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Social environmental factors influencing mutual recognition of inviduals in the ant Leptothorax Lichtensteini bondr. (Hymenoptera: Formicidae)
_tourat Proc
35
. Elsevier'
SOCIAL DlVIROIDoWfrAL FACTORS UlFLo:mtCIJl6 MUTUAL IECOGJIITlOff OF [NVlDl1ALS ' [ff THE AlIT lEPTOTHOUr
liC/lT'ElfSTEINI BORDI.
CHYMEliOPTEIlA : FOIIM[CIDAE) I!.PROVOST
C.If.R.S. Equipe d'i'lllOLOGII!,31 CIl. J. AIguItr,
1~402
MarseiUe, France
. ( Ae~eptcd 13 October 1980 )
ABSTRACT
PROVOST, E., 1989 . Soda! envtronment8.1 factol'6 IDfluenctng mutual recoguJtloD 01
iDdIVidlJals In the Ant l.~P">t/wilEBdJfi'~ 8ondr. (Hymenop~r$ : Formlcidae). Behav. Precess . 18: 35.. 59
.
In tile lramework of a study of the mectlaDlsmS UIIderlyiDg mutual recogDition phenomena between members of a Upt«/JOliIE Jk.!JtM$IMD/ ant colony, we <»&(\uc~ two series.of eJptrI:Denis, designed to investlga~ tile ertecls of an er.perlinentalseparatlOn of indiVidUals (rom lIIeJr coiony upon beirIg retntrOduced. Two parameters were ezaniJnec:\ : the length of tile separation period and tile social expertence lJved I>y these individuals during tIlelr separation. Worlc&rs uvlng in t.oups of 5 individuals flO1ll ttle Same colony or in an allen cOlOIIY wIlere tIIey had been Preylously adop~ wm ~ected. oy tIIelr own Sisters WIleD. they were relntrOduoec:l Into tIIeJr colony, tfter a 70, 811'~ a ~5-day period Of separation respectivel)'. W. moreover Investigatoo tile offects on group cobeston of separatIDg oDe . COlony into ·two .lWves, depending 011 wIletller 01 not tile qlleen was present. Alter a 120-day separation, tile 2 limes or a colony did not merge rapidly and w1t11out aggressiVity, WIIess tile Single reprodUctive female was transferred from tile one nest to the otller every 15 dajs dllfing tile separatiOn pertOd.
In Ibe 1IgI1t 01 Ibe results obtained, we conclU
037~S1189I$Ol.!O
€> 19li91!1sev1er Science Publisher, av. (Biomcdi
36
INTRODVCTIOH The oohesion of the SOCial group, particUlarly among ants, Is
~y
based on a
process of mutual reoogoition among Its members, which impUes the ability to detect individuals not belonging to the group. By reoordlng aggressive behaviour between members 01 different colQDies, it is possible to ew!uate their p~rs ~I discrimination, e.g. Wl:Jetlter tIIel' belong to a species in Which Ibe oolonles are characteristically of the "c!ooed" type. • A great many studies ha'{e dealt with IntersJ)';cific agQoistic behaviour. Since the
end of the last cootury, several authQfS already hypothesized that there
~xists
a
distinct "oolony odor" : Forel (1&71), Mc Cook (1877), Lubbock (1883) (\Od then
Fi~iil~ (1901-1902-1903-1904-1905); IIlQre recently, particularly 9ln~ the devel~r.m~)1I.
61 SlXiobioiogical theory, Investigations have fOCUsed mi>re on the
study of recognition mechanisms betWeen nestmates, wIlether or not they were related. From these studies, it has beoome cJeer that the various strategies Involved In mutual recognition between indiVidUals bas not only evolved In IIl& different famiUes of
ooc1al Insects,
but
also in
the
dillerent speIOfiging to the same
family.
• It slloUld be noted Utat a correlation does not always exist between recognition and aggressive behaViour. One and the.same oolooy can. be ather tolerant Qf very aggressive IOwal'ds anolber, depending on Ute el!p(lrimental conditions : a l. jir.btenstPJrJi colony can accept Intrudm and thon become very aggressive towards the sisters of the same intruders, wilen the two oolQoies are confronted (Provost, 1980 a).
.
37
Some authorS have suggested that the oolony odor. 'mlght have environmental origins; others are In favour of a genetic 'explanatiorJ wIlereby the odOr Is producod by tile workers; according to an "lndlvlduallstlc" model or a "gesialt" model (Crozier and DIx, 1919, reler to dlscusslon) or perhaps the queen mlght be the principal source 01 the odor (carlin and Holldobler, 1963, 1966). In fact, the recognltion cues .
.
.
mlght be basod on both genetic and environmental ' factors (ref.. revues by H611dobler and Michener, 1980; Gadag1v.r, 1965; Hepper, 1986; Page, 1966). Another lIn~ of research led to an analysis of the emergence
~f
the recognition
IOOChanl= through early olfactory learning during ontogeny : recognition by a
at the SpeciES level was made by Howard et al. (1978),. Bloolqulst et al. (1979), wIlo Showed that certain cuticular hydrocarbons of termites could be uWlzed as speciHc recognition' Clles. Alter anslyzlng the hydrocarbons of several species of .termites, these authors drew up chromatographic profiles characteristic of the species. Howard et aI. (982) has confirmed that. In two species of termltes, cuticular hydrocarbons as reoogllition cues betwoon species. Along the same lines, Clement's behavioural analyses 0976, 196I,1962).llave shown that elllllllination of the eplcuticle by the olfactory organs of tormlte workers oontrlbuw,; rowilf<1S oolony recognition. Clement ..t aI. (1964,1965) havo Shown that thm exisis "a good oorrelation between Interoolonlal aggression an
substances serve as the termites' "cbemical signature", and
are used by the the workers to recognize each other.
38
FortIler progress was aelilewd witll ants In a study of disC:rtmlnation a
be~
by Bonavlta-C<»Jg01lf
responslble for tile chemical Signature In CBmj»JMtus V3fJW ants : !1Jls signature is characterized by the relative proportions of dlmetllyl-alcanes, and the olfactory Signal value, characteristic of &ach colony, was demonstrated by m&ans of the 1ures metllOd". Very little lnforn')ation Is avallable about the mutual roo>gnltlon process..'S at work between members of the same colony in ants of
I~pWthcras
genus. Stuart
(985) bas shown tile importance of genetic and environmental factors In nestmate
recognition in . three North-American facultatively polygynous and polydol\lOUS species of !1Jls genus. DurIng prevIous e:zperlments (PrOyost, 1979, 1960 b, ! 985), I anaI}'200 som~ of
the dedSive
m~hanisms
of colony closure at the intra-specifiC 1&V&1, In several
monogynous specie'l of tJlis genus, and Showed in partfcular that the degree 01 closure of a given colony differs depending on the.colony of orIgIn of the Individual Introduced or on the type of colony With WIllcll it is confronted. The aim of the
pr~t
study was
to
investigate some aspects of nestmate
r&eogllltion In a met1Jan1s genus : L n.::!Jtf>.J1si#oi.
On the basis of experiments in which individUals (living in groups of 5), were
reintrOduced .into a colony
after Varying periOds of "Isolation-, as weU as
exPeriments in which 2 colonies were OOIlfrwted, tile one having previously adopted several workers Of tile other one, and oolony 5plltting experiments In which a colony coUld be deprived of IIll queen, we proposOO oertatn hypolJles.
39
MATERIALS AND METHODS
l~l't(l/JJ(lmf IklItMStqJoJ colonles were coUected from the surroundlogs of AUauch. near Marseille. ThIs species occupies the slopes of damP 1II11S; 'wlth a northern exposure and they nest prlDclpaI1y In craCkS 10 the rockS and .betweenwall stones. These sm8J1 colonies WeJ~ easily collected 10 their totality. by asplrotlolflnto .a plastic tube. At the labOratory. the contents 01' the tube were poured IDto a tray (30 x 18 em). the bottom of WhIch was covered With plaster. WIIere the n~ was placed. The nest conSisted of a plaster slab (II x 9 em) that provided the necessal!y humidity and a glaSS plate·placed above the Slab. supported ·by two glass sUd~S placed on the two sliort Sides, that delimited a Ilelgllt of I to 2 centimeters, qUl!~ accuratelyrecreatlng the Daturatllabltat of these ants. The glass platecould !)$ pertorsted to obtaln an openlng. for the removal3lld Introduction of' ants; It was covered to create darluless. A glass plats;platod I; Oentbneters from tile nest contalnlng food (honty With Wlt sand added to avoid drownlog and cricket larvae less than · 2weekS old, wed by freezlng),.was permanently avallable and renewed twice a week. '!"he whOle set-up was brightly Ut and the ants lIllmedlately settled Into thenesl Fille crumbs of plaster were left for thelt use, iIn$of ~closure .consisting ' of minerai .and veget:ible ' materials, Is often · to '.be foUnd lutroundlDg tile colony..ThIs Is an eX(eUent example of adaptaUon to · 8 · new !uvltonment by reconstruttlOn of the orlglnatllabltal The partlallSOlatlon experlrDents Were carried outon adults: foragers Or queens. Individuals were removed with a brusll from the glass food plate, andgroujled by 5, . n a plaster nest of tile same type but ~er In size (4,5 x 3 em) placed In a tray il5 x I; em), the bottom of WIlicb was also Uned Willi plaster.Here,agaln, the~ts :>ecaIIIe ' active, a1thoUgli they were .Slower than the entlre .colony .' to .beglD . :onstruttlng an entlosur~ tIlat obStructkd tile two longer sides of tlieilesl . . . ' . They collected tile food plt.ced 5centimeters from their Ileal The periOd of partial solatloll varied from 15 to 120 days, Each experi1lient .Wi.tIl 3 given.period of SOlation.was carried out on .3 groups Of 5 workers from 3 different colonles, )'IIlere lIey were laterrelntroduu
40
recorded under a ~ular megnilier (enlargem~t : X 16), continuously for 30 minutes and foUowed for a \\Wi. Simultaneously, contrOl experlments were carried out They consiSted of removing tora@Jaglndivldualsand rGlDtroduc.lng dlem sevefaJ mlnut.."S alter marklog them to ·cbect< wIlelber tbls operation did nol cause any dlsbJrbance. The introduction of workers Into aD ·aUen colony was carrI«l"Out In Ule· same manner. First, 3 workers from colony 8, etter sucoesslve intrOductions, wtr e adopted by colony A. Secondly, after a period varying from 2 to 3 weekll (6 tests), .or a 45-day periOd (4 tests), coloDies A et 6 were placed In a Similar tray (42 x27l. on eacb stde of a removable wall. Confrontation between these colonies was carried out by removln{( the wall, after the ants bad Ilved for a time laps of one week In tbelr new environment All the memberS of both «)loDies were marked. The Interactions ·between tile allen workers and partiCUlarly, the behavIOur of the previOUSly adopted .workers, III the openrteld and sometimes inside the nests were obs.!rved Qurlng the next few bours, and then every day. Colony splltting was carried out to obtain two groups wbtcb were equal as regards t.be number and age of th~ workers and larvae. To thIS end; the C naU colOnies Wolfe .then seWed into identical nests to those dcs«lbed JIbove, placed during the entire separation pertod In trays (30 x 18 em) lined with plaster. The plaster fragments InteDt.ed tor the construction of tht endosure and tile food Ymt piaced at tllelr dlsw.aJ. The queen _ either removed (6 tests) or left In one of the balf «>loDits (~ tests with a 4)-(1ay separation period, 5 tests with a 120~y separation period). SIle coula alsO be .transferred from on9 balf colony into the ether (5 tests). The ~paration at that point. had lasted 4 monlllS, and ~ transfers were carried out every 15 days (8 transfers). The last transfer was efftctuat.ed 24 hOurs before tile remoV31 of iii. wdIJ, so that at t.Ilis mQ1llO!lt. no groop had been d~prlved of tile queen for 15 days. TIle two.nem were placed 15 oenllmeters from each eUler In trays (42 x 27cm). The foOd was dlstrtbuted be~the 2 nests to fadlltat.e eDcounters. The observations were made through a blnocut!lf magnlfh>r (x 16) and the interactions between SIsters from different nests, not only In Ule opentteld, but also insi~ the Dests wer~ . observed and recorded as before, for severn hours consecutJvety, then every day.
