Nordic Society Oikos

Nesting Space Limits Colony Size of the Plant-Ant Pseudomyrmex concolor

Author(s): Carlos Roberto Fonseca
Source: Oikos, Vol. 67, No. 3 (Sep., 1993), pp. 473-482
Published by: Wiley on behalf of Nordic Society Oikos
Stable URL: http://www.jstor.org/stable/3545359
Accessed: 01-12-2015 21:04 UTC

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 1993
OIKOS 67: 473-482.Copenhagen

Pseudomyrmex
spacelimitscolonysizeoftheplant-ant
Nesting
concolor
Carlos RobertoFonseca

spacelimits
Fonseca,C. R. 1993.Nesting Pseudomyrmex
colonysizeoftheplant-ant
concolor. - Oikos 67: 473-482.

Thesizeandstructure ofthecolonyofthestinging plant-antPseudomyrmex concolor

occupyingtwomorphologically distinctTachigalimyrmecophytic hostspecieswas
studiedinorderto discriminate
betweenfactors limitingtheantcolonysize;specific
hypothesesbeinga) food,b) territorysize and c) nestingspace.Fromintraspecific
comparisonsitis suggested
thattheantcolonysizeisprimarily bythetotal
controlled
domatiaspaceoffered bythehostplant.The space-limited explainswhy
hypothesis
demonstrate
plant-ants foraging
host-limited I analysethespace-limited
territories.
hypothesisfromthehost'spoint-of-view byusinga cost-benefit model.It is
graphic
suggestedthatdomatiasize can be selectedin a waythatincreasestheplant'snet
benefitfromthemutualisticrelationship.

C. R. Fonseca, Animal Behaviour Research Group, Dept of Zoology, Univ. of

Oxford,South Parks Rd, Oxford,U.K. OX] 3PS.

Wilson(1971)estimated thatatanygiventimethereare 1991).The sizeof a singlematureantcolonyvariesby

about10'5livingantson theearth.Thisis notastonish- manyordersofmagnitude froma fewindividuals inthe
ingifit is consideredthatin sometemperate localities largestant Dinoponera(Ponerinae),to hundredsof
theantdensity can be 140workers perm2(Kajat et al. thousands in thepredatory armyantsEciton(Retten-
1971),and in thetropicstheantscan represent up to meyer1963).Antcolonysize in myrmecophytes varies
halftheinsectbiomass(FittkauandKlinge1973).In the froma fewtensof workers of Pheidoleinhabiting the
crowdedenvironment of rainforestspracticallyevery smallshrubMaieta(Melastomataceae), to an estimated
squareinchof surfaceis underthedomainof at least colonysize of 1.8-3.6millionworkers in somepolygy-
one antcolony.Interference betweenantsis notlimited nousPseudomyrmex inhabiting Acacia (Janzen1973).
to the groundlevel but the wholethree-dimensional Although thematurecolonysizeis knownformanyant
structure of theforestis occupied.Actually,manyant speciesmostof its variationremainsnot understood
generaarearboreal,passinga partorwholeoftheirlife (HolldoblerandWilson1991).Severalfactors can con-
in trees(Holldoblerand Wilson1991).At theextreme tribute to determine thematurecolonysize (Sudd and
are the ants whichnest in ant-plants, or myrmeco- Franks1987).It has beensuggested thatfoodcompeti-
phytes, insidespecialplantstructurescalledmyrmeco- tionamongcoloniesis an important factorlimiting the
domatia(Wheeler1942,Benson 1985,Beattie1986, productivity and fitnessof manyspecies(Pontin1961,
Huxley1986). 1963,Boomsmaet al. 1982).In thetropics, whereant
Muchof the ecologicalsuccessof the antscan be diversity anddensity is high,theevenlydispersed spac-
explainedbytheircooperative behaviourwithin genet- ingpattern ofantnestssuggests thatterritorial
interfe-
icallyrelatedcolonies(Wilson1971).In general,colo- renceamongandwithin speciescouldbe structuring the
niesare foundedbyqueens,and growbyworkerpro- community (Levingsand Traniello1981,Levingsand
ductionto reacha maturesize,whenproduction ofnew Franks1982). Holldoblerand Wilson(1991) listthe
reproductive alates starts(Holldoblerand Wilson mature colonysizeofmanyantspeciespointing outthat

Accepted 21 October 1992

(? OIKOS

OIKOS 67:3 (1993) 473

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 fiedas WetTropical(Holdridgeet al. 1971), theaverage
annual temperatureis 260C, and the average annual
Tachiga I
i/a rainfallfor the last 30 years is 2186 mm. The reliefis
myrmecoph
formedby plateaux at an altitudeof 80-140 m witha
deep, acid and
clay-sandysoil thatis characteristically
well drained(Sombroek 1966).
Domatium entrance

