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Explorations in Complexity Thinking:Pre-Proceedings of the 3rd International Workshop on

Complexity and Philosophy

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11. Homeostasis, complexity, and the problem of biological designScott TurnerSUNYCollegeofEnv�ronmentalSc�ence&Forestry,US

Pre-Proceedings of the 3rd International Workshop on Complexity and PhilosophyStellenbosch, South Africa, 22nd-23rd February, 2007

The harmonious melding of structure and function – biological design – is a striking feature of complex living systems such as tissues, organs, organisms, or superorganismal assemblages like social insect colonies or ecosystems. How designed systems come into being remains a cen-tral problem in evolutionary biology: adaptation, for example, cannot be fully explained without understanding it. Currently, the prevailing explanation for biological design rests on essentially atomist doctrines such as Neodarwinism or self-organization. The Neodarwinist expla-nation for design, for example, posits that good design results from selection for “good design genes.” Along the same lines, self-organi-zation posits that complex systems with sophisticated structures and behaviors can arise from simple interactions among agents at lower levels of organization. There is no reason to doubt the validity of either explanation. Nevertheless, it is doubtful whether such doctrines by themselves can adequately explain the emergence of design in complex systems. In this paper, I argue that the missing piece of the puzzle that can draw forth well-functioning and well-designed “organisms” from the low-level interactions of the myriad agents in a complex system is homeostasis, a classical concept that is not itself inherent in atomist explanations for adaptation and design. I couch my argument in obser-vations on the emergence of a spectacular social insect “superorgan-ism”: the nest and mound of the macrotermitine termites.

IntroductionAmongb�olog�sts,“des�gn”referstoapecul�arcoherencebetweenal�v�ng

structureandafunct�on�tperforms(Turner,2007).Bones,forexample,areexqu�s�tely constructed cant�levers, bu�lt to bear the�r loads w�th an eleganteconomyofformandmater�als(Currey,1984).Itseemsperfectlyapttosaythatbonesarewell-des�gned:�ndeed,todescr�bethem�nanyotherwayseemspedant�c.Awkwardnessattachestotheword,though,because�tread�lycon-juresupthenot�onofades�gner,l�kethatwh�chPlato�ntroduced�nh�sTimae-us, thattroublesomeMasterCraftsmanthatwaslongthema�nstayofnaturaltheology,andthatservesthatpurposest�llfortheresurgent“naturalde�sm”that�mbuestheIntell�gentDes�gn(ID)movement.

Darw�n�sm conv�nc�ngly undercuts th�s type of th�nk�ng about b�olog�-caldes�gn,ofcourse,butthepers�stenceofant�-Darw�n�smnevertheless�n-v�tesaquest�on:whywon’t �tgoaway?Onedoesn’thavetobeasupporterofIntell�gentDes�gntheory(Iamnot),norneedonebeaversetoDarw�n�sm(Iamnot)toseethattherearesome�nterest�ngph�losoph�cal�ssuesatplay,andthattheserevolvearoundthequest�onofb�olog�caldes�gn:whyare l�v�ngth�ngssoaptlyconstructedfortheth�ngstheydo?Darw�n�sm,atleast�n�tsNeodarw�n�st concept�on, puts forth what �s essent�ally an atom�st solut�on

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tothequest�on:b�olog�caldes�gnar�sessolelyfromthe�nterplayof“atomsofhered�ty”�ngenepools,converg�ngovert�meontowell-funct�on�ngpheno-typesthroughnaturalselect�onofpart�cularphenotype-spec�fy�nggenes.As�nclass�calatom�sm,des�gnemphat�callydoesnotar�sefromevolut�onbe�ng�nformedbyanybroaderpurposefulnessord�rectedness(Dawk�ns,1986).

Avastterritoryofphysiologyseparatesgenesfromfitness,though.Eventhough much of th�s terr�tory �s terra incognita, what is known about �t ex-h�b�tsastr�k�ngpurposefulnessthatseemsqu�teatoddsw�ththesupposedlypurposelessprocessthatg�vesr�seto�t.Th�sputstheDarw�n�ststanceaga�nstpurpose�nto�tsproperperspect�ve,asmoreaph�losoph�calpos�t�onthananemp�r�callydemonstrableone.