41
RESULTS
I Experiments relntroduclng workers aftm" variable periods of isolation a) Wbether IsolatlOIllasted a few minutes, a few lloorsor up to 15 days, the final
r$U\ts were always the same : all 01 the reintrOClucM workers were 'aoeepted by tboIr sisters. '!bls result applied to more tI1an two hundred reintroductions Into 70 colonles, after Isolatloo pocIods'of less
\JIan2~
hOurs,and the re!ntroductloo 015
;ororkers Into each of the 3 ooIOllies tested alter isolation periods 01 15 days. During the first few seconds following ~ reintroduction, a great numbei" of
individuals surroundfld tll~ worker, WIllCll was simply drummed lor a rew nlinutes. While the drumming tOn!lnUfld,seVeral workers then simulbmeoUSly Utked the Intruder over Its entire body, but partleularly on the mark. Only the .matk was bitten; no bii9s were ever observod on the appendages. During the flrst-24hours,
the worker could .rold Its appendages against Its body, wIliIe being ticked. It partlclpated In.tropllaJlattle ~~angos, playing ine role of donor". Afieiwar.is, the I!ck!ngs betam" less Irequent and it was r~~b~ only because of the m'll'k:' . '!be 5 qU<1roS reinlrodUCedinlo their ooIonyafte!:a 15-da1 isolation po::iod all acoopted, "Iso
after
wei'"
lite 2 prelilnlr!aty stag
at<:OlIIpanled by llct:Wg.
• 'Ibis behaviour tould be Interpreted as an appeasement behaviour as · has Imn suggested In ants by De vrooy and Pasmls (1976) in MJ'Ozicn robn, Bhai:kar (1979) In various specieS of .fo],o.nOpsis an~ In tile case of beeS by Rlbbands (1954),
Breed et.~. (1965) In ApjS111I"Jljfer.1.
42 b)
After an ioolaUon period QI ~5 days, 14 of Ule 15 relDtroduC@d workers In Ule 3
colonies were accepted, as were Ule 5 queens, by Uleir oolony. A ' s soon as Ule workers were reIDtegrated, Uloy were blttoo on Uleir appendages 'lor about
2~
hours. Progressively, tJlese bites llecame less frequent and UckIng became much more Irequent. Note tJlat Ulese bites. never caused a v Si ible wound. The worker let now a drop olliquld betweeD Its man
Two or the live lemales r. lntrOduC@d Into their ~Iony were takeo to the brood, by moans or their carrylDg method typical 01 MJ'(tnl~ a few minutes alter Uleir Insertion. The oUier U1r~ were bitten by severrJ WOrkers on their appendages and Ule petiole, lor I to 3 bO;Jm. ()n.;c agaln, a llckillg pbase lollowod the biting and Ule queens were transferred to the brood clu~. c)
After looger pertods oi Isolation (70 days-90 daYS-120 days;
15 tests were Oooducted work~rs
00
wltb every period,
3 ccloru~s), a very dlUereot result was obtalDed : Ule
wore blttoo immediately, violently and simultaneously by a large number
of IDdlVldUats (according to an -asterol workers trted to avOid contacts by fleeing aDd were pursued. Even Ulough the.nest was open, Only one escaped outside, by "forcing" Ule enclosure. The '/fOrbrs d:ed withID Ule first 2 days, after their arpendages were ampul;!.ted. Tbe 5 females relntroduC@d alter 120 days or Isolation were ali bitten vlolentty and klUed wiUlln a ( ewbours.
43
It. setIIlS (JOe! tIlat tIl~ longer
~
period of
~patatlon,
1M more dlffkult tile
readOption of Isolated individuals beeomes, WltII a t!lro..l\Old 91t:1ated tetween 45 and .70 days ollSolaUon. II
IlxDerlments confronting 2 colonies
rot
oj wIllcb
~ad pmiooOI!_~
workers 01 anotl~ Confrontation be~'n , 2 colOnies, tile one OODtalnlng 3 adUlt individuals originating Irom
tIl~
other colony !>rOUgIlt \.) UgIlt
dj(f~rellCes
In tile adopted
workers behaviOur, ' depending OIl the length or time spent In 1M allell colony and
the type 01 interaction manlfested between tile Workers of tile two groups, altllougtt it Is not)iosslble to say, for ttle moment, wtJether the 2 fattors 3.ct simUltaneously nor wlietller eltller one was preponderant. I\fter a period. of ~patation 01 2 to 3 weekS, and to the case of 3 colony pairs wIllctt merged, .tile 9·workers \'Me taken by tile adoptive workers, during a mass remo'la1, to tIl9lr original group, between tile 5th and 10th bour after the operung of tho Wall, After the same pertod O(S$patatlOll, In 3 olller pairs 01 colonies WIIiCIl had started flgbts Involvin& no deaths, anll wIllcb had not fll~, 7 of ~ 9, previously
adOpted workers returnee to their colony 30 hours altllr tile openlog of tile :Wall. During tile first enoo.uoters, we obserVed fleeing movements by . tIIolr sister
resident Wl)rkers aodtllen UCI:JDg and lropbaUactic ellCbaoges, (1M new amVals playing the role of dOnors). After a 45.ooy period of ~paratlon, In 4 pairs of colonies In wIllcb Wl)fkers hadstart.ed lights ending In.
44
other, or a "chain" typ9 01 lighting Where a previously. adopted .worker was bitten by one sister, and in turn bit another worker sister. III Experiments oonfr9ntJng 2 halves of We same colonv alter varying ~ ~
The following cases mre investigated : a) Il
The separation of the two groups lasted 120 days. With all 6 palrs of colonies tested, we noted the same interactions between sisters: on the fOCd only short bites, tllat left no wounds. LOIlg antennations
~l'e
often noted between workers of both groups.
[ndlviduals passed. from one nest to another. [n 2 out of 6 cases, alter many montl1s of contact, tIley all progressively reunited in the same nest
b) The queen was [eft in one of the two halves of the colony. Four tests with 45·day separation periods between 2 half colonies W&r-:> carried out. Whatever the strength of the groups (from 40 to lOa Workers),lbetr fUsion was observed to oceur between 30 and 40 !lours alter the ~nning of the experiment, during Which time we observed reciprocal visits that were non-aggressive. in 3 cases out of 4, the group with the queen moved to the ot'!er group's nest. [n one of these 3 cases, a small number of workers in the queen's group "carried off" the nymphs of the 'other group before moving. [n the 4th case, the fusion was reverSed. Five experiments "",re earrted out ( stze of the groups: oK> to [10 workers) with a 120-day separation period. During encounters numerous figbts occurred in the
45
oulslde area. It was very rare tIlat a worker penetrated Into tile nest of tile otller group : at tIlat point, tIley \'/We energetkaUy attaCked, bitten .and pulled oulslde. These attackS caused a few caoos of mortality. In any case, each group stayed In Its own nes~ even arter several montlls. c) The queen was alternatiVely transferred from
one nest to IIIe oilier.
In 4 out of tile.5 tests (sIz&ot COlonies: 65 to 135 worltors) WIler
15 days during tile.
'4 mOntllsof St>paraUon, fusion of tile two groups was obSerVed to o
35 to
40
hours alter llleremovaJ of tile partition beMen tile nests. Here &gain fusion' wis
prectede
experimeD~ tile
first week, witllout any massive moving. Note tbat in ·au tile queen's transfers, altor a 15~y period ?t separatioll, sh& was · readUy accepted by her ·dauglltors, WIIIcb immediately Ucked ber and carried
her to tile brood. CONCLUSION -1)1 SCIISSION Tb~
point to
results of tile above ellpeli!llenls earned out on tile L UdlfR.J1steJlZi ant tile follo'wIng conclusions:
, a worker, alter bellig separated from lis colony for 70 days, Is no longer
accepted by itS 51Stors on being reintroduced. - a WOrker, aft&!' a
45~ay
adoption period by an allen oolony of tile samo
spedeswiU fight lis own 'slstors and Is also attaCked by tIlem WIlen
tll~
Zcoloo'ies
ooo!roo.ted do not merge and WIlen fights t>eMe8 allen workers occur. - alter a 120~y separation petiQd, tile 2 halves of a colony will not fuse with aWessivlty, UDless tile queen Is transferred from the one nest to the other
(juring ttle periOd of separation. A On ttle basis of ttl_ data, b)'pOttleoos were formulated as to ttle me<:llanisms involved in ttle mutual re<:Ognltlon procwoos ootw*n ttle individuals In a oolon),. I The questionarloos as to why (I stoories of experiments) adult individuals isolated from ttleir oolon), for 70 days or more are killed by ttleir own sisters when ttley are reintroducod into ttleir colony. a) If we assume ttlat ttle odor OOIIIIllon to all ttle memoors of a tolony results from a continuous tzansfer of substanoes (by licking. food exchange or simple oontatt) between ttle group members (a
during ttle period of isolation in a small group. TIl!s liIodifitatlon, wlllth is signlfitant sinte it prevents ttlem Irom being re<:ognized when first reintlodutted, . may result from ttle fatt ttlat tile sma1I groups of live "isolated" individuals did not oontrlbute as much to ttle oommon odor as tile whole oolony did, Besides ttle odor of Utese small groups whlth had boon separated Irom ttle colony, andUtat of the stock COlony, whith was !Uuth more \X'pulous, presumably evolve and OOoome diversified, in ttl. oourse of .time, OOtause of ttleir different genetic variabillty.
