Table Of ContentReference: Biol. Bull. 202: 289-295. (June 2002)
Scaling in Nests of a Social Wasp:
A
Property of the Social Group
ROBERT L. JEANNE* AND ANDREW M. BOUWMA
Department ofEntomology, University ofWisconsin, 1630 Linden Drive, Madison, Wisconsin 53706
Abstract. The numbers of brood cells in nests built by their lifetimes. That is, every individual in the colony pos-
founding swarms of the Neotropical social wasp Polybia sesses the full repertory of acts required to build the nest.
occidentalis closely correlate with the numbers ofwasps in Thus, even the most complex nests of colonial species
the swarms. We analyzed nests of different sizes to deter- could, in principle, be constructed by a solitary individual
mine how they scale with respect to the allocation ofbrood working alone, given enough time. To the extent that this is
cells among combs. Three patterns were evident: compared true of the social wasps, it argues that the broad, species-
to smaller nests, larger nests have (1) more combs and (2) typical form ofthe nest does not depend on properties ofthe
larger combs; and (3) among nests containing the same group or on processes such as self-organization, but is
numberofcombs, the lasttwocombsdiverge in relative size simply the result ofthe additive contributions of individual
as nest size increases. Taken together, these results suggest actions by individual actors. In this view, the construction
that members ofa swarm somehow "know" the size of the process is directed by a mechanism in which builders re-
swarm they are in. This information feedsback to individual spond to stimuli arising from the structure of the nest.
builders, which quantitatively modulate their responses to Interactions among builders are only indirect, mediated by
stigmergic cues in ways that result in the nest-size-scaled the structure they are cooperating to build, a mechanism
allocation of brood cells among combs. The patterns also referredtoas stigmergy (Grasse, 1959; Theraulazand Bona-
suggest that swarms fine-tune the final size oftheir nests by beau, 1995; Camazine el ai. 2001).
making corrections as they build. But are there any patterns in the nest of a social species
that are under the more direct influence ofthe social group?
Introduction Here we provide evidence that the answer is yes. We show
for a swarm-founding social wasp, Polybia occidentalis
The process ofnest construction by a social wasp colony (Olivier), that nests of different sizes scale in ways that
does not differ fundamentally from nest construction by a point to a quantitative modulation of the building rules in
solitary wasp. In each case individuals construct the nest by response to feedback about the size of the swarm.
executing a series ofdiscrete innate building acts. Each act
adds to the nest one new load of material, oriented in
Nest Construction in Polybia
response to cues intrinsic and extrinsic to the nest. As faras
we know, in no social insect species do individual workers Polybia occidentalis is a Neotropical wasp whose nesting
specialize only in certain kinds of building activity over behavior has been described in some detail (Forsyth, 1978;
Jeanne. 1986, 1996). Colony-founding swarms comprise a
*To whom correspondence should be addressed. E-mail: jeanne@ small number ofqueens and a large number ofworkers. As
a swarm arrives at the nest site it has chosen, a few workers
entomology.wisc.edu
This paper was originally presented at a workshop titled The Limits In immediately begin constructing the first downward-ori-
Self-OrganizationinBiologicalSystems.Theworkshop,whichwasheldat ented, hexagonal cells. These are attached directly to the
the J. Erik Jonsson Center ofthe National Academy ofSciences. Woods substrate, typically a twig. As more cells are added radially,
Hole, Massachusetts,from 11-13 May 2001,was sponsoredbytheCenter the developing comb takes on a discoid form, extending
LfoarboArdavtoarnyc,edanSdtufduinedsedinbtyhethSepaNcaetiLoinfaelSAceireonncaeustiatcsthaendMaSrpianceeBAiodlmoigniicsa-l freely from both sides ofthe twig. As the comb grows, there
tration under Cooperative Agreement NCC 2-896. is space for increasing numbers of workers to become
289
290 R L. JEANNE AND A. M. BOUWMA
engaged in building. Meanwhile, the queens begin laying
eggs in the cells.