Naturalhistory

- Petiole | Rachis In Cabo Frio, Pseudomyrmexconcolornestsinsidethe

expanded leaf petiole and rachisof small host trees of
Tachigalimyrmecophila Ducke and Tachigalipolyphylla
Poepp. & Endl. which are scattered in the forest
Domatium Solid rachis(1 (Fig. 1). Workersfromadjacentplantsshowstrongago-
nisticbehaviouramong each otherwhen submittedto
replacementmanipulations,and behavioural observa-
Tachi tionsduringday and nightperiodsindicatethatone ant
gall
polyphylla colony is unable to occupy more than one host tree.
Characteristically,each leaf, with a single domatium,
Fig. 1. Schematicrepresentationof thecompoundleavesof containsa variable numberof workersand immature
Tachigalimyrmecophila and Tachigalipolyphylla.Pseudomyr- ants as well as alates, male and female. One to some
mex concolornestsand tendscoccidsinsidethe expanded
petioleandrachisofTachigalileaves.Someleafletsononeside queens can be normallyfoundclumpedin a singleleaf
ofeachleafare notshown. domatium.Pseudomyrmex concoloractivelypatrolsthe
leaves of Tachigali,protectingthe plants againstherb-
ivores(Fonseca 1991). However,theworkersdo noteat
thereis a strongrelationshipbetweenpreferrednestsite these insects.The only recordedfood of P. concoloris
and mature colony size. Although not explicit,these the honeydewand the bodies of the smallcoccids Cate-
data suggestthatnestingspace can limitthe colonysize nococcussp. thattheytendinsidethe domatia. Pseudo-
of those species withspecialized nest requirements. myrmexconcolor occurs mainly in young plants. In
The life historyof the stingingant Pseudomyrmex most cases, only one ant colony is foundoccupyinga
concolor(F. Smith)is closelyintegratedwithitslegumi- tree,thecolonybeingspreadover all thedomatiaof the
nous tree host, Tachigali;itsnestsare exclusivelyinside tree. However, when the tree growstallerthisant spe-
leaf rachisdomatia; its territorycomprisesroughlythe cies is replacedby anotherant species, thusbeginninga
whole tree; and most food seems to be providedby its successionalprocess thatinvolvesat least two Pseudo-
associated coccids Catenococcussp., a Tachigaliherb- myrmexand six Azteca species in this region. Then,
ivore. In thispaper I analyse the colonysize and struc- duringthetransition periodtwo antcolonies can coexist
tureof Pseudomyrmexconcolorin two species of myr- in a conflicting situationin a singlehost plant (Fonseca
mecophyticTachigaliwithdistinctleaf morphology.Us- 1991).
ing intraspecific comparisons I can discriminate
between factorslimitingthe ant colony size; specific
hypothesesbeing: a) food,b) territory size, and c) nest-
Colonycollection
ing space.
Young plants of Tachigalimyrmecophilaand T. poly-
phylla occupied by Pseudomyrmexconcolor were lo-
cated. All saplings used ranged from0.5 to 2.5 m in
height and were unbranched. For each species, the
Materialand methods plantswere groupedaccordingto the numberof leaves,
The plants were collected in the Cabo Frio reserve,a from4 to 11. An individualfromeach groupwas chosen
continuous1000 ha reserveof TerraFirmeforest(sensu randomly,thusforeach speciesthereare eightindividu-
Pires and Prance 1985) about 100 km northof Manaus, als withincreasingnumbersof leaves. As I was unable
Amazonas (2024'S, 59052'W). This reserveis linkedto to finda plantof Tachigalimyrmecophila with11 leaves,
the Biological Dynamics of Forest FragmentProject it was replaced by an individualwith 12 leaves. This
(InstitutoNacional de Pesquisas do Amazonas/Smith- procedurepermittedthe selectionof a desiredvariation
sonian Institution),being a controlplot of undisturbed both in morphologicaltraits of Tachigali and in ant
rainforest.The vegetationhas a variable canopy about colonysize and structure.
30-40 m and the Arecaceae provides a predominant Between8 and 10 October 1988,I collectedintegrally
understoreycomponent.The regionalclimateis classi- all ant colonies of Pseudomyrmexconcolor in order to

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 y= 1.347x- 3,264 G.L.) was introducedinto each domatiumforpreserv-
30,000 ing the internalmaterial.Most collectionswere made
afterrainfallwhenthe workerswere insidethe domatia
to minimizethe loss of workers.Workersoutside the
domatia were countedand added to the total inside.
so20,000 Each domatiumwas dissectedand thecontentsexam-
co 0 ined under a dissectingmicroscope (10-30 x). The
numberof workers,pupae, larvae, eggs, queens, and
C alate males and females was recorded,as well as the
10,000 y = 0.390x+ 235
numberof coccids, Catenococcussp.
0 0~~~~~~
0
0 5,000 10,000 15,000 20,000 25,000 Plant morphology
Leaf area (cm2) The numberof leaves and leafletson each individual
betweendomatiaspace and leafarea in
Fig. 2. Relationship Tachigali were counted. Each leaf was tagged, de-
Tachigalimyrmecophila(closed circles,n = 8) and Tachigali tached, pressedand dried. The leaf area was estimated
polyphylla(open circles,n = 8). by a Delta T Area Meter (Delta T Devices, Burwell,
Cambridge,U.K.) with 1 cm2 precision. Each doma-
tium was put in a plastic bag. In the laboratory,the
describetheircolonystructure. Adhesiveplasticwas domatia were longitudinallydissected and the length
putovertheentrance ofeverydomatium toprevent the and largestwidthwere measuredbya rulerwith0.5 mm
workersgettingout. Then, an alcoholic solution(70% precision. As there is no change in the shape of the

