Table Of ContentIum\mtiim\ t*ltin Htttiil.'iWitfrfrtfX Am? M'tWXl 122(21155-6: 55
VVI IIIN-NKST BEHAVIOUR IN A EUSOCIAL AUSTRALIAN
I
\LI OIUPINE BEE EXONEVRA (EXONEi'KEUA)
TKIOENTATA HOUSTON {APIDAK: XVLOCOPINAE)
by Zm\Sti:j\'4(S; Mk iimi P Sc iiw.\k/:,:
Summary
M
Silln. /. at StiiWM'/, I* | llMN) \Viihiivne*t behaviour m a eusocial /Vtistialian allodjpuic bee iiufHritrn
if\oncttrrltu} Irnlvnlala Houston JApicbe: \yloeopm;ie), 'Ihittx.K. So..S \ti\i 1220.95*03, -'' May, !'>l>8.
I'ndeisiaudin^ the processes involved in the evolution of .soeial behaviour kus become oik- of' ihe uintf
challenging areas ol modem l*ioloi»_y. Since bees and wasps exhibit j \ariei_v nl micijI 'M^jiusalions ihey are
panicukirlv useful lor aiklrvssutu social cvolintunur. qUctriOiK. Mlodapuic hces are especially useful lot
.Ajininmu mvial evolution,since speciesdisplay varying formsi>l social oryunis.ilion from solitary meusueial.
IInsstudyexaminesvvilhin nest bcHlUViftOI of lAo/ttmu \I:M>/u-nnfio)iritlrutttui, ;i nativeAusitalum.illmlapnie
|V\'. rhis -.penes has Ifjc latest known w1t)n> tftc* o| any allodapinc bec and exhibits sinking ni/c \analion
antone female Herniates suggesting lhal sociality UttlV be resided .is highly eusouuf Ileiv we assemble a
olHt-hteiravniulnlio.dialptijliieasl,otihmicssjfpole'ctiheissdsipHeeciressbuyni(theshmoawrkdeidalparlatchtoiucgehomfaonwynhcuhgugvricosiriircsinaidvisspilmaiyleadrIidnt(hheosfeorremcoolrdheitdilnocr
Ovtillj a*_'uiushe tvluoioitts have not1'ceii recorded "01 oilierAu«ai;ilian allodapmcs and have been recorded
only lately m oilu-t allodapinc hnina. Jhuwititt (riif'^tttttn appears to diller from olhoi highly eusocial species
where there is usually littleor no agression bin instead 'penile despotism".
Kl v Wouns. fwmlint irn/toiatu social behaviour, -illodupine bee*, agression
Inlrodiiclion aitangevl in a NOtjiiciiec Of piumtive l»» advanced'
has been qucslioncd (KuKuk W95J but lew studies
I'bfl allodapinc bees provide opportunities for have explicitly invesliyaled whethei prmiitivc 01
Miiiiparaiivu approaches lo the evolution oi social 'advanced' lorms of sociality within ta\a correspond
bchaviotu because ol ihe wide range: o( social to hasal tvrdistal positions wilhiti phylogenclic lo-e-,
organisation within and hclween species and ^eucru t.y'OUHHi Irittcnlttht isan Australian allodapinc bee
One -onull and endemic Australian subgenus lhal lives in .^cmi-arid environmenis. This species has
f strnt'tmlht. contains1 fours specie* lhal titttgp IVom ihe tatjiesl known volciiy swes ol any allodapinc bee
tilt predominantly solitary l\\o>t<'iiru tnw so/// and exhibits nun-pholopicul dilTereuiiatiou be!ween
kaymeut { Vlichenei |V0?| ^ iho etist.rial /'. pUUlfVc i-astes (Houston 1*-J77. Hursl cV Schwar/
ttitkflliflttfHotfStOn l'>77; Hursi & .Schwat/ \$%), |*9*Jfil Much of the informalion about social
In most comparative slticjies of insect social organisation has hcen inferreil from disseelion of
evolution tlTora is an implicit assumption that lies! occupants and brief observations o! lemales
small colony sr/c is a.-.socialed with flexible and ouiside ol their nests (Mntision 1077; Muini
beltav iourally medialeil reproduciivi- skew. I he oupub) M is suspevted thai this species exhibits
m.imleuauec ol dominance hieiarehtes via physical casie dilTerenlialion, where large females
ac'oiiisiii is cortsHJered u pnmili\e trail (Wilson (termed 'Majors') are citieeii like ami smaller
l'»7li C'orrespoiulinydv, ItirgC colony si/e> with lemales i'Minors') acl as workers within the
sliou^i repiocluctivc skew and non-aLonislically colonies (Houston 1077- Hursl |*)%). Ilowevei,
niainiuincd hiciatebie-s aiv Usually reijiirtled as mou- W|l mi oi->.i heha\iour;il studies Imvc not he-encarried
derived trait-. Wilson (1^71) su^yested that less olil to assess whrlhci lln:sr lwi> nn>iphs really are
sophisticated funns ij| siut;il niyailisatioii would lichavioiually dislmcl. Colony sueandiheassocialion
Invoke physical mechanisms ol control such £& Ixlwcen morphology and repnHluclivc slaltis su^^esi
a.L'^'iession wilhin acolony, hul thai IhiN is icplacctl by thai this species more closely approaches the highly
"gentle ilcspi^lism'1 in more advanceil lorms cri eusocial loim oforganisation characTcrisiic olapiue-
sotiabtv- It is* also generally assumed that a hojh rueliponme and highly eusocial halicline bees, than
level orbehavioitral spe.ialisalion isa more derived any other allodapinc hee.