When the first comb reaches a certain size, the builders'
behavior makes a qualitative shift (qualitative stigmergy;
Camazine et ai, 2001). Instead of adding more cells to the
edges ofthe comb, workers begin extending the outer walls
ofthe peripheral cells downward and outward to initiate the
envelope, starting at the back and sides ofthe comb. As this
sheet grows, it is warped toward the center to form a
domelike covering about 2 cm below the comb (Fig. 1A).
The envelope is not completely closed, however; a 1-cm
opening is left in the front to provide an entrance to the
comb. Then in the reverse qualitative shift, the second comb
is immediately begun, the walls of its cells being drawn
downward from the lower surface of the envelope just
completed. This comb is expanded from the center(bottom)
ofthe supporting envelope outward toward its margins (Fig.
IB). A new envelope is constructed over it in the same
manneras the first. Then the nextcomb isbegun in the same
way. The alternation between construction of combs and
envelopes continues until the nest is large enough to house
the adult wasps of the swarm and the brood they will rear.
The entire construction process typically takes a week to 10
days. The nest remains at this size for many weeks or
months; thereafter, enlargement occurs episodically (Wen-
zel, 1993; AMB, unpubl. data).
Thus the nests ofP. occidentalis are modular, each mod-
ule consisting ofa comb and its envelope. Swarms work in
complete modules: each comb + envelope module is con-
structed to its final size before the next one is begun, and it
is rare for a founding swarm, once it starts a new comb, to
leave it half-finished or uncovered (RLJ and AMB. pers.
obs.).
P. occidentalis swarms vary widely in size, yet each is
able to construct its nest with a number of cells that corre-
lates closely with the number of wasps in the founding
group (Forsyth, 1978; Jeanne and Nordheim, 1996). A sim-
ilar pattern is seen among founding groups of Polish's
(Wenzel, 1996). The size ofthe nest built by the swarm may
cweolllonyopotuitmpiuzteisthmeaxtirmaidze-eodf.fOonf tohpepoosnienhgancdo,stisftshuecshwathramt vineslFiodipege,urciosenns1te.raurciNtniegosntc.somTophtleeIte'inoovlnxe.hlioTapheienc-coruvilemcrntioinfigldnciarokumnbmdae3tr.erwciohanolssteirsuccretelicloesnn.atrley(Ava)idsidEbenl-de
builds too few cells, it will not have the space to house the carton, still wet. As more material is added to the envelope edge, the
brood it is capable of rearing, and the subsequent rate of openingwillbeconstrictedtoformthenewentrancetothenest,justbelow
colony growth will be limited. On the otherhand, ifthe nest the current entrance (line). The greatest widthofthe nest is about 6.5 cm.
is much larger than required to house the brood population, t(hBelsCpoacmebbceotnwseterunctcioomn,bf2roanntadlivtsieewn.veTlhoepe,neswthiecnhtrafnocrem,sctehnetebro,totpoemnsofitnhteo
forager mortality may be high due to the extra foraging nest. Comb 3. its cells exposed on the lower surface of the envelope
demands for nest material, leaving too few workers to rear covering comb 2, is expanding outward with the addition of new cells.
the brood efficiently (O'Donnell and Jeanne, 1992). Whenthecellsreachtheanglededgeoftheenvelope,theirouterwallswill
The form the nest takes is a function of two sets of heextendeddownwardandoutwardtoinitiateenvelope3,beginningat the
hack of the nest. Note the campanulate shape of the nest. The giealest
decision processes engaged in by individual builders in the width ofthe nest is about 5 cm.