Complexity,atleastasIunderstanditsscientificdefinition,iscutfromthesameatom�stclothasNeodarw�n�sm.Bothshareagoalofder�v�ngemergentphenomena–adaptat�on�ntheonecase,complexandcoord�natedfunct�on�ntheother–froms�mplerulesof�nteract�onamongmyr�adlow-levelagents.L�keclass�calatom�sm,however,Neodarw�n�sm(andperhapscomplex�ty)�spronetoaph�losoph�calquandary:�sthephenomenonweseektoexpla�nanemergentproductoftheagents,or�sthephenomenontheagents’dr�ver?

Iw�llsayattheoutsetthatIamnotapract�t�onerofcomplex�tysc�ence.Ihave,however,spentseveralyearsstudy�ngandth�nk�ngaboutagroupofsoc�al�nsectsthat�softenc�tedasoneofthemorecompell�ngexamplesofacomplexemergentsystem:thesoc�al�nsect“superorgan�sm.”Inmycontr�bu-t�ontoth�sworkshop,Iwouldl�ketotellyousomeofwhatwehavelearnedabouthowtheseattr�butesemergefromtheassemblageofagentsthatcom-pr�sethesesuperorgan�sms.Perhapstheseth�ngsw�llposesome�nterest�ngquest�onsforcomplexsystemssc�ence.

The Macrotermes superorganismIstudythecolonialphysiologyoftermites,specificallythosebelongingto

an advanced term�te fam�ly, the Macroterm�t�nae. Th�s group�ng compr�sesroughly350spec�es,d�str�butedamongfourteengenera(Table1).Allhave�ncommonthecult�vat�onofsymb�ot�cfung�asanadjuncttotheseterm�tes’nor-mal�ntest�nald�gest�onofcellulose(Batra&Batra,1979;Wood&Thomas,1989;vanderWesthu�zen&E�cker,1991).Twoofthegenera,Macrotermes and Odontotermes, are renowned for bu�ld�ng spectacular above-groundstructures(F�gure1).Istudyoneofthesespec�es,Macrotermes michaelseni, wh�ch�sw�delyd�str�butedthroughsub-SaharanAfr�cas.

Themound-bu�ld�nghab�t�snotun�quetotheMacroterm�t�nae,buttheuse to wh�ch these term�tes put the�r mounds �s. Most term�tes that bu�ldmoundsusethemasnests,that�s,asstructurestohousethecolony:themyr�-adster�leworkers,thequeenandthefert�lenymphsthatw�llserveult�matelyasthecolony’spropagules.Themacroterm�t�nemound�snotthenest,how-ever – few term�tes, save for occas�onal patroll�ng workers, are found there.Thenest�tself�sacompactsubterraneanstructurethat�ss�tuatedbelowthemound (F�gure 2), hous�ng both the colony’s complement of term�tes, andthecolony’scultureofobl�gatesymb�ot�cfung�,belong�ngtothebas�d�omy-cetegenus Termitomyces. Themound’s internalarchitecturedepartssignifi-cantly from the typ�cal arch�tecture of the term�te nest, wh�ch tends to the

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Genus # species Mound buildingAcanthotermes 1

Allodontotermes 5

Anc�strotermes 14

Eusca�otermes 1

Hypotermes 10

Macrotermes 54 *

Megaprotermes 1

M�crotermes 58

Odontotermes 187 *

Protermes 5

Pseudacanthotermes 6

Sphaerotermes 1

Synacanthotermes 3Table 1 Distribution of mound building among the Macrotermitinae.

Figure 1 A mound built by Macrotermes michaelseni, in northern Namibia. Two of my students are in the foreground: Wendy Park (l) and

Grace Shihepo (r).

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construct�onofhor�zontalgaller�es, �nterconnectedw�thsmalltunnels.TheMacrotermes mound,�ncontrast,�spermeatedw�thanextens�veandbroadlyconnectedret�culumoflarge-cal�bretunnelsthathaveastr�k�ngvert�calb�as(F�gure3).Theseram�fythroughthemound,�ntegrat�ngw�ththenestatthebottom, eventually to open to the surface through a number of t�ny egresschannels.