hail ami iluti this can leadlohigher levels ol colony I In- study invesicates Within-Mesl heluoioiii in
cllicieiicy I.Icmuuc (Wo. H<tvvevcr, the idea thai ijbservaliou c<m>nics oi I,, fritit'ntitht. A icitcilouv ol
thllcrcnl foims of social organisation can be behaviours is presented here in the loriu id* a
behavioural catalogue inul eompaicd with other
Sdtoal mI BiOll^liVll Vii-mo l-liiuk'^ Inivfrsilv l>l S.-ulh belntviuiiral studies ol allodapmes. I hesc data will
MKiralui 'i''*) ('flu 'i'"1 v-t'-i.ni. s \n,( viu i m also be used i\u- specific analysis til behavioural
/(I,ISlvHtlf"IlilHlct^AllH.OI specialisation which will appear in a futureseries of
V. / Sll-J NX M V S( flWAK/
publications, hi addition, the idea that morphological had approximately 12 hours in the artificial nest m
caste differentiation and large colony si/e mq allow theirodours to permeate the nesl before n was
associated Willi low levels H agonisiu in Colcftty possihk- dn them to leave tlhe tic\t morningr Sheks
mi* vr.ilion is discussed in relation lo the social were haphazardly plaeed near nesls lo ael as visual
oieanisalion ol /.. trirfi'iUitht cues foe returning beus,
Materials and Melhmls tit-htividumf nhscrvLttitMS
Oitcc obsetvalion ncMs were set up Ives wetv
Stmh •i/t'S allowed lo adjusl lo their new environment lor one
f\\<>natnt Iritlcrtfftta nests were collected from week het'ore observations began. Data colleehou
Lake Gilles Conservation Paris (13ft 48" \\. 32 34' Si involved 'scan* and 'foeal' sampling techniques
AluosctatreadliainItnhethinsnrafrleia.eaFs.twoildmKlvurentPenensitnssuwlea.reSporninI-h tIlAieJlpmoasnililol>n74o).f Seaccahn isnadmipvliidnuagliinnvotlhveedobsreercovradtiinogn
cipally »n disused beetle burrowsexcavated \uAtttittt nesi. jiMnji a 5 mm scale along Ilie glass and was
l><tf>\n<ittriw IJcnth (Weslern Myall) and Huhrlrytw conducted immediately belbte and after lotal
oUtiifulimn iDcM'.K (Hulloek Bushr Deail branches sampling. Tins was done to determine whether
ol both tree .•.peeics were examined lot nest certain bees were spending more Ihue than olhei in
.-Mi.mt.es i.e. the exit holes made by the original certain areas of the nest, lor example, near Ilie
hcelle occupants Intact colonies wetv collected entranee or near the brood. Pocal sampling involved
during lchruar> 19^5, t tvkl collection ol nests 2 mill observations ofeach bee in a nest. Nests .nui
took phtee when temperatures were eool f 12 C-20 inihviduals were raiulomly seleeted eaeh dav (t>i
O. to ensure thai all ueeupants weie present. »>rderol t>bseivations. A headband magmbci [^5
Once an entrance hole was loeated, iKli branch was m.tgnifieation) was used lo observe the behaviourolI
removed, entrances were blocked with tissue paper, individuals. All hchaviours pelformed in a 2 mm
the brunch was placed in a walerproot bag anil period lor each individual were recorded into a
stoied in an nisulaied containet with iuc [qr voice opeialed tecoidei Observations were linn
transport lo Hinders University. scribed on to data sheets at a later dale These
Al Hinders University the nests were stored in a behaviiitir.il data were used to eonslruel Ihe hchav
eonslanl temperature room al apptovhnalclv 10 ( toiiral catalogue and later lo examine behavioural
lor processing. Nests were opened using a kmle ^VLialisalion.