colony. One is the decision by a worker as to what kind of
building act to engage in. P. occidentalis workers perform reinforcement of the upper nest walls (Jeanne. 19S6). The
three primary kinds of building acts: brood-cell-wall con- second set ofprocesses has to do with the orientation ofthe
struction, envelope construction, and surface thickening for material being added to the nest during a particular kind of
SCALING IN NESTS OF A SOCIAL WASP 291
Table 1
Descriptive statisticsfurtit? Polybia occidentalis colonies usedin the
study
Component
292 R. L. JEANNE AND A. M. BOUWMA
500
A. Comb#1 B. Comb #2
120 400 -
300 -
80 -
200 -
40
100
o
I o o
o
o
C 800 1200
C. Comb #3 D. Comb #4
"o5
600 -
800 -
400
400
200 -
500 1000 1500 2000 2500 3000 500 1000 1500 2000 2500 3000
Nest size, C,
Figure4. Distributionsofsizesofindividualcombsasafunctionofoverallnestsize.Eachgraphplotssizesof
combsofthe indicatedordinalcombnumber. (A)Comb 1;(B)Comb2;(C)Comb3;(D)Comb4. Withinagraph,
eachplotisofnestsofthesametotalcombnumber,in:solidtriangles:in = 2(i.e., 2-combnests);opentriangles:in =
3; solidcircles: m = 4; opencircles: in = 5. Forall regression lines shown, P < 0.001 (regression forcomb I in
2-combnests:P = 0.11).Solidlinesrepresentlinearregressionequationsfornestsofthesamecombnumber,m:(A)
m = 2: v = 16.76 + 0.17.v.f = 0.37;m = 3:y = 6.87 + 0.08*,r = 0.58;in = 4: v = -5.07 + 0.05*,r = 0.60;
HI = 5: v = -0.08 + 0.03.V,r = 0.55. (B)m = 2: v = -16.76 + 0.83.V,r = 0.93;m = 3: v = 7.71 + 0.30*.r =
0.9l;m = 4:y= -3.91 + 0.17.x,r =0.77;m = 5:y= 15.31 + 0.09.V,r = 0.66.(C)m = 3:y = -14.58 + 0.62*,
r = 0.96;m =4:v = 42.55 + 0.30.V.r = 0.96;m = 5:v = -38.64 + 0.2Zv.r = 0.95.(D)m =4:y= -33.57 +
0.48.V.r = 0.93;in = 5:y = 84.35 + 0.28.x, r = 0.90. Dashedlinesrepresentfitted linearregressionequationsfor
alldataineachgraph(i.e..combiforallnests):(A)Comb 1:y = 43.5 + O.Ol.v,r = .25,n = 78. (B)Comb2:y =
133.1 + 0.05.V, r = 0.43,n = 78. (C)Comb3:y = 254.5 + 0.1Iv. r = 0.58.n = 70. (D)Comb4:y = 230.2 +
0.24.V, r = 0.73, n = 46. Note thatthe scaleoftheyaxis increases in the graphs from A through D.
same numberofcombs, m, (Fig. 4, solid regression lines) as tended to diverge as nest size increased (Fig. 5). Although the
well as across the set of all nests of 2-5 combs (Fig. 4. slope of only one regression differed significantly from zero
dashed regression lines). (comb 3 of4-comb nests) and the slopesofthe regression lines
for the last and the next-to-last combs differed significantly
Among nests ofm combs, the last two combs diverge in from each other only for 4-comb nests, for all four sets the
relative size as nest size increases slope ofthe regression ofcells in comb m on total cells in the
nest was positive, but that ofcomb m I was negative.
The third pattern is the least clear-cut, but is worth noting The number of combs in the nest depends on how indi-
nonetheless. Within each set of nests of a given number of viduul builders respond to the choice, "Now that the enve-
combs (m), the proportions of cells in combs m vs. m - I lope is complete overcomb i. do I initiate cells ofcomb ; +
SCALING IN NESTS OF A SOCIAL WASP 293
1 00
A. 2-comb nests 0.75 - B. 3-comb nest^s
0.75 -
0.50
050
.Q 0.25 -
025 -
O
o
21 o.oo 0.00
0O> 120 160 200 240 400 600 800
C
O
o
Q.