Carlin and H6Udobier (1963), stuart (1965), Errard (1906), using ttle experimental model 01 Ute heterospectric miXed oolonles, have shown Ute eXistence of a transfer of odors linked to re<:ognltion ootween individuals of a miXed colony. Carlin ,and H6Udobier (1963) bave re<:orded an indiscriminate acceptance on Ute
part of workers originaling from stock oolonles to'A'aI'ds workers of various species of t~mp.motw raised togeUter in a mixed oolony. On ttleottler hand, Errard (1966), tarrying out groupings of ants of different genera Waoka roNda and
ForJ)Jj(~
47
s#y.'Ii), has no~ tIIat tile longer tile period of separation between 2 groups 01
different genera tIIat had previously formed a mixed colony, the more aggressiveness between workers In both groups was observed. LaStly, Stuart (1985), carrying out eltperiments on 2 North-American species of ll'pf(ltIJrJraE.' t. /QDf{.i..
at11b1ffl1l1~
noted tllat individuals from several mixed colonies
originating from tho same parental n(''Sts showed little aggresslvlty ·toWards each otller and tIIat the fusion betWeen mixed colonies Involved llWe aggressive behaviour. Lastly, Morel and Blum (1988) have demonstrated the eldsl/)nce of a tranSfer of recognition cues from the nurses to·the oallow workers In c"mfX'l1~tl1$ nl>iidaDUs. II) If it is true 'that each member of the colOO.yproduces Its
own odor, which Is
recogniZable by the other members, (the indIvidualistic model by Crozlerand IJix, (979), it might not be the chemical signature of tile workers isolated In wall groups that cbanges, but the worker sisters' -memory bank- (or template, see Shellmann and Gamboa, i962) , WhlCb changed during the period of separation. The.Wl)rkers may have -forgotten' the Individual signatures of their isolated sisters. Jrolatlon expvriments ,carried out With the primitive bee ~"'5$IIJ11 ii¥'.pliyJ7lJ11 showed tllat the longer a bee was kept away from its nest (I to·72 bours:
BeU,1974; I to 12 days: Kukuk et aI., 1977J, the more It aroused the aggresslvlty of the guardian on reaChing the entrance to its own nest The authors conclude
th~
memorizing of numerous
different signatures, is highly unlikely to ap!)ly to L D(:bto?Jl5f<9ioi tolonies which
48
can contain 200 to 300 Individuals, My own results are thercfor~ more in line Willi lIIe "gestalt" ~ mod~I, Note lIIat very iow aulllors have used the Indlvidua!lstic model to explain recognition processes. Mintzer and VinSon (! (35), have taken tills model
to be
lIIat WhIch best fits lIIelr results ,on Psou
One might object that In my eRperiments, the ants separated trom their colony and living in very small groups might have been unable to produce their individual characteristic odor, However, It should be mentioned that the behaviour of ' workers, Isolated In very small groups, remained completely normal : they bullt an en<:losure around the nest, conducted foraging, took care or their brood, and had trophallaCtic contacts,,, When kept aJone tor several months, a single ant also bullt an enclosure, collected food, raised the larvae, questioning Ibe largely aooepted idea that an isolated SOCial Insect cannot survive (Grasse, 195&),
• I do not find these'tlndingsvery conclusive, however. These authors repol'WO that individuals from 1b9 same nest are otten treated differently when inb'Oduced into another nest, WIlereas In a "gestalt" model, lIIe expected frequency of rejection is either Oil: or iOO~, TIle fact that they recorded Intermediary values might be attributable to the experimental conditions : eaCh test lasted only 5 minutes and every colony was subjected to 20 Introductioos. The authors did 1I()t spect!y Whelller or not llleir sucmsiv. tests mOdified lIIe frequency of rejection. IWotUd recall (Provost, 1985) that stabilized interactions be~n Intruders and r~lver colonies were recorded In L b'tbtM$tMll In 651 of the cases sbIdied. T!lls resUlt was obtained alter several hundreds of introductions but 'with only 3 tests per colony, and the stabWty observed was In relation to the final result Obtained after several days : ,adoption or klIl1ng. During the first few minutes. the in~racUons be~ colony and Intruder coUld be extremely variable among 3 intruders or the same origin intrOduced into the saroo colony,
c) It is worlll mentioning that. In our
~lIp6rll1l.nts,
tilt indiViduals rtlntrodu()ed
Into their ~olony alter a long separation were neve. aggressive towards the res\dllllt
workers. We =ot, hO'flver, deduee that the former had DQt lost their , group odor. In
fa~t.
slllee they were simUltaneously attacked byse'f&ral workers, It was
probably not possible Cor them to underto:e any aggressive a~on. Wilson (1975) has reported a ~ WIlere l ept<>tlJorudulnfiC1/$ workers were attacked by their L
curvJsp.iDosu.< , slaves WIlen
~
slaves'were relntrodu()ed Into their colony alter a
50day ISOlation period. 2 Although the seoond series 01 experiments Is still In tile preJlmlnary iIa~,
the resUlts Obtained so Car have sllOwn that a worker UVing In an ullen ~olony (or 8 period of 45 days wlU fight Its own sisters WIlen Ute 2 oolontes are oonCronted and' that It w11I also be attacked by them. It Is as If theauen group's odor Is acquired by an Intruder, aboUShlng or maSkIng lis own odor, It !Jl!ght attack its sisters alter
oomparlng the ~el1lical signature 01 Its OrIginal group W1t1l its own newly acq~ odor (USIng Ute "itlf matdllng" process destrlbed by Blaustein, 1963; Holmes and
Sherman, 1963; Hepper. 1966). An alternallve,tIplanation Illlght be that some kind of learning In the adult stage, 'oColtactMy conditiOning
~ured
(Thorpe '1936;
JaIsson, 1975). Tbls stOOnd hypothesis dOes not exelud~ a trinscerof the ~em!c3t signatures and'a,stIt matdllng prooess, but Dilgllt be a l4ecMn1Sm Occurs WIlen
anls are introdueed Into alien oolonies.
wlll~
always
Free (1956) haS reported stmUar Clndlngs on 'bumbll)"bei)$. ~J11b1'$8IIW1l111 workers havUtg spent I to 2 hours in another oolony were vigorously attacked
WIlen they wereremlroduood Into their'nest. Ukewise, with ,the L ZIlj)lJputDbre; BeU(l974)transferre.s individUals frODl one oolooy toanotller an!! Showe.t that tbe
10000er the UlDe SpeDt In an aullll nm, tile more dlffleint tile subSequent a40ptlon by thE> original CQlony members beoomes. ,One might wonder wily a worker wt.l~ll has been itparated from Its group for
so 70 days or more, was found to 00 pas3ive WIllie being attacked by Its Sisters (1st series of
e~riments),
Whereas here, it fought them activ..ly. To answer this
question, It would b& necessary to carry out individual refntroduction experiments on workers bavlng lived In alien colony. As a matter of fact, the lack of experlenoe In having contacts With an alien colony migbt b& one explanation for Individual passiveness. Remember that a worker that bas been Isolated lor 45 days is accepted by Its sisters when refntroducted, whereas a worker Integrated Into an alien group lor the same period Is attacked by its sisrus. This difference shows that the soctaI environment plays an Import?.llt part in recognition mecbanlsms. 3-a) Conlrontation between two halves 01 a COlony, both depriVed 01 the queen, WIlICb bad been separated lor a 4-month period, led to very little aggressivity among the workers. The merging of the 2 groups Dever involved intorindividUai
trall~portation
during a massive removal. When
th~
rounion 01
individuals in a single nest occurred, this was a progressive process taking several months, possibly owing to a lamiliarization pbenomena. The fact that the workers of both groups stayed in their own MSts, at least during the first few months, may be attributable to the fact that a
J.~pt0tbara3
colony instalied In a nest .lor a long period manifests a very little exploratory activity in unknown territory (stable colonies by Aron, 1984). Our experimental conditions, where individuals instalied in their nest for a 4-month. period, are suddenly presented With an unknown territory, are not lavorable to the merging 01 the 2 groups, sinoe this behaviour reqUires considerable exploratory activity. b) When the queen was lett in one 01 the 2 colony halves during the 4-month
51
separation period, .Ill& workers of .bolll groups aiso stayed in tIIW nest; 011 ·belng confronted,', but Mre, during ·encounters In ' the openf!&ld, Clgbts were reeor4ed which gave rise to som& mortalities, Tb& . pr_ of th& queen In only one of Ille 2
groups causes a dltfereoUaUoll betmeo Ill& recognitlon cues. Arter a sborter period of separauon (45 da)l$), tlle 2 half colonies merged : tb!s dUfc,oouation did nothav. Urne to becom& estai>USIled. c) The previous assymeUy was belanced out by ttaasterrtng
Ill~
queen,
alwnatlvely from one nest to another, during Ille separaUon phase, Herefu;iOD of Uto 2 grouJi.~ was recorded, WIthout any: aggressive behaviour, The'errectil of the queen's pre*lIoo were found to pectllin even thougb th& 2 groups ha4 OCCUPIed their nest for more thBll 4 mooths and the outside was unknoWn to Illem : Ille. ·quwo eCfect· preclOlnlnatAls over any group StabWty errect, as detloed.by Aron (1964). Numerous auttJ
mtchanlsms WIlereby Ille queen"ls
recognized by her workers, as weU as Ille attraction She ell9rtS on them, ID tile ~ or many soc!aJ Insects. For·el3lllple, for tile domestic~, the studies by, BoCIi and Morse 0974·1919-1962)an4 those by &reed 0961·1963). As WltII ants,WatJdns ' and Cole (966) for DoryUoes, Jouvenaz et ai, (963) 10 jl;I/Mopsis itlPicta, have Clearly sbown the workers are more strongly attraeted to tbelr motller than to queens of tile same spedes belooglDg ttJ dltferent colonies. TII~ aulllors suggest that Ille colony's SpedllC odor may superlmpClSf !tself on Ille queen's·pllO.romone,
which attracts her own offspring, In the same way, Glancey et'at 0961) ,and Lofgren et ai, (983) have shOwn the el1steoce or a pheromone, ariSiDg froiD Ille po!son sac (Vander Meer et aI., 1930), WIIlCh !s used for both 'attracUOD and recognition purposes by tlle S. itlpicfD queen, The fOUowtng data have beo.!Il recorded, on
many dUferent, extremely
polygynous speaes.
Laog~
(1960) bas shown .!IIlt !lie separation of a kIm",,,
f't'l)'dena colony Into two parts was not suffiCient to transform the 2 groups . into
aliens : even alter 4 montbs of separation, Ule foragers ta\(ffi out of Ibe 2.groups oX(hanged food among ea(b oUler wllb tne same frequen(f as wltb individuals of Ibeir original colony. But Ibe two groups were UWl.elUler ellperimentaUy deprived 01 a queen or contained r~vely I to 14 quceus. For F. JlJ8Ubfi!; CberlxtJlld Gris (1978) bave pointed out Ibat Ibe ground snow WbI(b Isolated Interconnecting nests from ea(h olber for several months brougbt on no aggresstvlty at spring time between wouers from Ule various nests. In the ant Iddomyrmex 1111JJ1iJi.~ alter a slx-monlb separation period, small groups of 10 workers \'/We a((epted by Uleir nestmates Without any aggr~vlty (Giraud, 1963). In NynoJc!lfuNa Brian (1986) bas deDIonstrated that 2 groups of newly born Sister workers, raIsed for a period of 3 weekS WlUl queens ~, Ibe !'aJIlespeetes but of dlf!~r~ntorlgins (t.b~ Istgrou? WlIb tb~
molber, tile ot.b~r With an alien qUNn, or bolb groups WIt.b an alien queen),
coUccted food togelber ,,;thout bOStiUty When Uler were oonlronted. Tbese results coinCide WlUl What Is known about polygynous colonies, wbere Ibe ctosure Is often not obVIoUS (lbe bypolbeSlS generally put forward Is that·Ibe large number of femaJes might give rlst to a. vast range of ooors, so that It Is possible for many alien individuals to become a((Opted) ; and When the colonies are closed, ibis does not seem to be due to Ibe females. Tbe role of Ule queen In the ctosure of t.be group and in the mutual rtCOgDitiOll. prooasses between wouers of monogynous speetes was eluCidated by Holldobler (1962), Who pointed out Ulat If Ibe only female was removed from a CWf't'O
from their colony of origin, Iben these worker groups Without the femaJe became In-dillerent towardS worters 01 an alien COlony 01 the same spectes. Along the same U'oes, I have $bOwD (J>rovost, 1960 b) Ulat 2 CWf'l'l1"tus /afRJ8/Js colonies cannot
S3
fuse unless on~ of them Is ellptflmentaUy deprived of Its queen. HoUdobler and Wilson (977), HoUdobier and ",,~el1er (960) bave remarked tIlat U tile odors bave a partly genetic origill,lt Is easily con(&ivable that In monogynous species, Whose coloDies are usually close
important role in ttle production of the OdOr! because the genetic Variability or the workers will Increase tM diversity of odors to ".Cb a <»D1ustng level ,that reoegDition of l1estmal:$s W11I D.O longer be possible. TlIlsldea, I WOUld add; Is not appUcable to cases WIIere a ctJllUDOO odor Is tIlought to eXlst, ':onslstJllg ot a combination of individual odors. It is dllffcUlt to say for the moment WIIat mecbaJllsm brings Into p1&y tile "queen erfect". Does tile queen bave a privileged
ro~
in the 0010111'S odor
production? Car1ln and H611dobler (1963) bave demonstraWd the existence, among various species of C8mp.)fJ(I/Q$, of "diScrimfDators" linked to tile queen'& presence,
Wbicti are uWiZed during the recogDiUon promses, and are suttldentty £trongfor
the workers of tile orlgiDa1 colony not to be able to r~ s1SW!lI ralsedby a hel:$rosped1lc queen. In these autllors~ 'opiDlon, the substances produced by the queen. oonstitute the prlndpa1 mecbaDiSlll, predominating .over auy "gestalt" etlect (CarUo an.d H6Udobler, 1966). AMl:ber bypot1>.ests mlgbt be enVisaged : the female, by her prosenco, mtgbt SUmUiabi tile prodUction by tile WWkers of subStances intervening in tile recogDiUon processes. B
III OOI1c1uston, in L
1kJ1~
ants, tile COlony odor used '(or recognition
purposes among Its members mlgbt be based on several coexiSting systems : "an odor may be produced by eacb individual of the group. ThIs IndlvlclllGl odor dependS 011 a genetIC compound (Provost and Brun
1986 aDd
in preparation). i11IB !laS been demonstraWd With L .zt!JibJ'FUl11 (Greenberg. 1979), ApiS
m.¥lil«a (Br*
1':!IeIJdMJ)'J7J1eZ fenuSiJiM
54
(!(.tntzer illiG Vinson (1965); • our ~xperiments suggest the
~Xistence
of a colony odor common to all Its
memwrs, which results from the trllllsfer of individual odors, as described by the "gestalt" model; • the odor might partly derive fNm the physical envlronment (the nest for ~xample). Tills point Is
not tr~ated here;
• the queen plays a privileged role in the
closur~ meclla!:.~
of the SOCIal
group, as shown by the data recorded in this study. carlin and HoUdobler (196&) have proposed that the various types of
ch~pical
signatures of wopoJ1<")iu$ ants may W organlzed in a' llIerarchy : discrimlnators furnished by Ute queen, discriminators produced by the workers, auct· acqulred ,~vlronmental
odors. Although the pres~ilt"experlments show the role o~ l~0 queen's
presence, It must however be underlined that colorJes experimentally deprived of the queen are not systematically open and that a queen separated from her workers ior a period·of 70 days is no longer recognized as such and Is attacked In the same manner as a worker subjected to the same separation. It Is therefore not possible, at tills stage to conclude wnether any such hierarchy of recognition cues eXists in 1.. J.WJf&J$t.e.iJ.!i.