Table 1. Information
on completelydissectedplantsof Tachigalimyrmecophila (n = 8) and Tachigalipolyphylla(n = 8) occupied
by the ant Pseudomyrmex concolor.Each rowis an independentplant. Q is thenumberof queens. F and M are numberof alated
femalesand males, respectively.

Plant Number Number Leaf Domatia Number Number No. No. No. Q F-M
code of of area space of of of of of
leaves leaflets (cm2) (mm2) coccids workers pupae larvae eggs

Tachigalimyrmecophile
1 4 16 2268 699 30 59 23 40 76 2 0-0
2 5 31 4315 2704 143 334 65 110 68 2 0-0
3 6 42 8659 7936 206 466 106 362 323 1 0-0
4 7 38 4609 2631 101 118 24 128 122 2 0-0
5 8 56 12228 12860 454 737 243 1173 496 8 0-0
6 9 62 12087 15999 294 697 143 421 18 5 6-0
7 10 67 10981 8408 163 553 83 432 128 1 24-0
8 12 98 25099 30767 345 1104 199 1216 255 4 65-2

Tachigalipolyphylla
9 4 36 2894 1390 44 86 18 68 37 1 0-0
10 5 36 2258 850 30 28 8 28 55 2 0-0
11 6 55 4151 2215 50 141 43 60 92 6 0-0
12 7 53 3724 1902 76 52 33 18 98 6 0-0
13 8 100 12794 3377 50 83 16 75 110 4 10-3
14 9 77 4155 2020 71 22 15 17 96 7 0-0
15 10 170 17633 8165 365 257 67 625 241 1 2-35
16 11 133 9044 4087 635 324 101 428 236 2 0-0

Tachigalimyrmecophila
X* 7.6 51.3 10030 10250 217 509 104 485 185 3.1 12.1t
S.D.* 2.7 25.3 7183 9825 139 345 80 462 161 2.4 23.7

Tachigalipolyphylla
X* 7.5 82.5 7081 3001 165 124 37 165 121 3.6 6.3
S.D.* 2.5 48.5 5568 2330 219 111 32 230 77 2.5 13.2
* Median (X) and standarddeviation(S.D.) were calculatedby species (n = 8
plants) and are valid onlywithinthe scope of the
previouslydescribedsample procedure.t Consideringfemaleand male alates together.

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 amongthenumbers
Table2. Correlation ofdifferent stagesofPseudomyrmex
developmental coefficients
concolor.Correlation
(P) are respectively
(r) and probabilities exceptthose
belowand above thediagonal.Samplesize is 16 forall comparisons
involving P > 0.05.
alateswheren is 5. ns represents
Eggs Larvae Pupae Workers Queens Alates

Eggs 1 0.001 ns ns ns 0.005

Larvae 0.823 1 0.001 0.001 ns 0.005
Pupae 0.396 0.839 1 0.001 ns ns
Workers 0.405 0.823 0.978 1 ns ns
Queens -0.261 0.006 0.379 0.323 1 ns
Alates 0.949 0.953 0.643 0.653 -0.191 1

domatium in relation to its size, the space inside a F11,61= 40.498, P < 0.001), thisdifferencebeing highly
domatiumwas estimatedby the productof its length significant (F11,12]= 123.35, P < 0.001).
and width.

