Table Of ContentHYM. RES.
J.
Vol. 19(1), 2010, pp. 4-11
Foraging Behavior and Colony Cycle of Agelaia vicina
(Hymenoptera: Vespidae; Epiponini)
Otavio a. L. de Oliveira, Fernando B. Noll, and John W. Wenzel
(OALdeO, FBN) Departamento de Zoologia e Botanica; Institute de Biociencias, Letras e Ciencias
Exatas, UNESP, Sao Jose do Rio Preto, SP, Brazil
(JWW) Department of Evolution Ecology and Organismal Biology, Ohio State University,
Columbus, OH, USA
—
Abstract. TheneotropicalAgelaia vicina has thelargestnestbuiltamongsocialw^asps,yetlittleis
knownaboutnestconstruction, growthandstructure. Inthiswork,thedevelopmentoftwonestsof
A.vicinawasfollowed.Studiesweredonethroughanalysisofimagestoestimatethegrowthofnests.
The material collected below the nests was examined to estimate colony productivity. Nests were
collected to analyze their architecture and structure. Colony cycle was similar in the two colonies.
Coloniesincreaseinsizethroughoutthedryseasonandintotherainyseason,withasuddendropin
production atthe end ofthe rainy season. The colonies doubled insize inaboutsix months.
Social w^asps are important to the study initial structure. Subsequent expansion of
of social evolution. They fall into tw^o the nest in its following stage is equally
groups according to how^ they initiate quick, building hundreds or thousands of
colonies (Jeanne 1991). In independent- cells in a few days.
founding species, one or a small group of In tropical environments, the groups
queens start the construction ofa rvew nest, most studied for foraging behavior are
w^ithout the aid of w^orkers. In sw^arm- Polistes, Mischocyttarus, and Polybia (Dap-
founding species, a new^ colony is initiated porto and Palagi 2006; Hermann and Chao
by a large group of w^orkers and one or 1984; Hmcir et al. 2007; Jha et al. 2006;
more queens. Patterns in nest construction O'Donnell and Jeanne 2002; Richter 2000).
vary. The independent-founders are char- The importance ofthesewasps is related to
acterized by continuous nest construction; how they act in a trophic network as
that is, the size of the nest increases herbivores (sugar and nectar collectors)
gradually throughout the founding and and predators (Raposo Filho and Rodri-
ergonomic stages ofthe colonycycle, and is gues 1983). Necrophorus feedinghabits are
closely correlated w^ith oviposition rate known inAgelaia and Angiopolybia (O'Don-
(Richards and Richards 1951; Wenzel nell 1995). Agelaia is very commonly found
1991). at flowers (Mechi 2005) and is among the
In contrast, some several sv^arm-found- most abundant genera in neotropical for-
ing species engage in episodic nest con- ests (Hunt et al. 2001; Silveira et al. 2005;
struction, building the nest rapidly at the Zucchi et al. 1995), indicating its ecological
beginning of the founding stage. The new^ importance.
cells are constructed faster than the queens Agelaia vicina (Saussure) has the largest
fill them with eggs. The nest is completed colony size among the social wasps. Von
rapidly in this stage (Jeanne 1991; Wenzel Ihering (1903, 1904) first offered informa-
1991), and then the nest stays static for tion on this, reportinganA. vicina colonyof
weeks or months, while the colony ex- with more than 108,000 individuals, but
pands itspopulationwithin the limits ofits colonies may exceed one million adults
VOLL-^IE 19, Xl-mber 1, 2010
(Zucchi et al. 1995). The nests are built used these squares for counting and
commonly in cavities, such as caverns or weighing nest ceUs.
tree hollows. Builtinprotected places, they In February 2007 we gathered 42 hours
lack a nest envelope, as in many other of video segments at the entrance of the
Agelaia (Huntetal. 2001;Wenzel 1991). The Pindorama nest in order to record the
nest of A. vicina is composed of vegetable departure and return of foragers. These
fibers without wax or resin. Some parts, images were studied then in slow motion.
such as the pedicels receive additional We recorded for one hour each at starting
glandular secretion as a presumed rein- times of 06h, 14h, 18h and 24h.
forcement (Wenzel 1998). Workers build To study foraging behavior, we offered
cells that form combs. During nest initia- baits of meat 15m from the nest. Arriving
tion, several combs are built separately, foragers \vere marked on the thorax with
fixedbypedicels tothe substrate (generally non-toxic ink. This allowed us to estimate
ceilings of cavities), so that the combs are round-trip times. To determine whether
parallel to the substrate. The combs are the presence of baits increases the number
then expanded and merge to form a great of workers leaving the nest, we noted the
expanse of ceUs. Besides the considerable number of marked foragers present
amount of information regarding nest throughout the day. We designated the
architecture in A. vicina, \drtually nothing start of foraging when the first forager
is kno^\TL about its biolog}^ arrived in the bait.