and all nest occupants, including blood and nest Hchavioural observations took place m ihc aln-i
dCornht.entAsduslutcsh uwseproelleni,ndwievirdeuatlrlaynsfemrarrekdeldo auPseitnrgi Cnooann.d( Ibse0e0s- 1w7e0r0eh)a,ctwihveen Ilnemtpoeiraaklur1e0s nweesrles :_we2r1*e
IJtMntifoM*1 and TcslorsIM enamel paints applied to observed with up to four nesls ftifljlg ob-.eived ill any
ilie thorax and metasoma liee colonies were Ihen oiv session, fable provides information alioui
I
Iraiislerrcd lo artilleial ohservation nests, which nests were observed, when Ihes were obseiveil
Artificial nesls were similar in design to those and how many minutes ol observation each bee per
deserihed |>> Sehwavv A Overboil t |y^3} hut were IfliM teccived. In addiiion, the numbers ofbees ih n
ina<le ot ptne wood instead ol halsa, Bach nest weic present lor the initial a\k\ final obsciwitmn
consisted ni .« rectangular piece ot iinireaLed pine peliods ale giveu.
wood 210 \ 9j\ ^ |.s mill A gTttftyp was gouged into
one longitudinal lace o mm dfWfl \ 200 mm lengthi
'I he groove was smooihed out wilh a metal rod to Ktsoits
remove any sphnlcrs ol wood A piece ol glass. 210
\ 2<i mm. was placed flush against ilk groove and
secured al both ends wilh insulation 'ape. A blai4.
cardboard cover was plaeed ovci the gla-^ loexclude The contenls of nest> collected in bebrtiary l1*"^
IhJil hetweeu observation periods. are summarised m 'lable 1 Uunug lhc--c samphnv
t >l>sei\ulionnests wen: set upon suhhonvontal trivs peniKU. cotomes used for behaviouial observations
ina shade house/it HindersUniversity.Oneeiul olThe were rearing brood. In early bebruarv colonies
shade house was open so that Ives could loraee contained brood Hi all developmental stages, i.e.
heeiy outside, Nest enhances lacvd the open c^h\ ol r\';_'-., larvae, prepupae and pupae. By late bebiuaiy
the shade house, A maximum ol lour nesls wu- female bees in Ihe colonics had almosl c^ascit ci"j
plaeeil on each tray with approximate!) 15 um laving and hrood rnosllv comprised larvae. pfeptyVK
hetweeu each nest. Ohservation nests were fiisl and |>upae, There was a great deal ol variation in the
plaeed in the shade house ill dusk 5-h days atiei number ol adult lernales present in a nesl. rammer
eolleelion and opening- Thin eiisuied that the bees ftom I-1X ibi- I
BEHAVIOUR IN AN ALLODAPINE BEE -'
TABLE I- Detailsfarnests aj Hxoneura tridentata observedin thissludv.
Nest First Last tots1 nun ber Total minutes Initial no. of Final no. of
observations observations of of Individuals Individuals
observation observation
penoIs pel nest per bee pernest
1 7 Mar. 14Apr. 15 3d K 5a
6 7 Mar. 14 Apr. 15 M) 9 5U
9 7 Mar. 14Apr. 15 30 4 I2h
12 7 Mar. 14Apr, 1? M30 13 !5fl
3 5 Apr. 4 May IL> 3 5
4 5 Apr 4 May 1? AS ; 5h
:o > Apr 4 May 14 3? 4 5*
30 26Apr. 10 May 20 40 (i 5*
43 26Apr. 16 May 20 40 3 4'1
56 29Apt In May 20 40 4 4
Decreases in thenumber of indivduals were probably due Lo death whilst foraging ordispersal toother nests'1, Increases
weredue to the addition ofnewly eclosed bees'1, orintruders which swapped nestsc.
Tabu 2. Summaryofnest contents farcolonies oj"Exoneuru tridentata colletledin iehnutry 1995-fttym Lake (lilies.
SouthAustnilia.