Results Colonyfoundation,growthand reproduction

Plant morphology Field observationsuggeststhatcolonies of Pseudomyr-
Tachigali myrmecophila(Tm) leaves normallyhave mex concolor are foundedby only one queen (haplo-
smaller leaflet number,larger leaflet size and larger metrosis),neverthelessthe data presentedin Table 1
domatiumspace, than leaves of Tachigalipolyphylla indicate that later on they become polygynous.Only
(Tp) withcomparable leaf length.Althoughboth spe- fourfrom16 coloniesstudied(25%) were monogynous.
cies have about the same numberof leaves and conse- The polygynouscolonies had fromtwo to eightdealate
quentlyabout the same numberof domatia (Tm = 61, queens, normallybeing clumpedinto one or a few do-
Tp = 60, each leaf has a single domatium), T. myr- matia. In two dissectedcolonies two domatia had both
mecophilaplantshave 3.4 timesmoredomatiaspace per dealate queens and a highnumberof eggs, suggesting
leaf than T. polyphylla(Tm = 1344 mm2, Tp = 400 thatin Pseudomyrmexconcolor more than one queen
mm2).The difference in leaf area is about 1.4 times(Tm may be responsiblefor egg production.Interestingly,
= 1316 cm2, Tp = 944 cm2). The distinctionin morph- the correlationbetweennumberof dealate queens and
ological traitsbetweenthe species is displayedin Fig. 2. egg productionis not significant (r = -0.261, n = 16, P
The slopes of theregressionbetweendomatiaspace and > 0.05), suggestingsome process of hierarchicaldom-
leafarea show thatT. myrmecophila (1 = 1.347,Fl1,61= inance among the queens.
197.179,P < 0.001) offers3.5 timesmorenestspace to The numberof individualsof Pseudomyrmexconco-
theantsper unitleafarea thanT. polyphylla(1 = 0.390, lor at a givenstage of developmentseems to be a good
predictorof the numberof individualsin the following
stage (Table 2). The numberof eggs is highlycorrelated
70- with the numberof larvae (r = 0.823, n = 16, P <
0.001) but not significantlycorrelatedwiththe number
60- of pupae and workers(P > 0.05). The numberof larvae
is highlycorrelatedwithnumberof pupae (r = 0.839, n
iCis50- y=0.194x- 5.306 = 16, P < 0.001) and workers(r = 0.823, n = 16, P <
A-,40- 0.001). The numberof pupae is highlycorrelatedwith
0 the numberof workers(r = 0.978, n = 16, P < 0.001).
30- In Tachigalimyrmecophila the numberof eggs is only
significantlydeterminedby the numberof coccids (r2 =
20 -
z; 0.523, n = 8, P < 0.05). The determination coefficient
withboth leaf area (r2 = 0.262, n = 8, P > 0.05) and
10 - domatia space (r2 = 0.209, n = 8,' P > 0.05) are not
0- significant.In T. polyphyllathe numberof eggs is well
0- ll l l I
determinedbythenumberofcoccids(r2= 0.812, n = 8,
0 100 200 300 400 500 P < 0.001), leaf area (r2 = 0.610, n = 8, P < 0.05) and
Number of eggs domatia space (r2 = 0.760, n = 8, P < 0.005). A step-
Fig. 3. Relationshipbetweennumberof alates and numberof wise regression(Sokal and Rohlf 1981) was applied to
eggs of reproductivelyactivePseudomyrmexconcolorcolonies the pooled data, as a test to discriminatethe most
(n = 5). importantvariable to explain the egg productionin

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 Pseudomyrmexconcolor colonies, using four as F-to-
1,200 A * y = 2.106x+ 51.449 enter.Only coccidsfittedthemodel (IP= 0.471, F[1141 =
1,000 - 11.306, P < 0.01), leaf area (F = 0.457) and domatia
space (F = 0.275) being kept out of the model. This
800- suggeststhat a simple mechanismassociated withthe
o queens' feedingstatus can controlthe rate of colony
4 600- growthof P. concolor.
The numberof alates in a maturecolonyof Pseudo-
" 400 -y =0.466x + 47.233
myrmexconcolor is highlycorrelatedwiththe number
of eggs (r = 0.949, n = 5, P < 0.005, Fig. 3). The
z0 200 -
regressionline suggeststhat when the numberof eggs
accumulatedin a colonyin a giventime is higherthan
0 30, about 20% of the ants produced by the colonywill
be alates. The numberof alates is not correlatedwith
0 100 200 300 400 500 600 the numberof dealate queens (r = -0.191, n = 5, P >
Numberof coccids 0.05).
The sex ratio of the alates withina colony can be
highlyskewed to eithermale or female (Table 1). Al-
1,200- B thoughfemalebias was recordedonlyin Tachigalimyr-
mecophila,and male bias in T. polyphylla,thisis prob-
1,000- ably an indirecteffectof differencesin colonysize and
maturity.Althoughfewdata are available theysuggest
"U 800 y= 0.046x + 48.438 that largercolonies have a bias forfemale production
0~~~~~~ whilesmall colonies produce more males thanfemales.
4-- 60.0 -
600

400 -/
200 -
4 X ? y=0.012x + 36.871
Ant colonysize
200-
The size of the colonies of Pseudomyrmexconcolor
occupyingTachigalimyrmecophilais largerthan those
O 10,000 15,000 20,000 25,000
inhabitingT. polyphyllawitha comparablenumberof
5,000
leaves (Table 1). T. myrmecophilacolonies have on
Leaf area (cm) average 2.6 timesmore workersper domatium(Tm =
1,200- C 66.7, Tp = 25.4), 2.9 timesmorepupae (Tm = 13.7, Tp
= 4.7) and 2.9 more larvae (Tm = 63.6, Tp = 22.0),
than the colonies on T. polyphylla.Nevertheless,the
1,000 -
average numberof eggs per domatiumis only 1.5 times
' biggerin T. myrmecophila colonies (Tm = 24.3, Tp =
800 - y=0.033x + 167.200
0 S 16.1). Also, the average numberof coccids per doma-
4
tiumis 1.3 timeshigherin T. myrmecophila (28.5) than
600- in T. polyphylla(22.0).