Theegresschannelsservetwofunct�ons.F�rst,theyarethepr�nc�pals�tesofmoundgrowth.Themound�sbu�ltbyanettranslocat�onofso�lbyterm�tesfrom the mound �nter�or and deep so�l hor�zons to the mound surface: theegresstunnelsprov�detheterm�tesaccesstothemoundsurface.Theegresstunnelsarealsozonesofporos�ty�nthemound’sseem�nglysol�dsurface,andth�sservesthemound’spr�nc�palfunct�onasanorganofcolon�alphys�ology:�t�saw�nd-dr�venlungtovent�latetheundergroundnest.Theneedfornestvent�lat�on�sacute.TheMacrotermes nest�safocusofh�ghmetabol�cpower,wh�chrequ�resacommensurablyh�ghcollect�vedemandforoxygen,roughlyequ�valenttothatofamammalthes�zeofagoat.Bysomeest�mates,thenest’smetabol�crate�sequ�valenttothatofacow.W�thoutvent�lat�on,thenest’s�nhab�tants would suffocate (Darl�ngton, et al., 1997). Remarkably, most ofthe nest’s collect�ve oxygen consumpt�on �s attr�butable not to the term�tesbuttothecult�vatedfung�. Becausethemoundprojectsupwardthroughthesurfaceboundarylayer,�t�nterceptsw�ndandconverts�tsk�net�cenergy�ntoacomplexfieldofpressureoverthemoundsurface(Turner,2000,2001).Viatheporousegresschannels,thispressurefielddrivesacomplicatedflowofairthroughthemound’s�nternalnetworkoftunnels,ult�matelyvent�lat�ngthenest.

Figure 2 A cross section through a nest of a colony of Macrotermes michaelseni. The light-colored bodies are the fungus combs, where the symbiotic fungus is cultivated.

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Th�s assoc�at�on of term�tes, fungal symb�onts and soph�st�cated moundarch�tectured�splaysaremarkable�ntegr�ty.Theterm�tescult�vatethefung�,prov�d�ng them an env�ronment that �s r�ch �n nutr�ents and sh�elded fromthe�r pr�nc�pal fungal compet�tors (Batra & Batra, 1967; Batra, 1971). Thefung�,forthe�rpart,serveessent�allyasanaccessoryd�gest�vesystemforthecolony, compost�ng the hard-to-d�gest woody mater�al brought back to thenest�ntoamoreeas�lyd�gest�bled�et.Themound,meanwh�le,�sconstructedasanaccessoryorganofphys�ologythatservestheresp�ratoryneedsofbothtermitesandfungi.Byanyconceivabledefinitionoftheword,thismakestheent�reassemblageasuperorgan�sm.Bymyunderstand�ngoftheword,�talsomakes�tacomplexsystem.Thequest�onIw�shtopose�swhether‘bottom-up’interactionsamongtheagentsofthissystemaresufficienttoexplainthisstr�k�ngorgan�smal�ntegr�ty?Iw�llargue�nth�spaperthattheycan,butonlyuptoapo�nt.Therema�nderoftheexplanat�on,Ishallsuggest,l�es�nacon-cept that �s largely lost �n the reduct�on�st and atom�st m�nd-set of much ofmodern b�ology, complex�ty sc�ence �ncluded. That concept �s homeostas�s,wh�chIbel�evehastoberegardedasessent�allyax�omat�cforanysc�encethatpresumestocomprehendl�v�ngsystems.

Homeostasis of structure and function in the Macrotermes superorganism

Homeostas�s�saw�delyabusedword.Usually,�susedtodescr�beageneral-�zedtendencytostead�nessofpart�cularpropert�esw�th�nl�v�ngsystems,l�kebodytemperature,bloodac�d�ty,andsoforth.Abuseofthewordusually�n-trudeswhentheword�semployedw�thoutreferencetothemechan�smsthatmustunderlieit.Onefinds,forexample,meresteadinessofbodytemperaturebe�ngdescr�bedastemperaturehomeostas�s:w�thoutanapprec�at�onofwhatproducesthestead�ness,onecannotd�st�ngu�shthetemperaturesof,say,the

Figure 3 Plaster filled casts of the internal network of tunnels in Macrotermes mounds. Left: the vertically oriented network surrounding the nest, which is sit-uated in the center. Middle: the large vertically-oriented tunnels in the center of a mound. Right: a partly exposed cast of tunnels situated just beneath the mound surface. Note the numerous egress tunnels projecting to the surface. Mound casts were done in collaboration with Dr Rupert Soar of Loughborough University.