Nesl eontents Mean value (±S.E.) Mean valtie <+S.E.)
forearly February forlate February
(N=24) fN=B]
Hggs 1.21 (0.57) 04)8 (0.08)
Larvae 1.75 (0.63) 0.02(0.27)
hvpupae ()_(>7<0.2N) 0.31 (0 13)
I'upae 2.42(0,72) 2.23(0.7%
Majors 1.17(0.1(11 1.23(0.34)
Minors 4.17 (0,K3. 4.3XH.30)
Males 0.33<(U3> 0.3K(0.2I)
heluicitntntl repertoire
In Ihe following section behaviours observed during
the study are presented us a behavioural catalogue.
Observed behaviours ateclassified into four hinciional
groups (often iuler-eonneetcd or overlapping): (i| self
maintenance, hehaviours. (ii) nest maintenance
behaviours, (in) inter-adult behaviours, and fiv)
adult-brood interactions.
Mmnm
Si i.i NAWCI til ii wiDiiks
inv nvi:
Sees were reeordeLl as being "inactive" when no
Oilier behaviour was bciue. performed, hiuelivily
often occurred within a behavioural sequence. I;or
evample. a bee eould slap grooming, be inaelive Tot
some lime, and then navel forward in the nest Bees (v!S
I
eould either he standing 'upright1 or the> could be
lying 'upsidedown' on the floor o\ the nesl. Maeia at Females per nesl
cdtefscr(iIp9t9i2'o|n ioufeluadesdimislliagrhtbemhoavvieomuern,ts"Rienstitnhge"ir Fign.esIl)Hoifsthosgoureaumilott"teiniliho-nnytiistiazecso(llneucmtbeedrforlomleLmaakleesCipiellrcs
However, in this study bees were only recorded a SouthAustralia. Ivbruyrv l-995>
^S Z STTjEft* M. I*. SCIIWAKZ
inaelive when ihev were motionless. Exoncilrti Ct ratithi spp. which have U turning burrow
irtthnittift spent ii largo amount of lifftC inactive enlargement near (he nesi emrance (Macia a ul
Since inactivity can occur wiihm ami between 1992), Turningotlcnoccurrc<laspart ofa sequenceof
bch.oioill'Ul sequences il is difficult ttl show behaviours during interaction* between liulividllllki
numerically Lite mmaim ul tirtic upeui jiiuwive i.e. it UTUld occur during sequences which involved
because oi ihc wav die data were collected "nudging" "passing" or "avoidance" (see belowT l| ->
(ieiicialty. lh0Ugh( lIlC bCCfs wcie inoic active when bee appioaclicd but axoided anolhcr bcc. il inti'lii
temperatures were >,!0 (* aiul/or when a loragci cither "travel" up to Hie bee, and then back away iiv il
returned might "turuH and "Travel11 ill the opposite direction.
si 1 1 tU*i)OMINU NM'IAK l>l nVOKATlMN
"(iroommg" was observed lrci|iicutlv. ami included Individuals were observed flexing ami bending the
.inv iciivily where Ihc body suilace was cleaned proboscis anil although dropteis ot ueeiai could not
Sct|ucnccs (or cleaning dillcrcni areas li die body he seen with ai die magnifications used,, it wax
wivrc similar to those reported Tor fihttt/i<(<j>t.\ hrw/n assumed tlliU bbCJ WCl'c dehulraiing ik\tai as has
Cameron au«l (intfithi spp., (Mactar/ ni. I('92t.The been observed in olhcr allodapmes alter Iceding
mosi common sequences were: U) head cleaned In iMkheuer V>72; Maeiaw,// IW) Some bees slow
I
iniliaflj Wiping a forcing with the proboscis then ly fully extended and ictiacled the whole pro-
loivlcg used to wipe the length oi die antennae. boscis without hendint! it. The proboscis was
hi i.mini- HI the htwc; I'orcley a-'.tin Wiped Willi tllC extended and held out lor aboui 20 sec Hi *
proboscis, lollowcd h> Ilic wiping of the head rehacicd beIore beiag extendedmmagam Some
with the (orders, (h) the rnctasonia wascleaned hy iiulividnals spent die whole u\n observation
Using die ithial spins on the luudlcgs |o sciapc oil period pcrlorming this behaviour.