MATERIALS AND METHODS It is known that A. vicina discards
leftover food and the opercula of pupal
We obser\^ed t^vo nests in Sao Paulo cocoons below the nest (Zucchi et al. 1995).
state, Brazil, one in the municipalit}' of Because each operculum corresponds to an
Paulo de Faria BrazH (19'S 49=W) and the emergent adult, the number of opercula
other in Pindorama (21^S 48^W). The Paulo corresponds to the number of adults
de Faria nest was located in an abandoned produced in a period of collection. Plastic
wooden guard station, 3.5 m above the trays were put below the nests in order to
m
ground. The Pindorama nest was 2.5 coUect the discarded material (Fig. IC).
above the ground, inside a brick structure
RESULTS
inthe form of a shutto^ver inthebackyard
of an abandoned house. Xest growth was continuous during the
Images \vere captured using a digital period of obserA^ation. From the image
camera in order to measure nest gro^vth. analyses, the Paulo de Faria nest initially
The images of the Paulo de Faria nestwere had 459,143 cells, which increased to
captured from Xovember 2005 to April approximately956,340 cells over the course
2006, those of the Pindorama nest from of six months of obser\'ations, an increase
June 2006 to Februar}^ 2007. Xest growth of 108°0. After nest collection, it ^veighed
was estimated bv Axiovision, software that 13.8 kg with cells (or combs) organized in
calculates area increase from the images. 28 layers (Fig. IB), yielding an estimate of
At the end of the obser\^ations, each nest 69,300 cells per kg. Only the central area
%vas collected, weighed and dismantled (about 30°o) of the nest was used for the
comb by comb for a better understanding brood production, as seen in the presence
of its structure and composition (Fig. lA- of meconia in these ceUs. For the nest
B). The Paulo de Faria nest was collected studied in Pindorama it^vas notpossible to
after natural decline, and the Pindorama estimate nest gro^vth. When the nest was
nest was killed for collection. Subse- collected, it had approximately 745,564
quently, the combs of each nest were cut cells distributed in 41 layers and weighed
out in squares with areas of 100cm-. We 11.5kg (Fig. lA). As in the Paulo de Faria
JournalofHymenoptera Research: Festschrift Hoxoring Roy Snelling
B
Fig. 1. NestsofAgehiavicinafromPindorama (A) andPaulodeFaria(B),SP,Brazil.Positionoftraysbeneath
a nesttocollectmaterial discarded from the Paulo de Faria nest (C).
nest, a central area comprising about 30% day while the colony was in an active
of the nest was used for brood production. phase.
This nest had about 64,832 cells per kg. Foraging times of exiting the nest, arriv-
Foraging began early from, the Pindo- ing at the bait, then returning to the nest in
rama nest, so thatduring the 06-07hperiod Paulo de Faria averages 2 min (1.19-
when the colonywas in an activephase too 3.47 min). The increase in the number of
many workers were active to allow their foragers in the baits was linear (Fig. 2),
number to be estimated, even with slow- suggesting the absence of recruitment
motion playback (Table 1). Later, in the (Hmcir et al. 2007).
declining phase of the colony cycle, with In October 2005, the colony of Paulo de
fewer individuals and less activity, it was Faria was active, producing males and
possible to identify more foragers exiting workers,both ofwhich are easilyidentified
than returning. From 14h-15h to 18h-19h, in this species. Using operculum numbers,
there were more foragers returning. We we found a rise in the production of new
observed that about 30% of the "foraging individuals in the period from November
activity" was related to very brief absences 2005 to March 2006, reaching a peak in
that presumably brought nothing into the March, following by a decrease in April
nest. This behavior gave rise to a cloud of 2006 (Fig. 3A), with signs of nest desertion
workers outside the nest throughout the due to the absence of workers in the
\"oll"ME 19, Xl"Mber 1,2010 7
Table1. MeanratioofAgdmavicinaforagersexitingbythosereturningperminute(valuesreportedasexit/
return)indifferentperiodsofthedayatnestinPindorama,SP,Brazil.Thesearerecordedbothwhenthecolony
was active and ir. apparent good health and later ^vhen it was ir. a state oidecline.