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bodyanelephantfromthe�nter�orofalargerock.Homeostas�s,Iwouldargue,�sproperlyunderstoodasaregulateddynam�c

disequilibrium,sustainedbytheactivemanagementoffluxesofmatterandenergybetweenenv�ronments.Bodytemperatureregulat�onprov�desause-ful�llustrat�onofth�sconcept.Awarmbody�nacoldenv�ronmentrepresentsad�sequ�l�br�um�npotent�alenergybetweenenv�ronments–bodyandsur-round�ngs–thatcandr�veaphys�callossofheatfromthebody.Therateofloss�sproport�onatetothemagn�tudeofthed�sequ�l�br�um:hence,colderenv�-ronmentsel�c�tgreaterratesofheatlossfromthebodythandowarmerenv�-ronments.Th�sappl�estobothahotelephantandahotrock.Temperatureho-meostasiscanonlyoccur,however,�fthesephys�calheatlossesaresupplantedbytheexpend�tureofmetabol�cwork,�nth�s�nstance,d�rectedtothermogen-es�s.Furthermore,th�sthermogenes�smustproceedataratethat�smatchedtothephys�calheatlossrates.Thus,homeostas�s�sessent�allyaphenomenonoffluxes:physicalfluxesdownthermodynamicgradientsinpotentialenergybe-ingoffsetbymetabolicworktodrivefluxesofmatterandenergyagainstthesethermodynam�cgrad�ents.

ThisdefinitionofhomeostasiscanbereadilyappliedtotheMacrotermes superorgan�sm.Forexample,there�sasubstant�ald�sequ�l�br�um�nthecom-pos�t�on of the nest atmosphere w�th respect to the outs�de a�r: nest a�r �ssl�ghtly hypox�c, (nest pO2 �s roughly 2 kPa less than atmospher�c), sl�ghtlyhypercarb�c(nestpCO2�selevatedroughly2kPaaboveatmospher�c)andveryhum�d(Turner,2000,2001).Thed�sequ�l�br�um�npart�alpressures�sestab-l�shedbythenest’smetabol�cworkrate,wh�chIshallcall themetabolic de-mand.Thedisequilibriumalsodrivesaphysicalfluxofthesegasesacrosstheporousboundaryofthemoundsurface,wh�chIshallcalltheventilatory flux.Thecompos�t�onofthenestatmosphere�sthereforetheconsequenceofabal-ancebetweenthenest’smetabolicdemand,andthemound’sventilatoryflux.Homeostas�softhenestatmosphereoccurswhenthatmetabol�cdemand�smatchedwithventilatoryflux,whichappearstobethecase.Weknow,forex-ample,thatmounds�ze�sarel�able�nd�catorofthenest’smetabol�cdemand.Morepopulousnests(essent�allymoreeng�nesofso�l transport �ntheformofworkers)tendtobu�ldlargermounds,andmorepopulousnestshaveh�gh-eroverallmetabol�cdemands.Ifonemeasuresoxygenconcentrat�onw�th�nthenestsofthreedifferentsizeclassesofmounds,onefindsthatthenestpO2doesnotvary,desp�tethesubstant�alvar�at�onofmetabol�cdemandtheses�zeclassesrepresents(F�gure4).Thehomeostas�s�nth�s�nstance�sma�nta�nedbytheexpend�tureofworktomod�fythemound’scaptureofw�ndenergy.Morepopulous,andmoremetabol�callydemand�ngnestsbu�ldmoundsthatprojecth�gher�ntothesurfaceboundarylayerand�ntomorev�gorousw�nds,wh�chenablesthemoundtocapturemorew�ndenergyandeffectamorev�g-orousvent�lat�on.Moretothepo�nt,themound’sarch�tecture�sbe�ngadjust-edtoregulate thew�ndenergycaptured.

For�tspart,thestructurethatmed�atesnesthomeostas�s–themound–�t-selffitsthecriteriaforhomeostasisoutlinedabove.Themoundisastructureind�sequ�l�br�umw�threspecttograv�ty,ma�nta�nedbyabalancebetweentwofluxesofsoil.Ontheonehand,thereisaphysicalfluxofsoilfromthemoundontothegroundsurfacethatisdrivenbyerosionbywindorrain.Thisfluxof

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so�l�ssubstant�al,andcanamounttoseveralhundredk�logramsannually.Themound’sd�sequ�l�br�um�ssusta�nedbecausethesephys�callossesofso�lareoffset by term�tes work�ng to carry�ng so�l up �nto the mound, out throughthe egress channels, and depos�t�ng �t ult�mately to the mound surface. Themound’s arch�tecture �s therefore a dynam�c d�sequ�l�br�um ma�nta�ned bytwosoilfluxes,notsomuchastructureasaprocess,anembodimentoftwooppos�ngso�lmovements.