JijNl/pcllcn. (t1) die thora\ was cleaned with the mid
|Cy£ (die imTisoma and the thorax were often Nt SI AUSI N ISM
1I I
Luoimicd at the same tune with the diflcrcnt logs), (d) When individuals were regularly abseni from Ihc
Ihc winy surfaces were groomed by drat'i'tiiri ihe nest it was assumed that they were foraging
wiirjs under die mctasoma with the hind legs, However, il lhey were absent tor more than 5 obs.r
Wiping ihem t»CtWCn the mctasoma aiul hind Icy-. vation sessions In a iow. il was assumed lliat \\\>'\
and then flicking tlicm back inlo position, were either dead or had dispersed. Absenteeism (or
(booming did not occur as one |0ng uninlenupled foraging activity! was only observed when temper
sequence as has been Clbfcervnd lot $. hcwiiti alines were > 25 C. Poragcrs were idcitldied when
(Macia tt oi I1W1) Grooming could Iv briel' or they were seen reluming to the nest, I 'poii rvuiW-
la,i lor |lw whole 2 min observation peflod irtjj, Ionisers usually worked their >vo> down
the nest passing and interacting with other unh
si nail Koln M«>\ i.Mi Mis \nluals. ul'ten bavin;.' 'buccal ermtweP with othci
This was intermitlenl hehaviour. which was nftttfl individuals, pivsuntably provitliuy ihcm with iicl-
obseiwd during long bouts ol inactivity, and behav- lai (sec inter-adit11 bebavioursi. Often slilIi a
iour comprised slight movements of'head, body or bcc Would then leave ihc Ucst auaiu and rcluin
leg*, which did nol involve any olhcr type ol behav- lalei. foragers were nol observed IcLdniv tai
iour vae.
rM Wl>i i im; Nt:si VImnii nvnci Hmwin, i.:s
li:i\clling" involved nioMiiy lotwant-. or backwards
up or down the ncsi lor 1-20 cm Bees ihal were ia klthW!
liavvllme were Usually very active bill Ihc Uavclliug A ticc was recorded as guarding" when il occupied
speed vaued. Iiavclliug forward otlcn rcsullctl m a the position closest lo the nestentrance with its bodv
bee coming inlo contact with others and was usually oriented so that its bead svas facing away from die
followed by "passing" (see below) cnirance. Such a position allows the niciasouiu lo
block the nest entrance from intruders, as recorded
I! K-'SI'Si. for olhcr allodapine bees H hcuitri iMaola <t ttl
'liiruim'" was used lo describe a change of IM2), />'- MLWii (liatra ft ul. IVOii ami /•. i»n>h»
directum in the nest. Turning involved curling l|lC "Mi Im. ,v Sdtwaiv l'^3). Ilurmg cnardugj Ibc bcc
body and sonu-isaidiing. icsulting m Ihc bcc facing was inaclivc citheron ils back or standing upright, If
the opposite ilireelton. Both Majors and Minors a bee was closest to anil facing the nest enhance, it
appeared lo lurn with equal case. This behaviour was mn recorded as guarding, since bees in ilus
occurred anywhere in the nesr. unlike that in position would often be III ihc process ol leavim*
sy
BKllAVfOUK tN AN AI.LOHAI'IM; BIT *J
the tu'si. Minors wore tyfl&n scon guarding and ir< other's metasoma 01 lace. II 'individuals were lace
some nests, Majors, pur"ieulurly egg layers, were not to face the two individuals tapped each othci
seen t« guard ill all. antennae,
Guarding Jul HOI always occur near the nesi
enhance, In some nesls the "guard" was ^tutiopifd rvssisa;
'/4-1/* »>l ide way down the nesi but was Hit- bet "Passing" is the exchange ol positions by nesi
closes! 10 Hit" nest enhance. These guards were males. Passing occurred when individuals Were
sometimes seen 10 'pair;*!' (he nest from that section either facing each other or the "passer" was luciug
up to the entrance. This involved the bee rapidly Ihe mclusoma ol'lhe individual she intended lo pass.
"travelling" forward, whilst rapidly antennaim-1 In each case, iiuhwduaK oriented (hemselvcs \cn
("inspecting") the ties! luiuen bcfoie leluntiny to Ihe ter lo-venler. csscnhally walking over each other. A
guard position. In some nesls it also appeared thai pa>s was either simple or complex. "Simple pass
Iwo individuals would guard alternately or one in ing" involved ihe smooih exchange ol positions,
front of the other Although ihere were times when with individuals usually llaltening their bodies
moiv than one individual was seen in Hie gUtitil a;jaiusl Ihe nest wall. "Complex passing" involved
posilion. (here were individuals who never imc individual foiling a) anothei individual's Inm
I
"imarded". Owing ihe study, wo othet invctlcbiate-. pans., and/or simygliny and yrasping each other
wore observed entering the nesls. Since there was no with Ihe logs. Hi her one or both individuals would
l
inleHcieucc liom ttthitr inverichrale predators in thr int.- Sometimes one iimIivulual MajM bite the othci
captive situation, guarding hi 'his study may not on Ihe venlral side between ihe metasoma and lite
rcl'lcel nalural behaviourof this specks. thorax, near the articulation between the tiochaniei
and the thorax. Passing sometimes involved bite!