Active 150/145 00/00
Declining 03 06 07/04 00/00
external area of the nest. In front or above manv spiders (.Arachnida: .Araneaej. In the
the nests of A. licina we sometimes saw a two studied colonies, the taxonomic com-
cloud of foragers fl\TQg near the nest. This position of the discarded prey parts '^vas
cloud disappeared after April 2006. similar. Lepidoptera and Coleoptera, rep-
The colony cycle at Pindorama ^vas resented by remains of lar\-al mandibles
similar to that from Paulo de Faria. From and adult body parts, ^vere the most
May to June 2006, there was little activit}' common. Spiders ^vere also an important
and almost no production of new individ- item in their diet. The other orders \\'eie
uals. After July 2006 males ^vere found in found at much lower levels. In addition,
the population. Adult production in- we found two different seeds, one from a
creased to a climax in Januan.' 2007, grass [Fanicum sp.) and a Cyperus sp.
remained high up to the end of Februar}' Severalballs ofplantleafhairs ^vere found,
(2007) ^vhen the population lessened dras- ^vasp lar\"ae, and some small pebbles and
tically (Fig. 3B). sticks.
Agelaia licuia collects at least 10 different
DISCUSSIOX
orders of insects: Lepidoptera, Coleoptera,
Dermaptera, H}Tnenoptera, Heteroptera, Information on architecture of the ob-
Mantodea, Diptera, Xeuroptera, Blattodae ser\-ed nests corroborates that of Wenzel
and Homoptera. In addition, we found (1991j and Zucchi et al. (1995), in that the
MeanPIot(Spreadsheet16^*6c)
Mean:Whiter.MeardD.95Conf.Interval
24
22
2D
18 \
16
jj
S 14
o
12
B
1 10
^ 8
6
4
2
C -Q- Mean
SO 32 "e3rttD.95Conf.Intewal
Fig. 2. Xumbers ofAgelaia vicina foragers per minute ^mea: SE that foiind and collected meat baits at
I
Pindorama,SP,Brazil.
Journalof Hymenoptera Research: Festschrift Honoring Roy Swelling
21000
nov/05 dec/05 jan/06 feb/06 mar/06 apr/06
B
Fig. 3. Numberofopercula/daycollectedduringthemonthsofstudyfromnestsofAgelaiavicinaatPaulode
Faria (A) and Pindorama (B), SP, Brazil.
peripheral regions of combs do not fulfill a InA. vicina, initial construction of the nest
reproductive function but the act as an can also be considered rapid, with the
envelope. Detailed studies of nest devel- construction of several combs. Approxi-
opment in swarm-founding wasps are mately fifteen pedicels and initial cells may
largely limited to the genus Polybia (Jeanne be built in the first five hours (Oliveira pers.
and Bouwma 2004; Kudo et al. 2003, 2005; obs). However, A. vicina then shows a
Loope and Jeanne 2008), which provides a continuous increase in the size of the nest,
baseline for comparison. In swarms of P. rather than alternating periods of stasis and
occidentalis (Oliver), for example, rapid sudden expansion. The growth rate found
construction in the founding stage com- here shows that nests double in size in six
pletes the initial nest in two to three weeks, months. Factors that allow nests of the great
followed by almost no change during size of A. vicina include high growth rate,
much of the ergonomic stage. Renewed highpopulationandlargenumberofqueens.
expansion may occur several weeks or The large number of foragers producing
months later Qeanne and Bouwma 2004). a cloud of workers during the whole
VoLL-ME 19, Nl-mber I, 2010
activity period of the colony is visually Qeanne 1991). Based on Figure 3A-B, nests
impressive. As we obser\^ed, most exits differ greatly in the number of individuals
from the nest lead to very short flights that produced. The Paulo de Faria nest reached
appear unconnected with foraging. Hy- a production of 18,000 new individuals per
potheses to explain this persistent cloud day, but the Pindorama nest reached no
include that it a) ser\^es a defensive func- more than 300 individuals per day at peak
tion in obstructing the approach of pred- production. It is hard to account for this
ators or parasites, b) ser\^es as a landmark very large difference.