Assuch,themound’sarch�tecturecanberegulated,justasthenestatmo-sphere can be. Th�s can be shown dramat�cally by perform�ng a “completemoundectomy”onacolony,scrap�ngawaythemoundw�thafront-endload-er(F�gure5).Becauseth�sprocedureleavestheundergroundnest�ntact,theworkersareava�labletorebu�ldthemound,wh�chtheydo�nremarkablyshortorder.W�th�n90days,themound�srebu�ltto�tsshapepr�ortothemoundec-tomy,eventhepo�ntofbu�ld�ngasp�rethatpo�ntstothesun’saveragezen�th(F�gure5).Themound�srestoredto�tsfullfunct�onaswell,captur�ngw�ndtovent�latethenestandregulatethecompos�t�onof�tsatmosphere.

The mound’s arch�tectural regulat�on �s also ev�dent at a less dramat�cscale.Moundsoftenaresubjectto�njury,suchasabreach�ntheporoussur-facewroughtbyan�malsoreros�on.Th�s�njuryel�c�tsalarge-scalerebu�ld�ngprojecttorepa�rthebreachandrestorethemoundto�tsstructurepr�ortotheinjury.Theprojectproceeds in three stages (Figure6).Thefirst, or recruit-ment,stagebeg�nsw�th�nm�nutesofthebreach,and�nvolvesamob�l�zat�onofworkersfromthenest�ntothemound.Themob�l�zat�on�sel�c�tedbyd�s-turbanceofthenestatmosphere,wroughtbythesuddenadm�ss�onofturbu-lentw�ndenergy�ntothemoundenv�ronmentthroughthebreach.

Therecru�tmentphase�slastsforroughlyanhour,andmerges�ntothesec-ond,orstigmergic buildingphase.St�gmergy(l�terally,“dr�venbythemark”)�saself-organ�zedbu�ld�ngprocess(Stuart,1972).Aterm�telaysdownagra�nofso�lontoasurfaceandcements �t �ntoplacew�thasal�varyglueconta�n-�nganattract�vepheromone:thepheromone-ladengra�nofso�l�sthe“mark.”

Figure 4 Partial pressures of oxygen in the nests of three size classes of Macro-termes michaelseni. Despite the large variation of metabolic demand this size variation represents, the concentrations of oxygen in the nest are the same for the three size classes. After Turner (2000).

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Figure 5 Rebuilding of a mound following a complete moundectomy. Top: Mound prior to the moundectomy. Middle: The same mound (photographed from a different angle) following the moundectomy. Bottom: The rebuilt mound roughly five weeks later.

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Otherterm�tesareattractedtoth�smark,andaredr�vendepos�tnewgra�nsofso�lonto�t,eachnewgra�n,�n�tsturn,accompan�edbyanotherdollopoftheattract�vepheromone.Th�sproducesast�llmorepowerfulent�cementtootherterm�testodepos�ttheirgra�nsofso�lthere.Theoveralleffect�sanorga-n�zedtranslocat�onofso�ltoformlarge-scaleorderlystructures,e�therp�llarsorsheets�n�t�ally(Courto�s&Heymans,1991),merg�ngoverthelongertermintoacomplexspace-fillingarchitecturecalledaspongy build(F�gure7).

Follow�ngan�njury,st�gmerg�cbu�ld�ng�s�n�t�atedw�delythroughoutthemound(F�gure6).Th�s�sel�c�tedapparentlybystrongtrans�ents�ntheatmo-sphereofthebreachedmound,dr�venbyturbulentw�ndenergythathadpre-v�ouslybeenexcludedfromthemound�nter�or,butwh�charenowadm�ttedv�athebreach.Themost�ntensetrans�entsoccurnearthebreach,ofcourse,andtheseel�c�tthemost�ntensest�gmerg�cbu�ld�ngthere.Immed�atelyfol-lowing the injury, however, the transients are sufficiently intense through-outthemoundtoel�c�tfoc�ofst�gmerg�cbu�ld�ngnearlyeverywhere�nthemound.Thesubsequentcourseofthest�gmerg�cbu�ld�ngphase�sdeterm�nedbytherespect�veratesofso�lmovementsatthevar�ousfoc�.Therateofst�g-merg�cbu�ld�ng�smost�ntensenearthes�teof�njury,andthespongybu�ldtherewillbefilledinfasterthanspongybuildelsewhereinthemound,sealingthebreachbeforeanyofthedeepertunnels.Althoughth�sl�m�tsthew�nd-�n-ducedtrans�entsw�th�nthemound,st�gmerg�cbu�ld�ngcont�nuesforat�meeverywhere �n the mound, susta�ned �n�t�ally by the pheromone-med�atedpos�t�ve-feedbackprocessdr�v�ng�tunt�l�teventuallydecays,andst�gmerg�cbu�ld�ngceases,term�nat�ngthest�gmerg�cbu�ld�ngphase.