INSI'U'JINt. "buccal contact" between die iwo individual-,,
This behaviour involved a hoc abcrnalrly aim\t\ although il Was olieil dill'icull lo determine clearly
ualni;: ohieets. lor example Ihe nesi wall or whether buccal contact had actually occurred. Ii
brood. |yjg>i were frequently anleimated in this was noi always easy io distinguish between lhc
way, Sometimes bees travelled up and dow u the pas-.er and the "passed", except when one was
nest inspecting the lumen wall Owing ihis hehav initially stationary *m*l anothei was travelling
iour Ives moved their heads slightly and rapidlv
omm
moved antennae. MiK-VAL l r
Individuals were olteii observed to much each
MOVING lUIJRIS other's open mandibles with their own open
Debris in Ihe nesi was moved by passing it mulei mandibles; this was lermed "buccal contact". When
ihe hody with ihe forelegs to (he hind legs then individuals were involved in such interactions, one
pushing backwards with the hind legs or tnelasoma individual was sianding upright and the other was
This behaviour was nuv iappiov, (),>'; of the positioned upside down. Individuals also cn^a;-ed ill
obseivaliou tiiuei. since the nests were in haul, brief huceal couiact during passiue. Ilaritt^
liiic-giained wood w lich required little mam- approximately 5% o1 buccal contact inici'aclains.
U-nancr. Debits ohsctved in the nest included neelar flow between the ni'.»u(h parls ol individuals
exuviae and. occasionally, dead uulividuaIs was observed and individuals were observed placing
"Moving debris" \\t(s not usuullv observed utiless then proboscis between the mandibles of another
temperatures were 3 2& ( individual. lVoHennv ol ydobulesol neelar(Media &
Sehwar/, \fy)M, was not otv.cived m E, liii/ctihiia.
Inti k'- \i)t i r Ht iiAVioi r;s
k\ MfM^l
W \N1 i "Nudginj:" involved one individual tisinjj ils face
'Avoidance", it combnalion ol oilier behaviours, to nudge oi hull Ihe melasoma or lace ol anolher
involved one individual travelling towards another individual. The bee that "nudged" was usually
individual and "auicuuaiing" cnhei ihe metasoma upright Nudging usually resulted in tme ol' the
01 lace ol'ihat individual and then suddenly hackim- followjne:
away Of milling and liavelliuv it. the opposite at The nudyetl individual lurncd and the nudgci
direction. rctrealed. which someliiues invoKed the nmkvd
bee opening ils manilihles.
\\\) NfSAI CUNl Ml b» If nudged from behind, the bee being nudged
"Antennal contact" accompanied most inter-adult would sometimes posilion ils antennae laterally
behaviours. When an individual came in to contact (out lo ihe side)..Ihen il nntlged again il might open
will) another individual n either " mtcunaied" Ihe ils mandibles Thi> eventually ivsulted in ihe bee
N> A. S'lLLN & M P NCIIWAR/.
turning, investigating the "nttdgcr", and then simple MOVINC BROOri
til complex passing ami/or buccal contact Older brood (laic mslar larvae, prepnpae and
O The nudged or the nudger passing and "biting" pupae) were usually moved in a w;iy simikir to Mil
cadi other. way debris was moved w the nesl. In /:'. tridentala.
similar to fi hi' okV (P, S. llurst pers. eomm, l()95)-
MANOtm I.ATIM. the bee initially held the brood with Ihe fore tarsi
Mandibulatiug, i.e. the opening and closing of the then passed them under the body and pushed them
mandibles not associated with eating, appeared lo backwards using the hind legs. Repositioning of
occur before biting encounters. In some cases a brood occurred ollen within the nests ol fi irnhnfalti.
appeared that mandibulaling was a signal that one Sometimes a bee would move each pupa until il
individmil was rejecting an approach from another reached the end ol the nesl. then it would move thetii
individual- lor example VV approached 'B\ 'A' all back again; seconds later another individual
nudged 'B , K then opened mandibles, 'A' thru sometimes did the same thing. Some (Minors which
retreated. "Biling" encounters sometimes fallowed. consistently stayed near the brood were often
Similarly, il mi individual was nudged From behind observed perlorming this behaviour, In addition,
it sometimes opened its mandibles and/orturned and bees sometimes simply handled the pupae with the
laced tbe nudgeroften opening the mandibles again fine legs but did not actually reposition Iheim
In addition, flattening ofthe antennae lateralis often
i»uurred during mandibulaliug. This sometimes i.KOUMINri RWKHl
occurred when individual* eame face to race or tf Bees tKcu^inialU extended the proboscis lo the
one was nudged from behind. brood or bit gently al the brood wilh theii
mandibles, such beha\lour was categorised as
BIIINti "grooming brood". This behaviour was rarely
In this study aggressive encounteis were observed observed. Grooming may have occurred during
tot /. ttidt'iihtni. These involved biting laf mourn: or wilh handling but it was difficult h»
mandibles, anteniuu . neck, legs, ihe ventral side of ohserve Ihe liner movements of such behaviour
the thorax., iiround Ihe eo.xae ami melasoma. Often because ol die speed ol movement U the probosus
when one individual tried to eseape from such an and the limited magnification.