O 0.50
294 R. L. JEANNE AND A. M. BOUWMA
large a nest it will build, or does it make corrections as it varies little ifat all among species ofsocial wasp, except in
goes? Three observations suggest that the latter is the case. the interesting case ofthe Vespinae, where the queen builds
First, whereas the correlation between the size of combs 1 worker-sized cells, and the workers (which are smaller)
= =
and 2 is relatively strong (/ .83; n 85). the correlation build both worker- and queen-sized cells.
of comb 1 with later combs progressively weakens. The At the other extreme are species-specific rules those
ability ofcomb 1 to predict the overall nest size is not very that result in the nest architecture characteristic ofa species.
good (r = .46). Second, the amount of variance in comb In ourview, there is littleevidencethatthe resulting patterns
size that is explained by nest size increases with comb in nest structure at any of these levels are emergent prop-
number, i (Fig. 4, r values increase, A-D). Third, there is erties ofa self-organizing process. Rather, they appearto be
substantial overlap in size among nests of m and m + 1 largely the products of quantitative and qualitative stig-
combs, especially for nests of m > 2 combs (Fig. 2; Figs. mergy (Camazine et ai, 2001 ).
5B-D), suggesting that swarms adjust final nest si/e by At the intraspecific level, however, things may work
deciding whether to add a final module. The overlap is differently. The evidence we have presented clearly indi-
probably due to variation in the sizes ofthe first few combs cates that Polybia occidentalis swarms are able to allocate
built by swarms ofsimilar size. Consider, for example, two brood cells among combs so that size and number ofcombs
swarms, each of which will ultimately build a nest of 2000 scale with swarm size. What mechanism could give rise to
cells. Nestsofthis size may have fourorfivecombs (Fig. 2). this pattern? Several previous studies have suggested ways
If swarm A builds combs 1-4 smaller than average, it will that groups ofsocial insects might build their nests to a size
build a 5th comb, but this final comb will not need to be that accommodates them. One possibility is that the mass of
much bigger than comb 4 to achieve the total of 2000 cells the swarm itselfserves as a template to adjust the size ofthe
in the nest (see Fig. 5D). On the contrary, ifswarm B builds nest to the size ofthe swarm. This appears to play a role in
combs 1-3 larger than average, then it will get the 2000 construction of the two-dimensional nests of Leptothorax
cells by adding one more comb, but that comb will have to ants (Franks etul., 1992; Camazine etai, 2001 ). Swarms of
be disproportionately larger (see Fig. 5C). The nest of Metapolybia wasps build nests of single combs on a flat
swarm A is toward the low end of the size distribution of surface. A ring of"guards" is arrayed around the comb as it
5-comb nests, while that ofswarm B is toward the high end is constructed (Forsyth, 1978). If the guards are a fixed
ofthe size range of4-comb nests. The combs ofnest B will proportion of the swarm, then expanding the comb to the
average 25% largerthan those ofnest A. As Figure 5 shows, ring could produce a nest of the right size. But use of such
however, most of this average difference in proportions a template cannot explain the scaling patterns seen in P.
tends to be absorbed by the last comb. occidentalis, whose three-dimensional nests are extended
Taken together, these observations suggest that swarms into open space below a supporting twig, while the bulk of
fine-tune the final size of their nests in the later stages of the swarm remains clustered to the side on the twig.
construction. Thus, although comb I aims roughly in the A related idea is that construction stops when the nest is
direction of the ultimate nest size, the trajectory toward the large enough to house the swarm (Camazine etai, 2001 ). In
final nest size is guided en route, rather than ballistically its simplest form, this mechanism would predict that comb
following from comb 1. size would be constant across swarm size and that larger
swarms would simply build nests with more combs. It does
Conclusions not explain our observation in P. occidentalis that the scal-
ing ofthe nest to swarm size begins with the first comb and
The construction ofanestby asocial insectcolony involves continues throughout construction.