O!-,\lOsIte results were recorded by Kalmus and Ribbands (1952) . they demonMrated that in honey Wes the workers were preferentially attracted to the dish ~isited by melllbers of thelr own colony. This preferential attraction was shown to be based on the distinguishable odors emitted by the workers. The presence of th~
queen was unnecessary for the maintenan.:e of the preferential .attractiOil.
Similarly, MIntzer (1962), Stuart (1965,
1967) have dQlllOPstrated the
non-preponderance of queen' related factors in recognition processes. Mintzer has reported tb.at in P. t«rucioiii1, 2 worker groups ralsed from the larval
st:o~e
bl
55
different qUe
dori~ ~ receiver coioDtes did notlntluenl» !be, aCl»jltance of
Intiudlng individuals, regardless of WIletber or not tbey were of the same 'Sp.ci~. ,"
,"
-"
.
.
Lastly, Stuart (t 967) bas demonStiated In l. ron'/sp/MsV$, a faCUltatively pclygynous sp&CIes, that individual wOrken produce tOlony-speclUc r~oitlon cues alter ' eclOSlon, regardltsS of !be
number of que
In
queenless colonies. Tbls gives us some idea of tile diVersity of 1M recognitiOD systhms lIlat various sp&CI~ of
ants have developed In !be course of EvolUtion.
Aron, S. 1964. ROft du marqua~du lIml~lre et de la competition iIltiaSptculqu~ daIls fa dynaailque du recrutement ~enialr& Chez ltyWfJJNuiJlJlla5dawt< MemOlre, de ~nce. Un/venlie L1bre de BruHtUes., 97 pp.' , " IltU, W.j.,1974. ' Recognition . of .resident and' non-resident Individuals In Intraspeci!lc lIe$l defense of primitively eusocial ballctlne bet, ). Compo Pbyslol.. 9!d95,-202. ' ' , BbatJru,AP., 1979. ,Troph6nactlc appmement In ants from distant ColoDfes Folla/Entomol. MelL, 41 : 135-14'3. BlaUstAln, AR.; i 963. 'KIn reeogiutloll mechanisms: phenotype or r~tlOD aIIeles7 ,AmerJlat; 121:749-754. BlomqUist, G.).. Howard R.W., McDllllel, C,.A" 1979. Structures of ,tIlecuticutar bydrocarbons of !be teimlte io<>tNmopsi$ et:tUstkIN1Is (I!a~). Insect Blocb~m.
9: 365-370.
'
"
BoCh, R., Morse, R.A. 1974, Discrimination of faDlWar and fortfgDqueens l>ybOriey bee swam',:l. AmI. Entomol. SOc. Am., 67 : 709-711. ' BoCh, Ro' c.I¢'i5e, lA" 1979. Individual recongltlon of queens by boney bee swarms. Ann. f,ntoinol. SOc. Am., 12.: 51-53. ' , BOcb, R" Morse, B. 1982. Genetic factor iii queen recognition odors of boney bees. Ann. Entom?L SOc. Am., 75 : 65+656. , " , Bonavlta.l1{'llJs P3&1J$ seep. ).EntomOI. ScI.,22: 1-10. '
56
Breed, MD., 1981. Indlvldual t~tloo an~ leam!ng of qllooo ~ors by WIlrker honey bees. Proc. Natl. Acad. ScI. USA., 78 : 2635-2637. Breed, MD., 1963. Nestmate recognltlon!n boney bees. Anim. Behav., 31 : 86-91. Breed, MD., Butler, L., stiller, TM., 1965. Kin reoognltlon by WIltiter boney bees!rl genetically mIXed grOUp6. Prce.Nat!. Acad. ScI. ,U.s.A, 82 : 3058-30&\. Brian, M.V., 1966. Boodlog between WIltkers and queens In the ant genus Myimf<2 Anim. Bebav., 34: 1135-1145· Buckle, G.R., Greenberg,t., 1981. Nestmate recognition in S't.oeat boos (JasAW/(ISS11Dl lNp1J,rum) : does an Individual recognize its own ~our or Only odours of its nestmates? AnIm.Behav., 29: 802-809. carlin, NP., HoHdobler, B. 1963. Nestmate Iltld /tin recognition in lnterspeclf1c mixed colonies of ants. Science, 222 : 1027-1029. carlin, NP., HoUdobler, B., 1966. The !dn recongltlon system of Carpenter 'ants (CaIlJpoI1o/lls spp) i : iIIerarchlcal cues !n small colOnIes. Bebav. Ecol. SoCioblol., 19: 123-1~4. Cherllr, D., Grls, G., 1976. Relations at agreS$ivi1:e chez i' gen~tlc models lor tbe Innate components of colony ~ in social hymenotera. Behav. Ecol. SOOobiol., 4 : 217-224. ~ Vroey, C., Pasteels, ).M., 1978. AgOniStiC behaviour of MynJ1ic9 roNa 1. Insect.es SoCiaux. 25 : 247-265. Krrard. c., 19M. Influence des stlmulaUons SOCiaies precoces sur l'lli.:egtatlon soda!e de l'aduJte de CflJ11pono/lJs- lI1JdaminaJi$ (Hymenoprere, FOrmiCida:--). Coll. Inoom. Ethol., Bull. Inter_SP.E.CA., ~elone, 71-81. Errard, C., 1966. Role of early experience in mlXed-colony odor recognition in tile ants Manka robida and FimI11(a Mlys1 Ethology, 72 : 243-249. Fielde, A.M., 1901. Further study of an ant Pro<:. Acad. Nat ScI., Philadelphia. 54 : 521-544
57
FI~ld~; AM., 1902. Notes on an ant. Pro<:. Atad. Stl., PblladOlpbla, 54 : 599-625. Flelde, AM., 1903. Artlfltlal mlled nests ~f ants. BioI. Bull., 5 : 320-325. FI~ld~, AM., 1904. PoWer of recognition IllIlOIlg ants. BioI. SuII., 7 : 227-250 . FlelD1}'I111e3 hlU1JlJir; (Hymenoptera, DoIlChodtriDat) et,reCherChe de moyens de lulie. Volv. R. Descartes . PubUcations ~nUilqUts nooelerees. 3. Glan~i, 8.M., G!()V~, A., Lofgren, C.S., 1961. Pheromone production by virgin queens ot SoletJop5i>ioTlJdaDUIefJ.. Sotloblology, 6 : 119-127. Grasse, PP., 1953. L'eftet de groupe sur I'anlmal ot sur I'holllllle. I. PsyCh. Norm. Path. 129-146. Greenbefg.L. 1979. Genetic component oj bee odor in kin r~nltion. Selence, 206. 1095-1097. . Hare, 11., Alloway, TM., 1967: Early ltarnlllg and ~!'JOd dlscrimlDation ' in leptotlloracine ants OIymenoptera : Fonnlddae). Anlm. 8thav., 35 : 1720-.1724: Hepper, P.G. 1966." KIn reoognition : functions and ' mtcllanls!lls : areview. BioI. Rov.; 61 : 63-93. . ii6Udobler, B., 1962. Zur frage der oUgogynle bel CdoJp.'I/J(>flJ.<'IgJJl/Wda Late. und OUPJW1(Ito.<1JHC".dntJlIS L. (\lyra. FormICldae). Z. angew. £111;,, 49 :337-352. HoUdobl~r, D.; WUson, E.O., 1977: lbe number 01 queens : an mlportant trait in ant evolution. NaturwtSieoscbafteo, 64 : 6-15. Hori~obler, B. MiChener, CD., 1980.. MeChanisms of IdenUilcatlon and . dlscrlullnation in social Hymenoptera. In : H. Marl
58
cocons chez la jeune (ourm! rousse (FMJ1k8 t»/ymIP8 Forst). Bebavlour, 52 : 1-37. Jouvenaz, DP.,l3anks, WA., Lofgren, C.S., 1974. Fire ants : attraction of workers to queen (le(retiollS. Ann. Entomol. Soc. Am., 67 : 442-444. Kalmus, II., R1bbands, C.R., 1952. The origin of odours by WIlich llOoeyt>ees dlstlnguish their companions. Proc. Roy. Soc. (6), 140 : 50-59. Kuklllt, PP., Breed,·M.D., $obti, A., BeU, W., 1977. The contributions of klPship and conditioning to nest recognition In a· primitively eusoclal bee, l8$i~"UII1 .ll'pbf.TllOl (Hymenoptera : I/allcUdae). Behav. Ecol. SOC(oblot., 2 :319-327. Lange, V.R., 1960. Uber die fu~t.ergube ZWiSchen AJlgeMngen verschledeoer waldamelsoo. Z. Tterpsycbol., 17: 3&9-401. Le Moll, Y., PasseW, M., 1977. Til. effect of early learDing on recognition acceptance and.care of cocoons In the ant FarI11k8 nUa L. AU! Soc. Ita!. $(i. nat, MIlano, 116 49-64. Le Moll, F., Mon, A., 1962. Early teaming and oocoon nursing behaviour tn the red wood-ant Formka Jucu!Jris ZetJ. (Hymenoptera : FormIClda.). Boll. 2001., 49 : 93-97. Le MoH, F., Mort, A., 1964. The effect of early expeMnce on tile development of -aggreSSive- behaVIOur In FarmA..., JucubrisZett. (Hymenoptera: FormlddM). Z. Tlerpsycl10l., 65: 241-249. Lofgren, C.s., Glancey, 8M., Glover, A., Rocca, J.. TumbllsoD, J.1963. Behavtor of workers of ScJ~ iovicta to tM queen recognition pIleromooo: labOratory studies with an olfactometer aod surrogate queellS. Ann. Entomol. Soc. Am., 76 : 44-50. Lubbock, J., 1663. Ants, bees, and wasps : a ro<;ord of observations on the habits of the social Hymenoptera. Appleton, New York, 448 pp. Me COOk, .a.c., 1677. Mound-making ants of the Alleghenies. Trans. Am. Entomo1. SO('. 6 : 253-296. . Mlnl63r, A, 1982. Nestrnate recognition and incompatibility between colonles of the acaCIa-ant P$\tUdlW}'mti9..1·/"rr~. Behav. Ecol. SoCIobiol., 1(): 165-166. Mintzer, A., Vinson, S.8., 1965. KinShip and IncompatibiUty between colonies of the acaCia- ant P$\tud!wyrlmJi/imrcitM!. Behav. Eoot. SoCiobiol. 17: '15-76. Morel. L., .1982. Mise en place des processus de regut&t.ion du oomportE>ment agresslf et de la reconnaissance entre ouvneres d'Une soCl~te de CMlf»11Otul' "Bglis S (Hymenoptera: Fonniddae). COU. Inter. Sect. Fr. U.I.£.I.S. Jl·.u:celon&, pp. 127-136. Morel, L., 1903. Relation entre oomportement agresslf et privation soCiaie precoce Chez les jeunes immatures de la fourmJ c.wp.?/J(Jfo.' I'3$U$ Stop. CR, Acad. $(i. 296 : 4~H52.
