Erlbaum,Mahwah, NJ, 1997), pp. 265–296.

4. L. Cosmides, J. Tooby, “Evolutionary psychology: Aprimer” (Center for Evolutionary Psychology,University of California, Santa Barbara, CA) (availableat www.psych.ucsb.edu/research/cep/primer.html).

5. D. Symons, Ethol. Sociobiol. 11, 427 (1990).6. P. Hepper, Kin Recognition (Cambridge Univ. Press,

Cambridge, 1991).7. P. Sherman, W. Holmes, in Experimental Behavioral

Ecology and Sociobiology, B. Holldobler, M. Lindauer,Eds. (Verlag, New York, 1985), pp. 437–460.

8. R. Alexander, Ethol. Sociobiol. 11, 241 (1990).9. G. Johnson, Pol. Life Sci. 4, 127 (1986).

10. S. Balch, J. Soc. Biol. Struct. 8, 313 (1985).11. A. Taheri, Holy Terror: Inside the World of Islamic

Terrorism (Adler & Adler, Bethesda, MD, 1987), p. 91.12. R. Gunaratna, Inside Al Qaeda: Global Network of

Terror (Columbia Univ. Press, New York, 2002), p. 96.13. J. Chivers, D. Rhode, N.Y. Times, 18 March 2002, p. A1.14. D. Long, The Anatomy of Terrorism (Free Press, New

York, 1990), p. 21.15. C. McCauley, in The Psychology of Terrorism, vol. 3, C.

Stout, Ed. (Praeger, Westport, CT, 2002), p. 13.

ResponseQIRKO ARGUES THAT SUICIDE TERRORISM’Sequation of sincere displays of willingness-to-die-rather-than-submit with actual actsof dying-to-kill enemies nullifies anyevolutionary benefits in such displays.Only by translating personal cost intocalculations of inclusive fitness (sacri-ficing for kin) can we understand suchbehavior. Martyr-sponsoring organizationsdo this by indoctrinating recruits into inti-mate cells of “fictive kin,” which triggers anaturally selected disposition for kinaltruism. Qirko elaborates on how this maybe done, suggesting that sexual abstinence,cloistering, and sharing of cult bodysymbols facilitate manipulation.

These practices, which are manipulatedto trigger naturally selected cues associatedwith kin selection, can indeed encouragefictive kinship, but are not sufficient or

necessary for terrorism. French foreignlegionnaires exhibit Qirko’s characteristics:Candidates are stripped of names andbelongings and, through the tutelary figureof Father Legion, a fictitious filiation isestablished and identity restored. Thisinvolves physical isolation from outsidersand close training with comrades; tattoos,stylized beards, and strict dress codes; andsongs, fetishes, and bonding ceremonies(1). In terrorist groups, sexual promiscuitycan also be a bonding factor, either withinthe group or toward others. Also, clois-tering and cultlike behaviors may be moreprevalent among ideologically driventerrorist organizations than grievance-driven ones (which are more thoroughlyenmeshed in the local community thatsustains them).

In Moslem lands, exploding youth popu-lations crash against rigidly authoritarianregimes in the competition for political andeconomic opportunity (2). These youthsand their families also see hope for escapeblocked by rapidly rising anti-immigrationsentiment elsewhere. Dwindling returns onfuture life prospects for individuals trans-late into increasing recruitment and promptreturns for terrorist organizations andleaders. To ensure returns, organizationalindoctrinators lead recruits through an esca-lating series of commitments and entice-ments, ranging from initial encouragementof petty crime (3), to lures of Paradise, tothe “living martyr’s” final testament whoseretraction would make life unbearablyhumiliating (4).