The st�gmerg�c bu�ld�ng phase leaves the mound w�th a sealed spongybu�ldatthes�teofthebreach,ands�tesofcomparat�velyopenbu�ldelsewhereinthemound.Thisinitiatesthefinalremodelingphase,wh�chplaysoutoverthespaceofseveralweeks,and�nvolvesrestructur�ngthes�tesofspongybu�ldthroughoutthemound,restor�ngthetunnelarch�tecturetowhat�twaspr�ortothebreach(F�gure6).Theremodel�ngphaseappearstobet�ed�ntoanotheraspectofnesthomeostas�s,�nth�s�nstance,thenest’swaterbalance.

Althoughterm�tesaregenerally�ntolerantofdrycond�t�ons,theMacroter-m�t�naearecapableof�nhab�t�nghab�tatsw�thannualra�nfallsasl�ttleas250mm(Deshmukh,1989).Term�teshaveth�scapab�l�tybecausetheyconstructames�cenv�ronmentw�th�nthenest(Turner,2006).Eventhoughth�ssavesterm�tesfromhav�ngtoadapttoar�dcond�t�ons,�tneverthelesscomesw�thacost,becausethemes�cnestenv�ronment�s�nd�sequ�l�br�umw�ththesur-round�ngs,wh�ch�ncludedrysurfaceso�lsanddrya�r.Th�sd�sequ�l�br�umcandrivesubstantialfluxesofwaterbetweenthenestandsurroundings.Asinallhomeostat�csystems,th�sd�sequ�l�br�um�ssusta�nedbyabalanceofphys�cal-ly-andbiologically-drivenwaterflowsthroughthenestandmound(Turner,2007,F�gure8).Dur�ngdryper�ods,theterm�tesworktooffsetphys�calwa-terlossesfromthenesttothedrysurround�ngsbyact�velybr�ng�ngwater�ntothenestv�atransport�nmo�stso�l.Th�s�snotacasualprocess:term�tesw�llgotogreatdepthstoobta�nth�swater,asdeepasahundredmetersorsobysomeanecdotalaccounts.Theyalsoact�velyreconstructtheso�lenv�ronmentforseveraltensofmetersaroundthenest,mod�fy�ngso�lporos�tyandsubsur-facecatchmentssothatsparsera�nfallscanbegathered�ntoshallowperched

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Figure 6 The three phases of mound recovery from injury.

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Figure 7 Stigmergic building and the spongy build. Left series: Stigmergic building that produces pillars. Right series: Stigmergic building that produces walls. Bottom: The space-filling spongy build.

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watertablesthattheterm�tescanread�lyaccess.Dur�ngwetcond�t�ons,suchasep�sodesof�ntensera�nfall,watercanpercolate�ntothenestfromthenowmo�stersurround�ngs,andterm�tesw�llworktooffsetth�saswell,byact�velytransport�ngwater�nmo�stso�lupoutofthenest,�ntothemound,andult�-matelytothemoundsurfacewhere�tcanevaporateaway(Turner,2007).Theend result �s an �mpress�ve regulat�on of nest mo�sture throughout the year(F�gure9).

Duringthedrywinter,moistureregulationisconfinedtothenest,whichbecomes a narrowly c�rcumscr�bed zone of homeostasis (F�gure 10). Themound,meanwh�le,�sallowedtodry.Dur�ngthespr�ng,aspreva�l�nghum�d-�tyr�ses,themoundgetswetterunt�l�tsmo�sturealsoappearstoberegulated.Th�s gradual mo�sten�ng results not from the mound be�ng wetted by ra�n-fall,butfromterm�testransport�ngwater-ladenso�lfromthenestup�ntothemound.Themoundmo�sten�ngalsorepresentsanexpans�onofthezoneofhomeostasis,whichhadbeenconfinedtothenestduringthedryseason,untiltheent�remoundbecomesazoneofhomeostas�s.Oncetheent�remound�sensconced�nth�szoneofhomeostas�s,so�ldepos�t�onontothemoundsur-facebeg�ns(F�gure11).