Morel, L, 1986. Ontogenese de la reconnaissance des membres de Ia societe cI1ez la (ourm! CMlp.?Oo>tusHoridanus: Bull. Inter. S.F.E ..U, Mrker an!: : are sisters ~r neslmates recognized 1 AnIm. Bellav. 36, 710-125.
59
Page, Rli., 1966. KIn rerognltlon In socIa1lnsects·: an Informal overview. C.R. loth Int.e-rn. Congr. l.U.S.s.l., MilnIch, Workshop: kin recognition in socIa1lnoocts. Provos~ E., 1979. Etude de la fermature de la societe de fourmis chez dlverses espeCe5 de It'pt(!thMlEet chez C3mJlO11'.,ws/at<,.raJ/s(Hymenoptera, Formtctdae). C.R.Acad. ScI. Paris, 226 : 429-432. Prov~ E., 1960 a. La fermeture des socIet!fs de J..opt
35
. Elsevier'
SOCIAL DlVIROIDoWfrAL FACTORS UlFLo:mtCIJl6 MUTUAL IECOGJIITlOff OF [NVlDl1ALS ' [ff THE AlIT lEPTOTHOUr
liC/lT'ElfSTEINI BORDI.
CHYMEliOPTEIlA : FOIIM[CIDAE) I!.PROVOST
C.If.R.S. Equipe d'i'lllOLOGII!,31 CIl. J. AIguItr,
1~402
MarseiUe, France
. ( Ae~eptcd 13 October 1980 )
ABSTRACT
PROVOST, E., 1989 . Soda! envtronment8.1 factol'6 IDfluenctng mutual recoguJtloD 01
iDdIVidlJals In the Ant l.~P">t/wilEBdJfi'~ 8ondr. (Hymenop~r$ : Formlcidae). Behav. Precess . 18: 35.. 59
.
In tile lramework of a study of the mectlaDlsmS UIIderlyiDg mutual recogDition phenomena between members of a Upt«/JOliIE Jk.!JtM$IMD/ ant colony, we <»&(\uc~ two series.of eJptrI:Denis, designed to investlga~ tile ertecls of an er.perlinentalseparatlOn of indiVidUals (rom lIIeJr coiony upon beirIg retntrOduced. Two parameters were ezaniJnec:\ : the length of tile separation period and tile social expertence lJved I>y these individuals during tIlelr separation. Worlc&rs uvlng in t.oups of 5 individuals flO1ll ttle Same colony or in an allen cOlOIIY wIlere tIIey had been Preylously adop~ wm ~ected. oy tIIelr own Sisters WIleD. they were relntrOduoec:l Into tIIeJr colony, tfter a 70, 811'~ a ~5-day period Of separation respectivel)'. W. moreover Investigatoo tile offects on group cobeston of separatIDg oDe . COlony into ·two .lWves, depending 011 wIletller 01 not tile qlleen was present. Alter a 120-day separation, tile 2 limes or a colony did not merge rapidly and w1t11out aggressiVity, WIIess tile Single reprodUctive female was transferred from tile one nest to the otller every 15 dajs dllfing tile separatiOn pertOd.
In Ibe 1IgI1t 01 Ibe results obtained, we conclU
037~S1189I$Ol.!O
€> 19li91!1sev1er Science Publisher, av. (Biomcdi
36
INTRODVCTIOH The oohesion of the SOCial group, particUlarly among ants, Is
~y
based on a
process of mutual reoogoition among Its members, which impUes the ability to detect individuals not belonging to the group. By reoordlng aggressive behaviour between members 01 different colQDies, it is possible to ew!uate their p~rs ~I discrimination, e.g. Wl:Jetlter tIIel' belong to a species in Which Ibe oolonles are characteristically of the "c!ooed" type. • A great many studies ha'{e dealt with IntersJ)';cific agQoistic behaviour. Since the
end of the last cootury, several authQfS already hypothesized that there
~xists
a
distinct "oolony odor" : Forel (1&71), Mc Cook (1877), Lubbock (1883) (\Od then
Fi~iil~ (1901-1902-1903-1904-1905); IIlQre recently, particularly 9ln~ the devel~r.m~)1I.
61 SlXiobioiogical theory, Investigations have fOCUsed mi>re on the
study of recognition mechanisms betWeen nestmates, wIlether or not they were related. From these studies, it has beoome cJeer that the various strategies Involved In mutual recognition between indiVidUals bas not only evolved In IIl& different famiUes of
ooc1al Insects,
but
also in
the
dillerent sp
family.
• It slloUld be noted Utat a correlation does not always exist between recognition and aggressive behaViour. One and the.same oolooy can. be ather tolerant Qf very aggressive IOwal'ds anolber, depending on Ute el!p(lrimental conditions : a l. jir.btenstPJrJi colony can accept Intrudm and thon become very aggressive towards the sisters of the same intruders, wilen the two oolQoies are confronted (Provost, 1980 a).
.
37
Some authorS have suggested that the oolony odor. 'mlght have environmental origins; others are In favour of a genetic 'explanatiorJ wIlereby the odOr Is producod by tile workers; according to an "lndlvlduallstlc" model or a "gesialt" model (Crozier and DIx, 1919, reler to dlscusslon) or perhaps the queen mlght be the principal source 01 the odor (carlin and Holldobler, 1963, 1966). In fact, the recognltion cues .
.
.
mlght be basod on both genetic and environmental ' factors (ref.. revues by H611dobler and Michener, 1980; Gadag1v.r, 1965; Hepper, 1986; Page, 1966). Another lIn~ of research led to an analysis of the emergence
~f
the recognition
IOOChanl= through early olfactory learning during ontogeny : recognition by a
at the SpeciES level was made by Howard et al. (1978),. Bloolqulst et al. (1979), wIlo Showed that certain cuticular hydrocarbons of termites could be uWlzed as speciHc recognition' Clles. Alter anslyzlng the hydrocarbons of several species of .termites, these authors drew up chromatographic profiles characteristic of the species. Howard et aI. (982) has confirmed that. In two species of termltes, cuticular hydrocarbons as reoogllition cues betwoon species. Along the same lines, Clement's behavioural analyses 0976, 196I,1962).llave shown that elllllllination of the eplcuticle by the olfactory organs of tormlte workers oontrlbuw,; rowilf<1S oolony recognition. Clement ..t aI. (1964,1965) havo Shown that thm exisis "a good oorrelation between Interoolonlal aggression an
substances serve as the termites' "cbemical signature", and
are used by the the workers to recognize each other.
38
FortIler progress was aelilewd witll ants In a study of disC:rtmlnation a
be~
by Bonavlta-C<»Jg01lf
responslble for tile chemical Signature In CBmj»JMtus V3fJW ants : !1Jls signature is characterized by the relative proportions of dlmetllyl-alcanes, and the olfactory Signal value, characteristic of &ach colony, was demonstrated by m&ans of the 1ures metllOd". Very little lnforn')ation Is avallable about the mutual roo>gnltlon process..'S at work between members of the same colony in ants of
I~pWthcras
genus. Stuart
(985) bas shown tile importance of genetic and environmental factors In nestmate
recognition in . three North-American facultatively polygynous and polydol\lOUS species of !1Jls genus. DurIng prevIous e:zperlments (PrOyost, 1979, 1960 b, ! 985), I anaI}'200 som~ of
the dedSive
m~hanisms
of colony closure at the intra-specifiC 1&V&1, In several
monogynous specie'l of tJlis genus, and Showed in partfcular that the degree 01 closure of a given colony differs depending on the.colony of orIgIn of the Individual Introduced or on the type of colony With WIllcll it is confronted. The aim of the
pr~t
study was
to
investigate some aspects of nestmate
r&eogllltion In a me
On the basis of experiments in which individUals (living in groups of 5), were
reintrOduced .into a colony
after Varying periOds of "Isolation-, as weU as
exPeriments in which 2 colonies were OOIlfrwted, tile one having previously adopted several workers Of tile other one, and oolony 5plltting experiments In which a colony coUld be deprived of IIll queen, we proposOO oertatn hypolJles.