eucouniet the oilier bee would pull it back using its
forelegs- "Biting" cucoiiuicin were often complex. oVH'oMIl"-.'
Fur example. '\ fc&cd it* ftlCC IP midge B s lace. When "Ovipositing'1, the female ortenled hetsell so
Then one or both bees opened the mandibles ami .1 drat the head pointed mwauK the nest euuame
complicated pass followed. Whilst ihe bees were IHiring egg laying bees wereobserved in one ol thtee
venter 10 venter and struggling 1holding each oilier position'-.: ventral -airlate lacing upwards, dorsal
with legs) "iK would bite the othet on the ventral siulace lacing upwards and laleral surface lacing
side ol Ihe thorax. Alter ii struggle- lh» bftlCJI bee upwards, Prior 10 diui during "0\'iposiiion*' Ihe slim-
was \)W'\) observed on its back while Ihe bilei held Wis extended. Once an egg had been deposited
the othet bee's atiicnutie in its mandihles. in a "lug dte floor of the nesl. the hec reiiactcd the Hil
[\\ wat" eueounier. This tug-of war could last hn ,\ppro\intalel\ inm passed before the female
10 JO -ec. I'oIIovmh;- tl me ol Wfll ^TViOHIlW me mined around andI inspected theegg with the antennae.
individual w hich hud initialed ihe imv (tin- buiem Oviposilion occurred close lo Ihe nesl \^\ KJ .1
sometimes attempted |vi pUKl n^nn and ollen tj mini mid was observed lot 4 Majors and I Minor (*>
simple pass would follow. separate colonies) Individuals took approximately
\ ft mm to discharge an cug Howevct one Mn|>:r
Aln I I im« INIJ.KV tK'NS look \X nun 10 I,in .||1
1 \ \-.\.liln.\nM.iItUN <M1»tIIbKUr'o|o|dI was LlCC I'li.hed wilh ihe Discussion
antennae, and to a lessci CXKM |hfi mouth p.io-.
(openmy and elosme mandible-, on 'In- bl'OvXi) Ueliavioni lias previouslv been stuitttftl in dentil lor
Individual'- Itfpptal pupae, larvae oregt-s. with each ft. iwwiiii (Maela at ill W91). /<. mishi, it. ktlttm
anieunn Mlaiia tt ttl. iWh, A{k*firtpp <\<.tr>itm iSnand)
( VI..son 14>XH) and I hu tthn (Vlelni.V Si h;» .-\
NI ixa'-ai iii-amo lyy?}, B.Kunttm tthfcnttihi gC(WVi\) ^pv^pul jj t»fu*
Hioo.l wvtv \otnelimes nudged heloir Hiey Wiu amonul ol tune inactive, siiiukit tooih.i In es (M,i.-»,.
moved tjUl Mlttt ioUl did lift FC*Ull llOWCVfl nn! \W2\T\\\\ru*fiitti l('°M Ae|i\-tv tended to be
Ihi brood appt-M iHv cbam:iiig. position gteater on davs when the lempei.itnrcs weu aboxr
Ue'HAVIOL K IN AN At I ODAPINi: Ul.i; fl|
2?> Ci SinulaiU. when (he1 temperature was wanner mcJuded stuiymi! iliaira <t ol. \&$$\ Mason I^NKI,
bees lcn<Jcd to forage more and. especially aficr Auonislie behaviout between ;t host and its paralle-
iviuin of a forauci to Ihc nesl. general activity ls not uncommon ,vn\ often results in either host 01
appeared lo increase parasite heme removed bom Ihe nest tBatra cl at.