Remodel�ngoccursaspartofth�sexpand�ngzoneofhomeostas�s(Turner,2007).So�l�nadrymound�sessent�ally�mmob�le:term�tesavo�dthedryar-easofthemound,andthere�sl�ttlera�ntodr�veeros�on.Asthemoundmo�st-ens,theso�lw�th�nbecomesmob�le:eros�onratesk�ckup,andterm�tesarenolongerhes�tanttomoveaboutthemoreequablemound.Remodel�ngoccursaspartofageneraloutwardtranslocat�onofthenow-mob�lemoundso�ltothesurface.Howterm�teschoosewh�chso�lgra�nstop�ckupandmoveandwh�ch

Figure 8 Water balance of a Macrotermes superorganism. Solid arrows signify work-driven water transport by termites. Dashed arrows represent passive movements of water due to infiltration from wet soils and evaporation through the mound.

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toleave�nplace�sunclear,butprev�ouslydepos�tedspongybu�ldappearstobeone�mportantsource:term�tesareattent�vetoedges,thespongybu�ldpro-v�desanabundanceofedges,andth�sprobablyenhancestheprobab�l�tythatso�lgra�nstherew�llbep�ckedupandcarr�edtothesurface.Asaconsequence,the spongy bu�ld �s eventually demol�shed, restor�ng the smooth tunnel towhat�twasprev�ously.

Is self-organization enough?Icouldgoon,butIhopemypr�nc�palpo�nt�smade:th�ssystem�sthemost

�mpress�veexampleofasuperorgan�smofwh�chIamaware.Itexh�b�tscoor-d�nat�on,�ntegr�tyanddes�gn.It�salsoacomplexsystem,w�thself-organ�zedbehav�orsl�kest�gmergyplay�ngafoundat�onalrole�ntheemergenceofthesesuperorgan�smal tra�ts from the myr�ad �nteract�ng agents the system com-pr�ses(Bonabeau,et al.,1997).It�snowapttorev�s�tthequest�onIposed�nmyopeningcomments:isthisfoundationsufficienttoproducetheemergentsuperorgan�sm?

Myanswer�s“no”,andmyreason�ss�mple.Self-organ�zedbehav�orsl�kestigmergic building are not confined to theMacrotermitinae, but arewide-spread throughout the term�tes. Yet, �t �s only among the Macroterm�t�nae,

Figure 9 Moisture homeostasis in the nest of Macrotermes michaelseni. The moisture in the nest (blue trace) is maintained throughout the year, even as moisture in the adjacent soils (brown trace) dries considerably through the year. The center of the mound (green trace) is allowed to dry during the dry season, but becomes regulated during the rainy season. After Turner (2007).

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andfromonlyafewgeneraamongthem,thatthe�mpress�veMacrotermes su-perorgan�smar�ses.Thequest�onthereforebecomes:what,�fnotst�gmergy,drawsforthth�semergentsuperorgan�sm?Theanswer,Iargue,�ssometh�ngthat�snot�nherent�natom�stexplanat�onsfortheemergenceofsuchth�ngs:thephenomenonofhomeostas�s.

Term�tesareagentsofhomeostas�s,whosemodus operandi�stocreatenewenv�ronments upon wh�ch homeostas�s can be �mposed (Turner, 2007). Inthecaseofterm�tecolon�es,thatnewenv�ronment�sthenest�nter�or,createdbyexcavat�ngspaces�nso�lsthatarepart�t�onedfromthesurround�ngs,andregulated by constructed organs of phys�ology. Macrotermes are not un�queamongtheterm�tes�nbe�ngagentsofhomeostas�s.Theun�queMacrotermes

Figure 10 The expanding zone of moisture homeostasis in a Macrotermes michaelseni mound. As the rainy season proceeds, moisture throughout the mound comes to be regulated. After Turner (2007).

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superorgan�smemergeswhentheseterm�teagentsofhomeostas�sarecoupledtostrongphys�olog�caldr�versofmatterandenergy.Thesestrongdr�versare,ofcourse,thesymb�ot�cfung�.Th�s�saptlydemonstratedbytwophenomena,onethathasplayedoutovertheevolut�onoftheMacroterm�t�nae,andanotherthatplaysoutoverthel�feh�storyof�nd�v�dualMacrotermes colon�es.

The fungus-grow�ng hab�t among the Macroterm�t�nae probably got �tsstart asahyg�en�cmeasure. Fung�areusually ser�ous paras�tesonthe cellu-losefoodthatterm�tesbr�ngbacktothe�rcolon�es.Asaconsequence,term�tecolon�esoftenstorefood�nnumerouscachesthatareremotefromthecolony:�facachebecomes�nfected, �tcanbeabandonedand�solatedbothfromthecolonyandfromothercaches.Thesymb�os�sbetweenMacrotermesandTer-mitomyces probablybeganwhentheancestorsofTermitomyces proferredd�-gestivebenefitstothetermitesthatparasiticfungicouldnot.TheevolutionarytrendamongtheMacrotermitinaehasbeentogatherthese“beneficial”cachestogether,presumablytoprotectthemfrom�nfect�onbyparas�t�cfungalcom-pet�tors, culm�nat�ng �n the consol�dated fungus gardens that character�zeMacrotermesandOdontotermes.