400w+ < < y=0.035x + 19.702

200- Limitingfactorforant colonysize

0 5,000 10,000 15,000 20,000 25,00 30,000
Domatiaspace (mm2)
Fig. 4. Relationshipsbetween numberof workersof Pseudo-
myrmexconcolorand A) coccids, B) leaf area and C) domatia
space in Tachigalimyrmecophila(closed circles,n = 8) and
Tachigalipolyphylla(open circles,n = 8).
The numberof workersof Pseudomyrmexconcolorin-
habitingTachigalimyrmecophilais highlydetermined
bythedomatiaspace (r2= 0.901, n = 8, P < 0.001), leaf
area (r2 = 0.914, n = 8, P < 0.001), and numberof
coccids (r2 = 0.723, n = 8, P < 0.005). For T. poly-
phylla,the determinationcoefficients betweennumber
of workersand bothdomatiaspace (r2= 0.536, n = 8, P
< 0.05) and coccids (r2 = 0.851, n = 8, P < 0.001) are
butwithleaf area thecoefficient
significant, is onlynear
thesignificantlevel (r2= 0.384, n = 8, 0.10 <P ' 0.05).
The generallyhigh determinationcoefficientsof the

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 700- A The slope of the regressionbetweenworkersand leaf
A0 area for Tachigalimyrmecophila(1 = 0.046, F11,61=
600 - y = 0.060x - 13.808 63.964, P < 0.001) is about 3.7 timeshigherthanforT.
polyphylla(a = 0.012, F[l,6] = 3.733, P > 0.05), this
U 500- y =.O10x + 110.200
0
difference beinghighlysignificant (F[1,121 = 40.753, P <
0.001, Fig. 4B). Again, there is anotherfactorwhich
2 400- constrainsthe numberof workersin Tachigali.
- Thereareno significant
differences
(F11121= 0. 000, P
,8300 > 0.05) betweenthe slopes of the regressionsbetween
Z 200- numberof workersand domatiaspace in Tachigalimyr-
mecophila(1 = 0.033, F1161 = 54.794, P < 0.001) and T.
100 p polyphylla(13 = 6.919, P < 0.05, Fig. 4C).
= 0.035, F[1161
0
This means thatindependently of the hostplantspecies
-
the same colony size is predictedif a given domatia
0 5,000 10,00015,00020,00025,00030,000 space is available forthe colonyof Pseudomyrmex con-
Domatiaspace(mm2) color.
As an additional statisticalapproach a stepwise re-
gressionwas used withthepooled data fromboth Tachi-
gali species using workersas the dependentvariable,
700 - and domatiaspace, leafarea and coccidsas independent
0
variablesin the fullmodel. The F-to-enterwas 4.0. It is
600 -
expectedthatonlythe variablesrelevantto explainthe
numberof workersin both species will be significant.
C4

500 - )
oal *00 y= 0.020x+ 20.112 Onlydomatiaspace fittedthemodel (1 = 0.038, F[11141=
0400 100.319,P < 0.001), leaf area (F = 0.597) and coccids
'4-4
(F = 3.111) being kept out of the model. Therefore,
300- both these analyses suggest that in the Pseudomyr-
3200- I f y = 0.014x+ 76.068 mexlTachigalisystemnestingspace is the most impor-
200- tantfactorcontrollingant colonysize.