39
MATERIALS AND METHODS
l~l't(l/JJ(lmf IklItMStqJoJ colonles were coUected from the surroundlogs of AUauch. near Marseille. ThIs species occupies the slopes of damP 1II11S; 'wlth a northern exposure and they nest prlDclpaI1y In craCkS 10 the rockS and .betweenwall stones. These sm8J1 colonies WeJ~ easily collected 10 their totality. by asplrotlolflnto .a plastic tube. At the labOratory. the contents 01' the tube were poured IDto a tray (30 x 18 em). the bottom of WhIch was covered With plaster. WIIere the n~ was placed. The nest conSisted of a plaster slab (II x 9 em) that provided the necessal!y humidity and a glaSS plate·placed above the Slab. supported ·by two glass sUd~S placed on the two sliort Sides, that delimited a Ilelgllt of I to 2 centimeters, qUl!~ accuratelyrecreatlng the Daturatllabltat of these ants. The glass platecould !)$ pertorsted to obtaln an openlng. for the removal3lld Introduction of' ants; It was covered to create darluless. A glass plats;platod I; Oentbneters from tile nest contalnlng food (honty With Wlt sand added to avoid drownlog and cricket larvae less than · 2weekS old, wed by freezlng),.was permanently avallable and renewed twice a week. '!"he whOle set-up was brightly Ut and the ants lIllmedlately settled Into thenesl Fille crumbs of plaster were left for thelt use, iIn
40
recorded under a ~ular megnilier (enlargem~t : X 16), continuously for 30 minutes and foUowed for a \\Wi. Simultaneously, contrOl experlments were carried out They consiSted of removing tora@Jaglndivldualsand rGlDtroduc.lng dlem sevefaJ mlnut.."S alter marklog them to ·cbect< wIlelber tbls operation did nol cause any dlsbJrbance. The introduction of workers Into aD ·aUen colony was carrI«l"Out In Ule· same manner. First, 3 workers from colony 8, etter sucoesslve intrOductions, wtr e adopted by colony A. Secondly, after a period varying from 2 to 3 weekll (6 tests), .or a 45-day periOd (4 tests), coloDies A et 6 were placed In a Similar tray (42 x27l. on eacb stde of a removable wall. Confrontation between these colonies was carried out by removln{( the wall, after the ants bad Ilved for a time laps of one week In tbelr new environment All the memberS of both «)loDies were marked. The Interactions ·between tile allen workers and partiCUlarly, the behavIOur of the previOUSly adopted .workers, III the openrteld and sometimes inside the nests were obs.!rved Qurlng the next few bours, and then every day. Colony splltting was carried out to obtain two groups wbtcb were equal as regards t.be number and age of th~ workers and larvae. To thIS end; the C
41
RESULTS
I Experiments relntroduclng workers aftm" variable periods of isolation a) Wbether IsolatlOIllasted a few minutes, a few lloorsor up to 15 days, the final
r$U\ts were always the same : all 01 the reintrOClucM workers were 'aoeepted by tboIr sisters. '!bls result applied to more tI1an two hundred reintroductions Into 70 colonles, after Isolatloo pocIods'of less
\JIan2~
hOurs,and the re!ntroductloo 015
;ororkers Into each of the 3 ooIOllies tested alter isolation periods 01 15 days. During the first few seconds following ~ reintroduction, a great numbei" of
individuals surroundfld tll~ worker, WIllCll was simply drummed lor a rew nlinutes. While the drumming tOn!lnUfld,seVeral workers then simulbmeoUSly Utked the Intruder over Its entire body, but partleularly on the mark. Only the .matk was bitten; no bii9s were ever observod on the appendages. During the flrst-24hours,
the worker could .rold Its appendages against Its body, wIliIe being ticked. It partlclpated In.tropllaJlattle ~~angos, playing ine role of donor". Afieiwar.is, the I!ck!ngs betam" less Irequent and it was r~~b~ only because of the m'll'k:' . '!be 5 qU<1roS reinlrodUCedinlo their ooIonyafte!:a 15-da1 isolation po::iod all acoopted, "Iso
after
wei'"
lite 2 prelilnlr!aty stag
at<:OlIIpanled by llct:Wg.
• 'Ibis behaviour tould be Interpreted as an appeasement behaviour as · has Imn suggested In ants by De vrooy and Pasmls (1976) in MJ'Ozicn robn, Bhai:kar (1979) In various specieS of .fo],o.nOpsis an~ In tile case of beeS by Rlbbands (1954),
Breed et.~. (1965) In ApjS111I"Jljfer.1.
42 b)
After an ioolaUon period QI ~5 days, 14 of Ule 15 relDtroduC@d workers In Ule 3
colonies were accepted, as were Ule 5 queens, by Uleir oolony. A ' s soon as Ule workers were reIDtegrated, Uloy were blttoo on Uleir appendages 'lor about
2~
hours. Progressively, tJlese bites llecame less frequent and UckIng became much more Irequent. Note tJlat Ulese bites. never caused a v Si ible wound. The worker let now a drop olliquld betweeD Its man
Two or the live lemales r. lntrOduC@d Into their ~Iony were takeo to the brood, by moans or their carrylDg method typical 01 MJ'(tnl~ a few minutes alter Uleir Insertion. The oUier U1r~ were bitten by severrJ WOrkers on their appendages and Ule petiole, lor I to 3 bO;Jm. ()n.;c agaln, a llckillg pbase lollowod the biting and Ule queens were transferred to the brood clu~. c)
After looger pertods oi Isolation (70 days-90 daYS-120 days;
15 tests were Oooducted work~rs
00
wltb every period,
3 ccloru~s), a very dlUereot result was obtalDed : Ule
wore blttoo immediately, violently and simultaneously by a large number
of IDdlVldUats (according to an -asterol
43
It. setIIlS (JOe! tIlat tIl~ longer
~
period of
~patatlon,
1M more dlffkult tile
readOption of Isolated individuals beeomes, WltII a t!lro..l\Old 91t:1ated tetween 45 and .70 days ollSolaUon. II
IlxDerlments confronting 2 colonies
rot
oj wIllcb
~ad pmiooOI!_~
workers 01 anotl~ Confrontation be~'n , 2 colOnies, tile one OODtalnlng 3 adUlt individuals originating Irom
tIl~
other colony !>rOUgIlt \.) UgIlt
dj(f~rellCes
In tile adopted
workers behaviOur, ' depending OIl the length or time spent In 1M allell colony and
the type 01 interaction manlfested between tile Workers of tile two groups, altllougtt it Is not)iosslble to say, for ttle moment, wtJether the 2 fattors 3.ct simUltaneously nor wlietller eltller one was preponderant. I\fter a period. of ~patation 01 2 to 3 weekS, and to the case of 3 colony pairs wIllctt merged, .tile 9·workers \'Me taken by tile adoptive workers, during a mass remo'la1, to tIl9lr original group, between tile 5th and 10th bour after the operung of tho Wall, After the same pertod O(S$patatlOll, In 3 olller pairs 01 colonies WIIiCIl had started flgbts Involvin& no deaths, anll wIllcb had not fll~, 7 of ~ 9, previously
adOpted workers returnee to their colony 30 hours altllr tile openlog of tile :Wall. During tile first enoo.uoters, we obserVed fleeing movements by . tIIolr sister
resident Wl)rkers aodtllen UCI:JDg and lropbaUactic ellCbaoges, (1M new amVals playing the role of dOnors). After a 45.ooy period of ~paratlon, In 4 pairs of colonies In wIllcb Wl)fkers hadstart.ed lights ending In.
44
other, or a "chain" typ9 01 lighting Where a previously. adopted .worker was bitten by one sister, and in turn bit another worker sister. III Experiments oonfr9ntJng 2 halves of We same colonv alter varying ~ ~
The following cases mre investigated : a) Il
The separation of the two groups lasted 120 days. With all 6 palrs of colonies tested, we noted the same interactions between sisters: on the fOCd only short bites, tllat left no wounds. LOIlg antennations
~l'e
often noted between workers of both groups.
[ndlviduals passed. from one nest to another. [n 2 out of 6 cases, alter many montl1s of contact, tIley all progressively reunited in the same nest
b) The queen was [eft in one of the two halves of the colony. Four tests with 45·day separation periods between 2 half colonies W&r-:> carried out. Whatever the strength of the groups (from 40 to lOa Workers),lbetr fUsion was observed to oceur between 30 and 40 !lours alter the ~nning of the experiment, during Which time we observed reciprocal visits that were non-aggressive. in 3 cases out of 4, the group with the queen moved to the ot'!er group's nest. [n one of these 3 cases, a small number of workers in the queen's group "carried off" the nymphs of the 'other group before moving. [n the 4th case, the fusion was reverSed. Five experiments "",re earrted out ( stze of the groups: oK> to [10 workers) with a 120-day separation period. During encounters numerous figbts occurred in the
45
oulslde area. It was very rare tIlat a worker penetrated Into tile nest of tile otller group : at tIlat point, tIley \'/We energetkaUy attaCked, bitten .and pulled oulslde. These attackS caused a few caoos of mortality. In any case, each group stayed In Its own nes~ even arter several montlls. c) The queen was alternatiVely transferred from
one nest to IIIe oilier.
In 4 out of tile.5 tests (sIz&ot COlonies: 65 to 135 worltors) WIler
15 days during tile.
'4 mOntllsof St>paraUon, fusion of tile two groups was obSerVed to o
35 to
40
hours alter llleremovaJ of tile partition beMen tile nests. Here &gain fusion' wis
prectede
experimeD~ tile
first week, witllout any massive moving. Note tbat in ·au tile queen's transfers, altor a 15~y period ?t separatioll, sh& was · readUy accepted by her ·dauglltors, WIIIcb immediately Ucked ber and carried
her to tile brood. CONCLUSION -1)1 SCIISSION Tb~
point to
results of tile above ellpeli!llenls earned out on tile L UdlfR.J1steJlZi ant tile follo'wIng conclusions:
, a worker, alter bellig separated from lis colony for 70 days, Is no longer
accepted by itS 51Stors on being reintroduced. - a WOrker, aft&!' a
45~ay
adoption period by an allen oolony of tile samo
spedeswiU fight lis own 'slstors and Is also attaCked by tIlem WIlen
tll~
Zcoloo'ies
ooo!roo.ted do not merge and WIlen fights t>eMe8 allen workers occur. - alter a 120~y separation petiQd, tile 2 halves of a colony will not fuse with aWessivlty, UDless tile queen Is transferred from the one nest to the other
(juring ttle periOd of separation. A On ttle basis of ttl_ data, b)'pOttleoos were formulated as to ttle me<:llanisms involved in ttle mutual re<:Ognltlon procwoos ootw*n ttle individuals In a oolon),. I The questionarloos as to why (I stoories of experiments) adult individuals isolated from ttleir oolon), for 70 days or more are killed by ttleir own sisters when ttley are reintroducod into ttleir colony. a) If we assume ttlat ttle odor OOIIIIllon to all ttle memoors of a tolony results from a continuous tzansfer of substanoes (by licking. food exchange or simple oontatt) between ttle group members (a
during ttle period of isolation in a small group. TIl!s liIodifitatlon, wlllth is signlfitant sinte it prevents ttlem Irom being re<:ognized when first reintlodutted, . may result from ttle fatt ttlat tile sma1I groups of live "isolated" individuals did not oontrlbute as much to ttle oommon odor as tile whole oolony did, Besides ttle odor of Utese small groups whlth had boon separated Irom ttle colony, andUtat of the stock COlony, whith was !Uuth more \X'pulous, presumably evolve and OOoome diversified, in ttl. oourse of .time, OOtause of ttleir different genetic variabillty.