This issue, too, may gain from evolu-tionary psychology’s insights. The attemptto monopolize social and economicresources—most often by males, andperhaps rooted in evolved reproductivestrategies involving sexual competition—isarguably a factor in creating exploitativepolitical systems that are organized tobenefit those controlling resources (andpower) and reduce fitness in (and competi-tion from) those who do not (5). The morethat people who are dominated face risk inattempting to realize their hopes (6), themore they tend to become aggressive andtolerant of prospects for a shorter life (7).Indoctrination into martyrdom convertstolerance into desire, even necessity (8).

SCOTT ATRAN

CNRS–Institut Jean Nicod, 1 bis Avenue Lowendal,

75007 Paris, France, and Institute for Social

Research, University of Michigan, Ann Arbor, MI

48106–1248, USA. E-mail: [email protected]

References

1. R. Stopin, introduction to C. Fréger, Légionnaires(779/Le Château d’Eau, Paris, 2002).

2. G. Hammel, Demographic Appendix to DiscouragingTerrorism (National Academies Press,Washington, DC,2002) (available at http://books.nap.edu/books/0309085306/html/38.html#pagetop).

3. A. Silke, Terrorists, Victims, and Society (Wiley,Chichester, UK, 2003), p. 35.

4. A. Merari, Statement before Special Oversight Panelon Terrorism,“Terrorism and Threats to US Interests inthe Middle East” [HASC No. 106-59] (U.S. Congress,Washington, DC, 13 July 2000) (available athttp://tinyurl.com/g10v).

5. J. Sidanius, F. Pratto, Social Dominance (CambridgeUniv. Press, New York, 1999), p. 265.

6. One way the PLO managed to reduce terrroristactivity among members of Black September wassimply to marry them off (B. Hoffman, The Atlantic,December 2001; available at www.theatlantic.com/issues/2001/12/hoffman.htm).

7. J. Chisholm, Death, Hope and Sex (Cambridge Univ.Press, New York, 1999), p. 236: “Political planningshould give preference to reducing the security short-fall of those at the edge of a fitness cliff.”

8. According to Sulayman Abu Ghayth, Al Qaedaspokesman, “There are among the youth of thiscommunity (Islam) thousands desirous of death inthe same way as Americans are desirous of life… Jihadfor the sake of God now is a must for every Moslem”(Al-Jazeera Television, 9 Oct. 2001).

CORRECTIONS AND CLARIFICATIONS

News of the Week: “Gene suggests asthma drugsmay ease cardiovascular inflammation” by I.Wickelgren (13 Feb., p 941). The credit for theimage was incorrect. It should be “R. Spanbroek etal., PNAS 100 (3), 1238 (2003).”

TECHNICAL COMMENT ABSTRACTS

COMMENT ON “A Reservoir ofNitrate Beneath Desert Soils”

R. B. Jackson, S. T. Berthrong, C. W. Cook,

E. G. Jobbágy, R. L. McCulley

Walvoord et al. (Reports, 7 Nov. 2003, p. 1021)reported a large nitrate pool beneath desert soils (upto 104 kg N ha–1) and similarly shaped soil nitrate andchloride profiles. Analyzing 16 new desert cores, wefound nitrate values at least an order of magnitudelower (50 to 100 kg N ha–1) and no relationship tochloride profiles. The generality of the deep nitratepool is questioned.Full text at

www.sciencemag.org/cgi/content/full/304/5667/51b

RESPONSE TO COMMENT ON “AReservoir of Nitrate BeneathDesert Soils”

Michelle A. Walvoord, Fred M. Phillips,

David A. Stonestrom, R. Dave Evans,

Peter C. Hartsough, Brent D. Newman,

Robert G. Striegl

Desert subsoil nitrate inventories are spatially highlyvariable. Smaller inventories measured in theChihuahuan Desert (particularly in areas of recentdesertification as reported in the comment by Jacksonet al.) relative to those in the Sonoran and Mojavedeserts reported in our study confirm that subsoilnitrate retention in desert ecosystems is influenced byprecipitation patterns, vegetation type, and vegeta-tion history.Full text at

www.sciencemag.org/cgi/content/full/304/5667/51c

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