in the orientation of returning foragers, or For less complex societies, like Polistes,
c) is simply a way of reducing crowding feeding efficiency may not to be a limiting
inside the nest during the active part ofthe factor for nestsize (Strassmann and Orgren
day. The absence of feces on the substrate 1983). In A. vicina, however, the fall in
near the nest indicates that these are not worker production may be a consequence
defecation flights, as Richards (1978) sug- of the difficulty of obtaining food in the
gested. If it is found that the cloud is rainy season, associated with the implica-
composed of young workers who are not tions of a high relative moisture for the
yetfullymature, this wouldbe inconsistent maintenance of the colony, an increase in
with h}^othesis (a) and consistent with (b) predation, or appearance of fungus or
and (c). parasitism (Hunt et al. 2001; Richards
No recruitment to meat baits was de- 1978). Because the forest remnant of Paulo
tected. This is in agreement with previous de Faria (435 ha) is larger than that of
obser\^ations on Agelaia Qeanne et al. 1995) Pindorama (128 ha), it may also provide
and contrar}^ to what was obser\^ed for more resources. Nevertheless, the differ-
Polybia paiilista (Ihering) (Hmcir et al. 2007) ences presented regarding the production
in which authors found recruitment for ofnew individuals may notbe tied only to
sugar sources. In terms of diet, our results resource availability but also may relate to
are similar to that from many other social the differences in colony age and preda-
wasps (Edwards 1980). A. vicina has a very tion.
broad diet, foraging for water (O. OHveira The term ''keystone species" was coined
pers. obs), plant tissues, proteins and by Paine (1969). A keystone species influ-
carbohydrates. They use plant fibers (cel- ences several organisms in an ecosystem
lulose) fornestconstruction, proteins (from with a effects on the other species out of
captured arthropods and carrion) and proportion to its abundance. A keystone
sugar from fruits (probably from the pulp species may determine the types and
ofthe seeds found) as energy source for the numbers of various other species in a
brood and adults (Akre 1982; Rossi and communit}^ Several aspects of our results
Hunt 1988; Spradbery 1973). A. vicina is a suggestthatA. vicina may actas a keystone
generaUst predator of land arthropods, species. A. vicina, besides having the
taking spiders and abroad range ofinsects. largest nests and colonies among social
Wecaninferthatitplaysimportantroles in wasps, has a very high rate of brood
their ecosystem as a predator of large production (up to several thousand indi-
numbers of invertebrates (see daily pro- viduals per day). The quantitv^ of prey
ductivity, below). brought to the nest is evidently very
The colony cycle of the two studied substantial, especially if we take into
colonies of A. vicina was similar. In the account the rough rule of a 10% efficiency
dry season, population increases possibly energy transfer between trophic levels. A.
indicated preparations for reproductive vicina preys upon an impressive diversity
swarming, which causes an abrupt fall in of arthropods and must impact their
colony size, as is known in other Epiponini populations locally. We propose A. vicina
10 Journalof Hymenoptera Research: Festschrift Honoring Roy Snelling
as a candidate keystone species, so that it Jha, S., R. G. Casey-Ford,J. S. Pedersen, T. G. Piatt, R.
would be fruitful if future studies were to Cervo, D. C. Queller, and J. E. Strassmann. 2006.
Thequeenisnotapacemakerinthesmall-colony
evaluate its influence in neotropical envi- wasps Polistes instahilis and P. dominuhis. Animal
ronments. Behaviour 71: 1197-1203.
Kudo,K.,R.Zucchi,andK.Tsuchida.2003.Initialnest
ACKNOWLEDGMENTS
developmentintheswarm-foundingpaperwasp,
Polybia paulista (Hymenoptera: Vespidae, Epipo-
We dedicate this paper to Roy Snelling, who liked nini): cases of building multiple initial combs.
social wasps and helped to inspire young hymenop- Journal ofthe Nrcv York Entomological Society 111:
teristsofeverystripe.Hewasoneofthoserarepeople 151-158.
who excelled in doing difficult, dangerous, and ,S.Tsujita,K. Tsuchida,W. Goi,So.Yamane,S.
sometimes unpleasant work if it would open doors Mateus, Y. Ito, S. Miyano, and R. Zucchi. 2005.
to a pro\ocative new view of the fascinating insects Stable relatedness structure of the large-colony
aroundus.Wethinkhewouldha\'eenjoyedreturning swarm-founding wasp Polybia paulista. Beha-
a critique of this paper. This work was funded by vioral Ecologyand Sociobiology 58: 27-35.
FAPESP (2005/03569-8; 2008/07633-1). Loope, K. J. and R. L.Jeanne. 2008. A testofadaptive
hypotheses for rapid nest construction in a
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