100-

0 - I I
0 5,000 10,000 15,000 20,000 25,000
Leafarea(cm)
Fig.5. Relationshipsbetween number ofcoccidsandA) doma-
tia space and B) leafarea in Tachigali
myrmecophila (closed
circles,n = 8) and Tachigali
polyphylla(opencircles,n = 8).
associations
describedaboveseemtobe theresultofthe
generaltrendof all variablesto increasewiththein-
crease in plant size.
The intraspecific comparisonbetween the linear re-
gressionsof colony size of Pseudomyrmexconcolorin-
habiting Tachigali myrmecophilaand T. polyphylla
sheds lighton the factorsaffectingant colonysize. Al-
thoughhigh determinationcoefficientsbetween work-
ers and coccids were foundforcolonies occupyingboth
Tachigali species, the slope of the regressionfor T.
myrmecophila(1 = 2.106, F[16] = 15.645, P < 0.01) is
about 4.5 times higherthan for T. polyphylla(a =
0.466, F1161= 34.147, P < 0.001), thisdifferencebeing
highlysignificant (F1112] = 33.106, P < 0.001, Fig. 4A).
This means that the same numberof coccids predicts
differentnumbersof workersof P. concolor according
to the hostplantspecies. Thus, a factorotherthanfood
mustbe limitingant colonysize.
I
Limitingfactorforcoccids
The same type of intraspecificcomparisonsas were
made above can be performedto ask what factoris
controllingthe numberof coccids occupyingeach spe-
cies of Tachigali.In T. myrmecophilathere are good
determination coefficients betweenthe numberof coc-
cids and both domatia space (r2 = 0.542, n = 8, P <
0.05) and leaf area (r2 = 0.527, n = 8, P < 0.05). In T.
polyphylla the determinationcoefficientsare not so
good foreitherdomatiaspace (r2= 0.401, n = 8, 0.05 '
P ' 0.10) or leaf area (r2 = 0.270, n = 8, 0.20 ? P '
0.10).
The slope of the regressionbetweencoccids and do-
matiaspace forTachigalimyrmecophila (1 = 0.010, F[1,61
= 7.091, P < 0.05) is about 5.7 timeslower than that
presentedby T. polyphylla(1 = 0.060, F[161 = 4.015,
0.05 ' P ' 0.10), thisdifference beinghighlysignificant
(F[1,121= 14.727,P < 0.01, Fig. 5A). So, thereis another
factorconstrainingthe numberof coccids in Tachigali.
The relationshipbetweennumberof coccids and num-
ber of workerswas analysedpreviously,the numberof
coccidsper workerbeingdifferent forthe two Tachigali
species (Fig. 4A).
There is no significant difference(F11121 = 0.615, P >
0.05) between the slopes of the regressionsbetween
numberof coccidsand leaf area between Tachigalimyr-