Carlin and H6Udobier (1963), stuart (1965), Errard (1906), using ttle experimental model 01 Ute heterospectric miXed oolonles, have shown Ute eXistence of a transfer of odors linked to re<:ognltion ootween individuals of a miXed colony. Carlin ,and H6Udobier (1963) bave re<:orded an indiscriminate acceptance on Ute
part of workers originaling from stock oolonles to'A'aI'ds workers of various species of t~mp.motw raised togeUter in a mixed oolony. On ttleottler hand, Errard (1966), tarrying out groupings of ants of different genera Waoka roNda and
ForJ)Jj(~
47
s#y.'Ii), has no~ tIIat tile longer tile period of separation between 2 groups 01
different genera tIIat had previously formed a mixed colony, the more aggressiveness between workers In both groups was observed. LaStly, Stuart (1985), carrying out eltperiments on 2 North-American species of ll'pf(ltIJrJraE.' t. /QDf{.i..
at11b1ffl1l1~
noted tllat individuals from several mixed colonies
originating from tho same parental n(''Sts showed little aggresslvlty ·toWards each otller and tIIat the fusion betWeen mixed colonies Involved llWe aggressive behaviour. Lastly, Morel and Blum (1988) have demonstrated the eldsl/)nce of a tranSfer of recognition cues from the nurses to·the oallow workers In c"mfX'l1~tl1$ nl>iidaDUs. II) If it is true 'that each member of the colOO.yproduces Its
own odor, which Is
recogniZable by the other members, (the indIvidualistic model by Crozlerand IJix, (979), it might not be the chemical signature of tile workers isolated In wall groups that cbanges, but the worker sisters' -memory bank- (or template, see Shellmann and Gamboa, i962) , WhlCb changed during the period of separation. The.Wl)rkers may have -forgotten' the Individual signatures of their isolated sisters. Jrolatlon expvriments ,carried out With the primitive bee ~"'5$IIJ11 ii¥'.pliyJ7lJ11 showed tllat the longer a bee was kept away from its nest (I to·72 bours:
BeU,1974; I to 12 days: Kukuk et aI., 1977J, the more It aroused the aggresslvlty of the guardian on reaChing the entrance to its own nest The authors conclude
th~
memorizing of numerous
different signatures, is highly unlikely to ap!)ly to L D(:bto?Jl5f<9ioi tolonies which
48
can contain 200 to 300 Individuals, My own results are thercfor~ more in line Willi lIIe "gestalt" ~ mod~I, Note lIIat very iow aulllors have used the Indlvidua!lstic model to explain recognition processes. Mintzer and VinSon (! (35), have taken tills model
to be
lIIat WhIch best fits lIIelr results ,on Psou
One might object that In my eRperiments, the ants separated trom their colony and living in very small groups might have been unable to produce their individual characteristic odor, However, It should be mentioned that the behaviour of ' workers, Isolated In very small groups, remained completely normal : they bullt an en<:losure around the nest, conducted foraging, took care or their brood, and had trophallaCtic contacts,,, When kept aJone tor several months, a single ant also bullt an enclosure, collected food, raised the larvae, questioning Ibe largely aooepted idea that an isolated SOCial Insect cannot survive (Grasse, 195&),
• I do not find these'tlndingsvery conclusive, however. These authors repol'WO that individuals from 1b9 same nest are otten treated differently when inb'Oduced into another nest, WIlereas In a "gestalt" model, lIIe expected frequency of rejection is either Oil: or iOO~, TIle fact that they recorded Intermediary values might be attributable to the experimental conditions : eaCh test lasted only 5 minutes and every colony was subjected to 20 Introductioos. The authors did 1I()t spect!y Whelller or not llleir sucmsiv. tests mOdified lIIe frequency of rejection. IWotUd recall (Provost, 1985) that stabilized interactions be~n Intruders and r~lver colonies were recorded In L b'tbtM$tMll In 651 of the cases sbIdied. T!lls resUlt was obtained alter several hundreds of introductions but 'with only 3 tests per colony, and the stabWty observed was In relation to the final result Obtained after several days : ,adoption or klIl1ng. During the first few minutes. the in~racUons be~ colony and Intruder coUld be extremely variable among 3 intruders or the same origin intrOduced into the saroo colony,
c) It is worlll mentioning that. In our
~lIp6rll1l.nts,
tilt indiViduals rtlntrodu()ed
Into their ~olony alter a long separation were neve. aggressive towards the res\dllllt
workers. We =ot, hO'flver, deduee that the former had DQt lost their , group odor. In
fa~t.
slllee they were simUltaneously attacked byse'f&ral workers, It was
probably not possible Cor them to underto:e any aggressive a~on. Wilson (1975) has reported a ~ WIlere l ept<>tlJorudulnfiC1/$ workers were attacked by their L
curvJsp.iDosu.< , slaves WIlen
~
slaves'were relntrodu()ed Into their colony alter a
50day ISOlation period. 2 Although the seoond series 01 experiments Is still In tile preJlmlnary iIa~,
the resUlts Obtained so Car have sllOwn that a worker UVing In an ullen ~olony (or 8 period of 45 days wlU fight Its own sisters WIlen Ute 2 oolontes are oonCronted and' that It w11I also be attacked by them. It Is as If theauen group's odor Is acquired by an Intruder, aboUShlng or maSkIng lis own odor, It !Jl!ght attack its sisters alter
oomparlng the ~el1lical signature 01 Its OrIginal group W1t1l its own newly acq~ odor (USIng Ute "itlf matdllng" process destrlbed by Blaustein, 1963; Holmes and
Sherman, 1963; Hepper. 1966). An alternallve,tIplanation Illlght be that some kind of learning In the adult stage, 'oColtactMy conditiOning
~ured
(Thorpe '1936;
JaIsson, 1975). Tbls stOOnd hypothesis dOes not exelud~ a trinscerof the ~em!c3t signatures and'a,stIt matdllng prooess, but Dilgllt be a l4ecMn1Sm Occurs WIlen
anls are introdueed Into alien oolonies.
wlll~
always
Free (1956) haS reported stmUar Clndlngs on 'bumbll)"bei)$. ~J11b1'$8IIW1l111 workers havUtg spent I to 2 hours in another oolony were vigorously attacked
WIlen they wereremlroduood Into their'nest. Ukewise, with ,the L ZIlj)lJputDbre; BeU(l974)transferre.s individUals frODl one oolooy toanotller an!! Showe.t that tbe
10000er the UlDe SpeDt In an aullll nm, tile more dlffleint tile subSequent a40ptlon by thE> original CQlony members beoomes. ,One might wonder wily a worker wt.l~ll has been itparated from Its group for
so 70 days or more, was found to 00 pas3ive WIllie being attacked by Its Sisters (1st series of
e~riments),
Whereas here, it fought them activ..ly. To answer this
question, It would b& necessary to carry out individual refntroduction experiments on workers bavlng lived In alien colony. As a matter of fact, the lack of experlenoe In having contacts With an alien colony migbt b& one explanation for Individual passiveness. Remember that a worker that bas been Isolated lor 45 days is accepted by Its sisters when refntroducted, whereas a worker Integrated Into an alien group lor the same period Is attacked by its sisrus. This difference shows that the soctaI environment plays an Import?.llt part in recognition mecbanlsms. 3-a) Conlrontation between two halves 01 a COlony, both depriVed 01 the queen, WIlICb bad been separated lor a 4-month period, led to very little aggressivity among the workers. The merging of the 2 groups Dever involved intorindividUai
trall~portation
during a massive removal. When
th~
rounion 01
individuals in a single nest occurred, this was a progressive process taking several months, possibly owing to a lamiliarization pbenomena. The fact that the workers of both groups stayed in their own MSts, at least during the first few months, may be attributable to the fact that a
J.~pt0tbara3
colony instalied In a nest .lor a long period manifests a very little exploratory activity in unknown territory (stable colonies by Aron, 1984). Our experimental conditions, where individuals instalied in their nest for a 4-month. period, are suddenly presented With an unknown territory, are not lavorable to the merging 01 the 2 groups, sinoe this behaviour reqUires considerable exploratory activity. b) When the queen was lett in one 01 the 2 colony halves during the 4-month
51
separation period, .Ill& workers of .bolll groups aiso stayed in tIIW nest; 011 ·belng confronted,', but Mre, during ·encounters In ' the openf!&ld, Clgbts were reeor4ed which gave rise to som& mortalities, Tb& . pr_ of th& queen In only one of Ille 2
groups causes a dltfereoUaUoll betmeo Ill& recognitlon cues. Arter a sborter period of separauon (45 da)l$), tlle 2 half colonies merged : tb!s dUfc,oouation did nothav. Urne to becom& estai>USIled. c) The previous assymeUy was belanced out by ttaasterrtng
Ill~
queen,
alwnatlvely from one nest to another, during Ille separaUon phase, Herefu;iOD of Uto 2 grouJi.~ was recorded, WIthout any: aggressive behaviour, The'errectil of the queen's pre*lIoo were found to pectllin even thougb th& 2 groups ha4 OCCUPIed their nest for more thBll 4 mooths and the outside was unknoWn to Illem : Ille. ·quwo eCfect· preclOlnlnatAls over any group StabWty errect, as detloed.by Aron (1964). Numerous auttJ
mtchanlsms WIlereby Ille queen"ls
recognized by her workers, as weU as Ille attraction She ell9rtS on them, ID tile ~ or many soc!aJ Insects. For·el3lllple, for tile domestic~, the studies by, BoCIi and Morse 0974·1919-1962)an4 those by &reed 0961·1963). As WltII ants,WatJdns ' and Cole (966) for DoryUoes, Jouvenaz et ai, (963) 10 jl;I/Mopsis itlPicta, have Clearly sbown the workers are more strongly attraeted to tbelr motller than to queens of tile same spedes belooglDg ttJ dltferent colonies. TII~ aulllors suggest that Ille colony's SpedllC odor may superlmpClSf !tself on Ille queen's·pllO.romone,
which attracts her own offspring, In the same way, Glancey et'at 0961) ,and Lofgren et ai, (983) have shOwn the el1steoce or a pheromone, ariSiDg froiD Ille po!son sac (Vander Meer et aI., 1930), WIIlCh !s used for both 'attracUOD and recognition purposes by tlle S. itlpicfD queen, The fOUowtng data have beo.!Il recorded, on
many dUferent, extremely
polygynous speaes.
Laog~
(1960) bas shown .!IIlt !lie separation of a kIm",,,
f't'l)'dena colony Into two parts was not suffiCient to transform the 2 groups . into
aliens : even alter 4 montbs of separation, Ule foragers ta\(ffi out of Ibe 2.groups oX(hanged food among ea(b oUler wllb tne same frequen(f as wltb individuals of Ibeir original colony. But Ibe two groups were UWl.elUler ellperimentaUy deprived 01 a queen or contained r~vely I to 14 quceus. For F. JlJ8Ubfi!; CberlxtJlld Gris (1978) bave pointed out Ibat Ibe ground snow WbI(b Isolated Interconnecting nests from ea(h olber for several months brougbt on no aggresstvlty at spring time between wouers from Ule various nests. In the ant Iddomyrmex 1111JJ1iJi.~ alter a slx-monlb separation period, small groups of 10 workers \'/We a((epted by Uleir nestmates Without any aggr~vlty (Giraud, 1963). In NynoJc!lfuNa Brian (1986) bas deDIonstrated that 2 groups of newly born Sister workers, raIsed for a period of 3 weekS WlUl queens ~, Ibe !'aJIlespeetes but of dlf!~r~ntorlgins (t.b~ Istgrou? WlIb tb~
molber, tile ot.b~r With an alien qUNn, or bolb groups WIt.b an alien queen),
coUccted food togelber ,,;thout bOStiUty When Uler were oonlronted. Tbese results coinCide WlUl What Is known about polygynous colonies, wbere Ibe ctosure Is often not obVIoUS (lbe bypolbeSlS generally put forward Is that·Ibe large number of femaJes might give rlst to a. vast range of ooors, so that It Is possible for many alien individuals to become a((Opted) ; and When the colonies are closed, ibis does not seem to be due to Ibe females. Tbe role of Ule queen In the ctosure of t.be group and in the mutual rtCOgDitiOll. prooasses between wouers of monogynous speetes was eluCidated by Holldobler (1962), Who pointed out Ulat If Ibe only female was removed from a CWf't'O
from their colony of origin, Iben these worker groups Without the femaJe became In-dillerent towardS worters 01 an alien COlony 01 the same spectes. Along the same U'oes, I have $bOwD (J>rovost, 1960 b) Ulat 2 CWf'l'l1"tus /afRJ8/Js colonies cannot
S3
fuse unless on~ of them Is ellptflmentaUy deprived of Its queen. HoUdobler and Wilson (977), HoUdobier and ",,~el1er (960) bave remarked tIlat U tile odors bave a partly genetic origill,lt Is easily con(&ivable that In monogynous species, Whose coloDies are usually close
important role in ttle production of the OdOr! because the genetic Variability or the workers will Increase tM diversity of odors to ".Cb a <»D1ustng level ,that reoegDition of l1estmal:$s W11I D.O longer be possible. TlIlsldea, I WOUld add; Is not appUcable to cases WIIere a ctJllUDOO odor Is tIlought to eXlst, ':onslstJllg ot a combination of individual odors. It is dllffcUlt to say for the moment WIIat mecbaJllsm brings Into p1&y tile "queen erfect". Does tile queen bave a privileged
ro~
in the 0010111'S odor
production? Car1ln and H611dobler (1963) bave demonstraWd the existence, among various species of C8mp.)fJ(I/Q$, of "diScrimfDators" linked to tile queen'& presence,
Wbicti are uWiZed during the recogDiUon promses, and are suttldentty £trongfor
the workers of tile orlgiDa1 colony not to be able to r~ s1SW!lI ralsedby a hel:$rosped1lc queen. In these autllors~ 'opiDlon, the substances produced by the queen. oonstitute the prlndpa1 mecbaDiSlll, predominating .over auy "gestalt" etlect (CarUo an.d H6Udobler, 1966). AMl:ber bypot1>.ests mlgbt be enVisaged : the female, by her prosenco, mtgbt SUmUiabi tile prodUction by tile WWkers of subStances intervening in tile recogDiUon processes. B
III OOI1c1uston, in L
1kJ1~
ants, tile COlony odor used '(or recognition
purposes among Its members mlgbt be based on several coexiSting systems : "an odor may be produced by eacb individual of the group. ThIs IndlvlclllGl odor dependS 011 a genetIC compound (Provost and Brun
1986 aDd
in preparation). i11IB !laS been demonstraWd With L .zt!JibJ'FUl11 (Greenberg. 1979), ApiS
m.¥lil«a (Br*
1':!IeIJdMJ)'J7J1eZ fenuSiJiM
54
(!(.tntzer illiG Vinson (1965); • our ~xperiments suggest the
~Xistence
of a colony odor common to all Its
memwrs, which results from the trllllsfer of individual odors, as described by the "gestalt" model; • the odor might partly derive fNm the physical envlronment (the nest for ~xample). Tills point Is
not tr~ated here;
• the queen plays a privileged role in the
closur~ meclla!:.~
of the SOCIal
group, as shown by the data recorded in this study. carlin and HoUdobler (196&) have proposed that the various types of
ch~pical
signatures of wopoJ1<")iu$ ants may W organlzed in a' llIerarchy : discrimlnators furnished by Ute queen, discriminators produced by the workers, auct· acqulred ,~vlronmental
odors. Although the pres~ilt"experlments show the role o~ l~0 queen's
presence, It must however be underlined that colorJes experimentally deprived of the queen are not systematically open and that a queen separated from her workers ior a period·of 70 days is no longer recognized as such and Is attacked In the same manner as a worker subjected to the same separation. It Is therefore not possible, at tills stage to conclude wnether any such hierarchy of recognition cues eXists in 1.. J.WJf&J$t.e.iJ.!i.