the performance of a set of behavior patterns that vary in A third possible mechanism is that cells are constructed
species-specificityandevolutionary age (Wenzel, 1996). Some to keep up with the oviposition rate of the laying queens
may be invariant across highertaxa. The use ofthe mandibles (Deleurance, 1950; Camazine et ul., 2001; but see Wenzel,
to manipulate nest material, for example, is universal among 1996). Again, this mechanism cannot be working in P.
social Hymenoptera and Isoptera and apparently pre-dates the occidentalis, because cells are built at a rate that well
evolution ofsociality in both groups. The rules by which nest outpaces the collective rate ofoviposition by the queens in
material is applied in responsetostigmergiccues fromthenest the swarm (RLJ and AMB, pers. obs.).
also vary in their taxonomic breadth. A fourth possibility is that self-organization plays a role.
At one extreme, tactile feedback via the antennae is used However, there is no evidence that the scaling of the nest
tocenterconstruction ofasharedcell wall between opposite proportions by a particular swarm is an emergent pattern
walls oftwo adjacent brood cells and to determine the size arising at the colony level from interactions among workers,
of the cells (West-Eberhard, 1969). This is an example of nor is there any apparent involvement of positive feedback
the use of the body as a template to produce the regular in the process.
hexagonal pattern ofthe comb. This building rule probably None of these mechanisms adequately explains our re-
SCALING IN NESTS OF A SOCIAL WASP 295
suits. Likewise, stigmergic cues, although important, arc through cues, of information about the size ofthe group. In
clearly insufficient alone to account for the swarm-size- response, builders subtly modulate their responsiveness to
dependent patterns we see among nests. Instead, we suggest quantitative stigmergic cues so as to yield the appropriate
the following mechanism. All three of the scaling patterns nest proportions. Although the mechanisms by which
we describe for P. occidentalis indicate that information group-size information is transferred to, perceived by, and
about group size flows from the group to the individual acted upon by individuals are unknown, there is little evi-
builders. We suggest that the quantitative rules governing dence that a self-organizing process is involved.
the details of nest size and proportions in response to
stigmergic cues are plastic and are modulated by group size. Acknowledgments
sAtlitghmoeurgghicncoutheisngusiesdyebtykP.noowcncidaebnotuatlist,hetbheuilfdoilnlgowriunlgeshyo-r We thank Kory Kramer and Peter Bouwma for helping to
pothetical example illustrates how this mechanism might collect data in Costa Rica. Carl Anderson, Jeffrey Baylis,
work. The size of a comb may be determined by a rule David Curson, Ellen Davis, and members ofthe Genes. Neu-
according to which a builder decides between adding an- rons, and Societies work group at the Santa Fe Institute pro-
other new cell at the periphery of the comb being con- vided valuable discussion and gave us feedback as our ideas
structed and beginning the envelope for that comb. The developed. Lee Clippard. Ken Howard, and Cristie Hurd
quantitative set point for such a rule apparently differs helped improve early drafts ofthe manuscript. Erik Nordheim
according to whether the builder is in a large or a small provided statistical help. Research supported by NSF grant
swarm. A possible stigmergic cue in this case is the angle of IBN95140IO to R. L. Jeanne and by the College of Agricul-
the surface of the envelope on which the cells are being tural and Life Sciences. University ofWisconsin, Madison.
built. The first cells in the comb are built in the centerofthe
envelope, that is, where the envelope's curved surface is Literature Cited
tangent to a horizontal plane, or0. Because the envelope is Boinvma, P. E., A. M. Bouwma.and R. L.Jeanne. 2000. Social wasp
domed, as the comb expands radially across the surface of swarm emigration: males stay behind. Efluil. Ecol. Evol. 12: 35-42.
the envelope, each new cell is built at a steeper angle from Camazine,S.,J.-L.Deneubourg,N.R.Franks,J.Sneyd,G.Theraulaz,
the horizontal than the previous cell (Fig. IB). Thus, the and E. Bonabeau. 2001. Self-Or,i>ani;atian in Biological Systems.