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mecophila(a = 0.014, F[1,6] = 6.673, P < 0.05) and T.
polyphylla(f=0.020, F1161=2.220, P > 0.05, Fig. SB).
The same leaf area predictsthe same numberof coccids
in both Tachigalispecies. Therefore,leaf area seems to
controlthe numberof coccids.
A stepwiseregressionwas applied to thepooled data.
Only workersfittedthe model (I = 0.346, F[1,14] =
8.358, P < 0.05), leaf area (F = 0.688) and domatia
space (F = 0.665) beingkeptout of themodel. Thus, by
this analysis the predatoryactivityof Pseudomyrmex
concolorseems to controlthe totalnumberof coccidsin
Tachigalidomatia.
Discussion
The upper limitof the colony size of Pseudomyrmex
concoloris constrainedby the space available fornest-
ing activitiesofferedby the leaf domatia of Tachigali.
However, the three-trophic level interactionbetween
ant, coccid and myrmecophyte seems to be the key
factorin theunderstanding oftheantcolonygrowthand
maturation.P. concolor feeds upon the coccid colony
which feeds on the phloem sap of Tachigali. Conse-
quently,the energyand nutrients consumedby the ants
are producedbythephotosynthetic activityof Tachigali.
Plantsgrowingin a productiveenvironment(e.g. good
lightconditions)and experiencinga low level of herb-
ivoryare able to maintaina highproductionof coccids
and consequentlya highrate of egg and alate produc-
tion.
If the ants do not patrol the leaves and drive off
herbivores,the photosyntheticrate of the plant will
decrease and so willthe productionof coccids. Then, if
an antcolonypermitstheplantto be highlydamagedby
herbivores,the ant colony would become food limited
and thecoccid colonyoverexploited.As a result,theant
colonywould not reach the maximumcolony size per-
mittedby the host and would probablypresenta lower
fitness,as measuredby the numberof alates.
Pseudomyrmexconcolor is a very aggressive ant
whichbitesand stingsmostof the insectherbivoresthat
itfindson thehostplant.However,thispatrollingbeha-
viouris not associatedwithforagingbecause the poten-
tial preyare thrownoffthe plant. How can such beha-
viour evolve? The three-trophic level frameworkpro-
posed above seems to shed lighton the evolutionof the
aggressivenessin ant-plantsystemswherethe plantsdo
not offerdirectlyany food rewardfor the ants. Ants
presentinga higher efficiencyof patrollingactivity
against herbivores,and presumablycompetitors(Da-
vidsonet al. 1989), were providedindirectly withhigher
food availabilityand were able to presenthighercolony
growthand reproductionthancoloniespresentinga tim-
id behaviour.
The phylogenyof the pseudomyrmecineants con-
firmsthe view that they repeatedlyhave developed
OIKOS 67:3 (1993)
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obligateassociationswithmyrmecophytes (Ward 1991).
As Janzen (1966) stated, increased aggressiveness
seems to be a convergentbehaviouraltraitamongPseu-
domyrmexplant-antsbecause most free-livingspecies
show very timid behaviour. Outstandinglyaggressive
behaviourcan be foundin Pseudomyrmexfromdiffer-
ent lineages associated withAcacia, Tachigaliand Tri-
plaris (Benson 1985). In cases where the ant feeds di-
rectlyon the plant products (e.g. Beltian bodies of
Acacia) thereis a directlinkagebetweenthe plantpho-
tosyntheticrate and the ant colonyfitness.
foragingand space-limitedcolony
Host-restricted
size
The ratiobetweenenergyintake and the timespentto
retrievethe food is an importantvariablein manycen-
tral place foragingmodels (Brown and Orians 1970,
Holldobler and Lumsden 1980). Most of the ants nest-
ing in myrmecophytes stronglymaximizethisratio be-
cause theirnestingand feedingsites are sometimesvir-
tually the same. Host-restricted foragingis a general
rule among dominantants associated with myrmeco-
phytes.In a Peruvianrainforest,six of the numerically
dominantant species occurringin eightmyrmecophytes
foragedonlyon the hostsurface(Davidson et al. 1989).
In about 15 myrmecophytes occurringin the Cabo Frio
reservemy observationscorroboratethis ant foraging
pattern. Although many ants are generalistsin their
food habits, plant-antsusually tend coccids inside do-
matia.These coccidsrepresenta regularfood sourcefor
the ants, acting as a bufferfor colony growthduring
decreasingfood productivity.Pseudomyrmexconcolor
seems to be an extremecase, feedingits colony almost
entirelywith the coccids Catenococcussp., and these
ants are never foundoffthe host plants except during
defensiveevents when they fall down in order to re-
move eitherantcompetitors, or phytophagousor preda-
toryinsects.
If foodwerethelimitingfactoron the developmentof
plant-antcolonies,whatwould explainthislimitationin
territoryarea? The nesting space-limitedhypothesis
presentedin this paper can explain these facts satis-
factorily.If the colonysize is space-limitedand the host
offersdirectlyor indirectly enoughfood to its partners,
there is no reason to extend the territory beyond the
plant boundary.As a corollary,ants that are able to
escape the space limitationare not expected to exhibit
host-restricted foraging. Davidson et al. (1989) re-
cordedthreeAzteca species thatare able to buildcarton
nestsoutsidethe host domatia. As expected,the forag-
ing areas of all thesespecies were not restrictedto their
host. Furthermore, Crematogaster cf. victimaoccupying
Maieta guianensisand Clidemia heterophylla(Melasto-
mataceae) was considered"unusual as a commonplant-
ant not restrictedto its host" (Davidson et al. 1989). In
the Cabo Frio reserve,Maieta guianensisoccurs in ag-
479
 Cost (e.g. by coccids) for productionof most of the food
Maximum resourceobtainedby the ant colony. Assumingthatthe
net requirementof energyand nutrientsforthe production
benefit and maintenanceof a workeris uniform,itis reasonable
to suppose that to supportcolonies of larger size the
plant needs to allocate a directlyproportionalamount
of resources,the cost growingcontinuously(Fig. 6).
The simple presence of ants has been demonstrated
I InefI to decrease herbivorousinsect activityin several ant-
defencemutualisms(Way 1963, Bentley 1977, Beattie
1986). The higherthe densityof patrollingworkersthe
MutualismParasitism higherwill be the effectiveness of the plant defence.
Nevertheless,as moreworkersare added to thepatroll-
N Max ing activityon the leaf surface,the importanceof each
Colonysize individualin thesearchand aggressionagainstthe herb-
ivores becomes lower. At some stage theirpatrolling
Fig. 6. Graphicmodelofcostandbenefit to a myrmecophyte a maximumand eventuallythe
of maintainingincreasingantcolonysize. N is thecolonysize efficiencyapproaches
thatproducesthegreatest to theplant.Maxis the benefitto the host plant reaches a limit.
netbenefit
colonysizewithnullnetbenefit. The intersectionof the cost and benefitcurvesrepre-
sents the maximumant colony size in which the net
benefitis positiveand, by definition,mutualisticinter-
gregatedpatchesproducedby asexual reproductionand action is possible (Fig. 6). If these argumentsare cor-
an ant colony can be spread over several stemsin the rect,some colonysizes presenta negativenetbenefitto
same clone. So, the trailson the forestfloorcannotbe the plants,the ants playinga parasiticrole in the rela-
consideredan exceptionto the host-restricted rule. In- tionship. The almost complete absence of patrolling
terestingly,Davidson et al. (1989) had no directevi- activityby some ant species inhabitingAcacia, and the
dence that Crematogastercf. victimawas foragingoff correspondingdrop in the benefitcurve,leads to their
the host plant. parasiticlifestyle(Janzen1975). Many ant-plantsoffer
Pseudomyrmex concolorand P. nigrescensare closely domatia space and othermyrmecophytic traitslater in
related species, both classified withinthe P. viduus their development(Davidson and Fisher 1991). This
group (P. S. Ward, 1991, pers. comm.). Both species suggeststhatant-plantseedlingsare delayingthe devel-
inhabitTachigaliat mystudysite,butP. concoloroccurs opmentof myrmecophytic traitsuntila size when they
onlyin small treesup to 7 m, whileP. nigrescensoccurs are able to maintainthecostof a biggerand efficient ant
mainlyon mediumsized trees but also occupies large colony.
canopy trees (Fonseca 1991). While colonies of P. con- Accordingto the model, thereis a colonysize where
color are relativelysmall, the colonies of P. nigrescens thenetbenefitreachesa maximumand theplantshould
can be one or two orders of magnitudelarger. This presentthe best performance.In myrmecophytes, do-
suggeststhat phylogeneticconstraintsare not limiting matia are producedas modularstructures.The number
the colonysize of Pseudomyrmex.The absence of phy- of domatiaas well as theirsize willdefinethetotalspace
logenetic constraintson mature colony size was sug- available to be occupied by the ants. If ants are space-
gested at a larger taxonomicscale by Holldobler and limitedthe controlof these variableswould permitthe
Wilson (1991). Furthermore,Janzen (1973) has esti- plantto manipulatethe colonysize. In myrmecophytic
mated thatonly one colonyof the polygynousPseudo- Tachigalithereis alwaysone domatiumper leaf,but the
myrmexveneficamay contain 1.8-3.6 millionworkers size of the domatia seems to be species specific. In
spread over hundreds of acacias. As Janzen (1973) Tachigalitheratioof domatiaspace to leafarea is highly
pointedout, "[the ant colony]size is set by how large a uniformand is probablytheresultof a simpleallometric
standof acacia can growin the face of competitionwith rule. Nevertheless,this ratio can be visualized as the
otherplants",suggestingthatalthoughthisoutstanding relationshipbetweeninvestmentin myrmecophytic de-
ant species has broken the boundaryof an individual fenceand the amountof tissueto be defended.If thisis
host plant,it could not escape the limitimposedby the the case, Tachigali myrmecophilais investingabout
overall nestingsite. three times more in myrmecophytic defence than T.
polyphylla(Fig. 2). This differencein ant defenceallo-
cation could be expected if T. myrmecophilaleaves
The plant's pointof view suffereithera higherherbivorypressureor a smaller
allocation in chemical defences than T. polyphylla
How does colony size affectthe plant performance? leaves.
Host plants are generallyresponsible either directly
(e.g. by Mullerian and Beltian bodies) or indirectly