O!-,\lOsIte results were recorded by Kalmus and Ribbands (1952) . they demonMrated that in honey Wes the workers were preferentially attracted to the dish ~isited by melllbers of thelr own colony. This preferential attraction was shown to be based on the distinguishable odors emitted by the workers. The presence of th~
queen was unnecessary for the maintenan.:e of the preferential .attractiOil.
Similarly, MIntzer (1962), Stuart (1965,
1967) have dQlllOPstrated the
non-preponderance of queen' related factors in recognition processes. Mintzer has reported tb.at in P. t«rucioiii1, 2 worker groups ralsed from the larval
st:o~e
bl
55
different qUe
dori~ ~ receiver coioDtes did notlntluenl» !be, aCl»jltance of
Intiudlng individuals, regardless of WIletber or not tbey were of the same 'Sp.ci~. ,"
,"
-"
.
.
Lastly, Stuart (t 967) bas demonStiated In l. ron'/sp/MsV$, a faCUltatively pclygynous sp&CIes, that individual wOrken produce tOlony-speclUc r~oitlon cues alter ' eclOSlon, regardltsS of !be
number of que
In
queenless colonies. Tbls gives us some idea of tile diVersity of 1M recognitiOD systhms lIlat various sp&CI~ of
ants have developed In !be course of EvolUtion.
Aron, S. 1964. ROft du marqua~du lIml~lre et de la competition iIltiaSptculqu~ daIls fa dynaailque du recrutement ~enialr& Chez ltyWfJJNuiJlJlla5dawt< MemOlre, de ~nce. Un/venlie L1bre de BruHtUes., 97 pp.' , " IltU, W.j.,1974. ' Recognition . of .resident and' non-resident Individuals In Intraspeci!lc lIe$l defense of primitively eusocial ballctlne bet, ). Compo Pbyslol.. 9!d95,-202. ' ' , BbatJru,AP., 1979. ,Troph6nactlc appmement In ants from distant ColoDfes Folla/Entomol. MelL, 41 : 135-14'3. BlaUstAln, AR.; i 963. 'KIn reeogiutloll mechanisms: phenotype or r~tlOD aIIeles7 ,AmerJlat; 121:749-754. BlomqUist, G.).. Howard R.W., McDllllel, C,.A" 1979. Structures of ,tIlecuticutar bydrocarbons of !be teimlte io<>tNmopsi$ et:tUstkIN1Is (I!a~). Insect Blocb~m.
9: 365-370.
'
"
BoCh, R., Morse, R.A. 1974, Discrimination of faDlWar and fortfgDqueens l>ybOriey bee swam',:l. AmI. Entomol. SOc. Am., 67 : 709-711. ' BoCh, Ro' c.I¢'i5e, lA" 1979. Individual recongltlon of queens by boney bee swarms. Ann. f,ntoinol. SOc. Am., 12.: 51-53. ' , BOcb, R" Morse, B. 1982. Genetic factor iii queen recognition odors of boney bees. Ann. Entom?L SOc. Am., 75 : 65+656. , " , Bonavlta
56
Breed, MD., 1981. Indlvldual t~tloo an~ leam!ng of qllooo ~ors by WIlrker honey bees. Proc. Natl. Acad. ScI. USA., 78 : 2635-2637. Breed, MD., 1963. Nestmate recognltlon!n boney bees. Anim. Behav., 31 : 86-91. Breed, MD., Butler, L., stiller, TM., 1965. Kin reoognltlon by WIltiter boney bees!rl genetically mIXed grOUp6. Prce.Nat!. Acad. ScI. ,U.s.A, 82 : 3058-30&\. Brian, M.V., 1966. Boodlog between WIltkers and queens In the ant genus Myimf<2 Anim. Bebav., 34: 1135-1145· Buckle, G.R., Greenberg,t., 1981. Nestmate recognition in S't.oeat boos (JasAW/(ISS11Dl lNp1J,rum) : does an Individual recognize its own ~our or Only odours of its nestmates? AnIm.Behav., 29: 802-809. carlin, NP., HoHdobler, B. 1963. Nestmate Iltld /tin recognition in lnterspeclf1c mixed colonies of ants. Science, 222 : 1027-1029. carlin, NP., HoUdobler, B., 1966. The !dn recongltlon system of Carpenter 'ants (CaIlJpoI1o/lls spp) i : iIIerarchlcal cues !n small colOnIes. Bebav. Ecol. SoCioblol., 19: 123-1~4. Cherllr, D., Grls, G., 1976. Relations at agreS$ivi1:e chez i'
57
FI~ld~; AM., 1902. Notes on an ant. Pro<:. Atad. Stl., PblladOlpbla, 54 : 599-625. Flelde, AM., 1903. Artlfltlal mlled nests ~f ants. BioI. Bull., 5 : 320-325. FI~ld~, AM., 1904. PoWer of recognition IllIlOIlg ants. BioI. SuII., 7 : 227-250 . Flel
58
cocons chez la jeune (ourm! rousse (FMJ1k8 t»/ymIP8 Forst). Bebavlour, 52 : 1-37. Jouvenaz, DP.,l3anks, WA., Lofgren, C.S., 1974. Fire ants : attraction of workers to queen (le(retiollS. Ann. Entomol. Soc. Am., 67 : 442-444. Kalmus, II., R1bbands, C.R., 1952. The origin of odours by WIlich llOoeyt>ees dlstlnguish their companions. Proc. Roy. Soc. (6), 140 : 50-59. Kuklllt, PP., Breed,·M.D., $obti, A., BeU, W., 1977. The contributions of klPship and conditioning to nest recognition In a· primitively eusoclal bee, l8$i~"UII1 .ll'pbf.TllOl (Hymenoptera : I/allcUdae). Behav. Ecol. SOC(oblot., 2 :319-327. Lange, V.R., 1960. Uber die fu~t.ergube ZWiSchen AJlgeMngen verschledeoer waldamelsoo. Z. Tterpsycbol., 17: 3&9-401. Le Moll, Y., PasseW, M., 1977. Til. effect of early learDing on recognition acceptance and.care of cocoons In the ant FarI11k8 nUa L. AU! Soc. Ita!. $(i. nat, MIlano, 116 49-64. Le Moll, F., Mon, A., 1962. Early teaming and oocoon nursing behaviour tn the red wood-ant Formka Jucu!Jris ZetJ. (Hymenoptera : FormIClda.). Boll. 2001., 49 : 93-97. Le MoH, F., Mort, A., 1964. The effect of early expeMnce on tile development of -aggreSSive- behaVIOur In FarmA..., JucubrisZett. (Hymenoptera: FormlddM). Z. Tlerpsycl10l., 65: 241-249. Lofgren, C.s., Glancey, 8M., Glover, A., Rocca, J.. TumbllsoD, J.1963. Behavtor of workers of ScJ~ iovicta to tM queen recognition pIleromooo: labOratory studies with an olfactometer aod surrogate queellS. Ann. Entomol. Soc. Am., 76 : 44-50. Lubbock, J., 1663. Ants, bees, and wasps : a ro<;ord of observations on the habits of the social Hymenoptera. Appleton, New York, 448 pp. Me COOk, .a.c., 1677. Mound-making ants of the Alleghenies. Trans. Am. Entomo1. SO('. 6 : 253-296. . Mlnl63r, A, 1982. Nestrnate recognition and incompatibility between colonles of the acaCIa-ant P$\tUdlW}'mti9..1·/"rr~. Behav. Ecol. SoCIobiol., 1(): 165-166. Mintzer, A., Vinson, S.8., 1965. KinShip and IncompatibiUty between colonies of the acaCia- ant P$\tud!wyrlmJi/imrcitM!. Behav. Eoot. SoCiobiol. 17: '15-76. Morel. L., .1982. Mise en place des processus de regut&t.ion du oomportE>ment agresslf et de la reconnaissance entre ouvneres d'Une soCl~te de CMlf»11Otul' "Bglis S (Hymenoptera: Fonniddae). COU. Inter. Sect. Fr. U.I.£.I.S. Jl·.u:celon&, pp. 127-136. Morel, L., 1903. Relation entre oomportement agresslf et privation soCiaie precoce Chez les jeunes immatures de la fourmJ c.wp.?/J(Jfo.' I'3$U$ Stop. CR, Acad. $(i. 296 : 4~H52.
Morel, L, 1986. Ontogenese de la reconnaissance des membres de Ia societe cI1ez la (ourm! CMlp.?Oo>tusHoridanus: Bull. Inter. S.F.E ..U, M
59
Page, Rli., 1966. KIn rerognltlon In socIa1lnsects·: an Informal overview. C.R. loth Int.e-rn. Congr. l.U.S.s.l., MilnIch, Workshop: kin recognition in socIa1lnoocts. Provos~ E., 1979. Etude de la fermature de la societe de fourmis chez dlverses espeCe5 de It'pt(!thMlEet chez C3mJlO11'.,ws/at<,.raJ/s(Hymenoptera, Formtctdae). C.R.Acad. ScI. Paris, 226 : 429-432. Prov~ E., 1960 a. La fermeture des socIet!fs de J..opt