behavioral rule in thecontextofa small swarm might be, "If DelePurriancnecteo,nEU.niPvhe.rsi1t9y50P.ressS.urPrliencmeetcona.niNsJm.e de la monogynie fonctio-
the angle at which the current edge of the comb is >25, nellechez lesPollutes(Hymenopteres-Vespides). C. R. Hebd. Seance*
then begin building the envelope instead of adding another .4ai</. Sci. Paris 230: 7X2-7S4.
cell." We suggest that in a large swarm, this quantitative set Forsyth,A.B. 1978. Studiesonthebehavioralecologyofpolygynoussocial
point may be nudged up to, say, 30 in response to infor- wasps. Ph.D. dissertation. Harvard University, Cambridge. MA. 226pp.
mation about swarm size fed back to the builder from the Franks, N. R.. A. \\ilby. B. \V. Silverman, and C. Tofts. 1992. Self-
organizing nest construction in anls: sophisticated building by blind
group. This change would result in a comb's being larger bulldozing. Anim. Beha\: 44: 357-375.
when being built by a large swarm than when built by a Grasse, P.-P. 1959. La reconstruction du nid et les coordinations inter-
small swarm. Because the envelope subsequently built over individuelles chez Bellicositermes nata/ensis et Ciibitemie.i sp. La
the larger comb would also be larger, the increased size theorie de la stigmergie: essai d"interpretation du comportement des
termites constructeurs. InscctesSoc. 6: 41-83.
would propagate itselfthroughout the remaining modules of Jeanne, R. L. 1986. The organization ofwork in Polyhia occidentalis:
the nest. In other words, we are hypothesizing that infor- the costs and benefits ofspecialization in a social wasp. Behav. Ecol.
mation about group size modulates the quantitative set Sociobiol. 19: 333-341.
points of the rules of response to stigmergic cues. Jeanne, R. L. 1996. Regulation ofnest construction behaviourin Poly-
In conclusion, we see little evidence that self-organizing hia occidentalis. Anitn. Bt'hav. 52: 473-488.
Jeanne,R.L..andE.V.Nordheim. 1996. Productivityinasocialwasp:
processes play a role in nest construction in Polyhia occi- percapita output increases with swarm size. Behav. Ecol. 7: 43-48.
dentalis. Rather, construction ofthe species-typical features O'Donnell. S., and R. L. Jeanne. 1992. The effects ofcolony charac-
ofthe nest can be understood as quantitative and qualitative teristics on life span and foraging hchaxiorofindividual wasps (Poly-
stigmergic mechanisms, wherein cues from the nest struc- hia (iccidentali.\. Hymenopleia: \cspidae). Insectes Soc. 39: 73-80.
ture at each stage ofconstruction provide information to the Theraulaz, G.. and E. Bonabeau. 1995. Coordination in distributed
builders as to what building act to perform next, where to Wenzbueill,dinJ.g.WS.cie1n9c9e3.269A:pp6lSioca-toiSo8n ot the biogenetic law to behavioral
perform it. and how to orient the addition of the new ontogeny: atestusing nestarchitecture inpaperwasps.J. Eml. Bid. 6:
material. In accomplishing these tasks, individual workers 229-247.
interact only indirectly, via the structure of the nest (Cam- Wenzel, J. W. 1996. Learning, behaviour programs, and higher-level
ainzinneestetparlo.,po2r0t0i1on).sWaecchoamvpeapnryovcihdaendgeesviidnenscweatrhmatscizhea.ngWees rEOuvxlofelosurtidinonUnensintvfecProasnipstetyrru-PcWrtaeissospn,*.oOfxSPf.oolTuiulsrhi'llsa./-Pzpi.a5n8d-7M.4iJ.nWNeasttu-rEableHrihsatrodr.yeadnsd.
argue that these patterns cannot be explained by stigmergy West-Eberhard, M. J. 1969. The social biology of polistine wasps.
alone, but appearto involvedirectcommunication, nodoubt A//M. Pnhl. Mus. Zool. Univ. Mich. 140: 1-101.