Figure 11 The link between expanding zones of homeostasis and soil trans-port. Once the entire mound is enveloped in a zone of moisture homeostasis, soil deposition to the surface commences.

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W�thconsol�dat�onoffungalb�omass,however,hascomeconcentrat�onofmetabol�cdemand(express�ble�nun�tsofwatts),culm�nat�ng�nneststhatare character�zed by a h�gh metabol�c power density (express�ble �n un�ts ofwattspercub�cmeterofnest).Th�selevat�ngmetabol�cpowerdens�tyappearstobethepr�marydr�veroftheevolut�onofthemound-bu�ld�nghab�tamongthe Macroterm�t�nae (Turner, 2007). When food caches, and the metabol�cpowertheyembody,arew�delyd�spersed,there�sl�ttleev�denceoforgan�zedso�ltransport.W�th�ncreas�ngmetabol�cpowerdens�ty,however,comesthepowertoseverelyperturbthenestenv�ronment:dr�v�ngupnesttemperatures,nestcarbond�ox�deconcentrat�onsandlevelsofnestmo�sture.Whenthesefungal-dr�venperturbat�onsarecoupledtotheterm�teagentsofhomeostas�s,the well-des�gned mound �s the result. Locally h�gh carbon d�ox�de recru�tsterm�testotranslocateso�l.Locallyh�ghtemperatures�mpartbuoyantforcestothenesta�r thatd�rectth�sso�l transportupward.Locallyh�ghmo�sturespromotetheongo�ngupwardmovementofso�l,andasthemoundgrowsup-ward,�tbeg�nstoencounterthestrongw�nd-dr�ventrans�entsthatpromoteso�l translocat�on from the mound �nter�or to the surface, open�ng the largevert�cally-or�entedvo�dsw�th�nthemound.

Th�sprocesscanbeseen�nreverse�nthel�feh�storyof�nd�v�dualMacro-termes colon�es.Eventhoughacolony’sfungusgardensaretyp�callyconsol�-dated�ntoacompactnest,so-calledaccessoryfungusgardensoftenbecomeestabl�shedper�pheraltothema�nnest.Whytheseaccessoryfungusgardensar�se �s unknown. However they ar�se, though, an accessory fungus gardenrepresentsanewfocusofh�ghmetabol�cpowerdens�tythat�sper�pheraltothema�nnest.Remarkably,anaccessoryfungusgarden�nvar�ably�sassoc�atedw�tha“moundlet”,thebu�ltrepresentat�onofasmallfocusof�ntenseupwardtransportofso�l,dr�venbythesamestrongfungalperturbat�onsthatdr�vetheconstruct�onofthepr�nc�palmound.Andtheyhavethesameconsequence:construct�onofades�gned “organofphys�ology”tomeet themetabol�cde-mandsofth�snewfocusofmetabol�cpower.

Whence the superorganism? Allth�spo�nts,�nmyop�n�on,toaph�losoph�calconclus�onthatperhaps

somewillfindtroubling.Oneoflife’smoststrikingattributesisthetendencyofl�v�ngagentstoassemble�ntowhatwem�ghtcall“organ�sm-l�ke”ent�t�es:cells�ntot�ssues,t�ssues�ntoorgans,organs�ntoorgan�sms,ororgan�sms�ntosuperorgan�sms (Turner, 2000, 2006). Why should th�s be? Atom�st doc-tr�nes,l�keself-organ�zat�on,orNeodarw�n�sm,assertth�stendencyemerg-es spontaneously from s�mple agent-level �nteract�ons, w�th no overarch�nggoaltod�rect�t:no“skyhooks”asDan�elCDennetthascompell�nglyput�t(Dennett,1995).IntheemergenceoftheMacrotermes superorgan�sm,suchagent-levelprocessesclearlyoperate,buttheyaloneare�nadequatetoexpla�ntheemergentphenomenon.Whatdoesdrawforththesuperorgan�sm�s�tselfak�ndofa“skyhook”–large-scale,constructedenv�ronmentsthatarema�n-ta�nedbyagentsofhomeostas�s.

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