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480

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 weaver ant Oecophyllalonginodathatbindsleaves into
Consequencesof space limitationforthe ant
tightnest compartmentsusuallyconsistsof more than
community 500000 individuals.It is suggestedthat in the tropics
ofthewettropical
In thecomplexenvironment rainfor- thesespecies are actuallyexceptionsto a generalruleof
estmanysitesbelowandabovegroundare availableas nestingspace-limitedant species.
antnestingsites:dead matter, hollowand hollowable
live stemsand manydiversestructures of theplants. Acknowledgements - I am especially indebted to W. W. Ben-
colonies in sonwhoinitially introduced me to the ant-plant system. I am
Nevertheless, only appropriate nesting sites extremely gratefulforthefieldassistance ofG. Moreira.S. M.
willbe successfulandtheability to findthemshouldbe Bezerragenerously aidedmeinthelaboratory. The useofthe
rewardedbynaturalselection.The evolutionary capa- DeltaT AreaMeterwaskindly facilitatedbyM. T. F. Piedade.
bilityto nestin a completely new micro-habitat has I thankC. R. Huxley,W. D. Hamilton, P. S. de Oliveira,P. S.
evolvedmanytimesin the tropicsand in somecases Ward and M. A. W. Pachecoforcomments
manuscripts.
on the earlier
Also,I thankG. GanadeandJ.Johnfora contin-
resultsin a higherfitnessassociatedwiththisenemy- uedexchange ofideas.Thisstudy wassupported inpartbythe
freeenvironment. I haveobservedqueensof Pseudo- WorldWildlife Fund,theInstituto Nacionalde Pesquisasdo
myrmex concolorbeingkilledby bothopportunisticAmazonas(INPA),andtheSmithsonian Institution andrepre-
spidersandforaging Crematogaster ants.Saplingsofthe sents publication 95 intheBiologicalDynamicofForestFrag-
mentsProjecttechnical series.Thisworkwas also supported
ant-plant Cecropiafrequently containnumerousinci- bya CNPq studentship (200140/91-4).
pientAztecaant colonies.Duringthe plantdevelop-
mentonlyonecolonysurvives, themaincauseofqueen
mortality being parasitism(Wheeler1942, Longino
1991).ThebroodoftheantPachycondyla luteolaseems
to be particularly
susceptible to hymenopteran parasit-
oids becauseof itsnonclaustralbehaviour(Davidson References
and Fisher1991).The solitary alatequeenis primarily Beattie, A. J. 1986. The
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