Exec ttni uui,in,ihi was. nut observed lo exhibit ISWl). \yyressi\e interactions are also Icumd in
tin: Lvpcs »>r ucM mainteitamJO behaviours found in social species ol the bee tnbes Halidmi ami
nfhorallodapities. probably due lo Ihebard nature of \stoc.ipim flkced it til. I07S; Michener \WU),
die nesl substrate Most allodapines excavale their However. /:. {rithniutu was «d'ien observed to
own lu'sts in pithy simstrate material., wheicas /•„ engage in aggressive encounters which involved a
in<fr,rtui.t do not. Alihough observation nests greaj deal ot rtidng and Mniggflrtgi wilh some
provided no opporlunity \\x nest walls to dc^av encounters becomiiiy quite savage. Such encounters
dming the course ol the study, natural nestr are were otieri picceded b\ imdLMU" and lollowed by
also unlikely to rei|iurc tepuiis W MlC nest wall or passing The mandibujatmy dial occurred sonn
miranee, since Lbey alsooccur in line grained Wood limes, either prior lo or in response lo nudeiue and
"Jilts contra^ with /• hu olttr which pcrTovms biting. Ini^lil also be aeeacssivc in nature Tanc \
\anous nesl inainlenance activities such Etf Michener tll)K.^) toutni that some r.\"i<cnfti spp.
cleariur ami larnpini' (removing loose- material produce iriitanh which elivti vigorous gniomine
from llic nesl wall and shaping nesl lumen). responses in prcdaioiy ants. Halra ti w, |Iw3)
csictnliHg ihe nest lunieii (excavating rear ol the descttbed mainlibulalinj.1 dtinue ayy.ie^sion
bmiow). eollat cunsltucti*>n (Uiu)ptng wood into a between ft. uuMn and its social parasite ti. ttufniRn
uillar neai nest entrance) arul removing debris and su^^csted th-il manLlibulai vectviioris wea
(wood strand^i l-.wnaim irt/lvtiftitti may exhibit involvctl. Il may Iheivfore be sii,L'.L:csted ituu v\licn /
nest maintenance netivlics ttj a ereatci debtee when rtfili'tuuiu mandibulaic at each »i!hef, Ihcv also
nt'iv msis are tounded and Lheie is a iKVd to remove release clicnucal secretions which may be ucoriNic
bass kit behind by beetle luiwic. or relay information about dominance sUKis.
Ihis sludy is the firs! lo descriheegg laving to an Thcayonistic behaviours observed m /:. trkltlifilHi
Iwotumtt species. £gj« laying ^as only ohsctved sii-ecsl that domiiiansc hiemivbies may be pieseui
durum, (he day alihomdi it ina> also have occutred within colonies II appears that sonic lutlividuals
u.ght li'bsetvatnnts were only made during ihe enea^e m certain types nfbehaviour which could be
•jl\
day) Leg laying wassimilar lo thai described ha />'. interpreted as assertion ofdominance. Bees that are
tnuttb (Kara vfttl- IWmirI t> /irnnVnMnci.i | , if/. often midyed or hitii-n -iinlthose thatexhibit avoulanee
\W>2\. However two ol the three /:, ttitlrtiiuhi behaviour may have more suboidiuale toles in l|n-
majors thai were observed ovipositing were rarely or nesl. Differences in the way individuals icspond to
ticvei seen guarding. Che thud fllthUI was seen U\ othei individuals 111 terms ol these behaviours mas
y_\u\v\\ luil she was usually 5 em from the base ot (lie be iclated lodominance (i.e. when >ome individuals
not and nut near the entrance. This differs Ironi l< arc nudged lhe> euya^c in a simple pass, wherca.-
lu'ivttii (Maeia <H tii- IWi and I ItnnUn whenother individualsarenudgedand/orbiileti UfteJ
(llogcudoorn & Sehwar/ WK: hull .-/ ttt. in ptess) eu/aee m acomplicated pass). Brothers lx: Michener
wIn re reproductive dominants are guards Rjig I Iv74t found lhat qneens' id Ui*it/%ltt\\tM\
laying In this species appears to be a vers \\iw\ :sf>fivf(ii>t ^cK' die maxima! nudyers in the colony
processcompared wul othei bees (58 sec. H. In ivif T'he> suggested thai ninigfn^ behaviom indicnlc
ti) (Maeta r< «// IW/. in term-, til" both the time dominance siniihir lo thai observed in other primi-
taken LO depos(| *fl ry,:j ;nul the frequency ftI tfgg tively eusocia! wasps ;urd bees Hioiheis X
laying, Oik- female, in pjiOLulac spent 3S mill Micheuei (l')74i cxperimenlalK showed, lot /.
depositing an fcgg which ma> ha\e hecn related td _t{>l>vnw!. that nutlymy by ihe queen plays a role ill
Hie 1'act thai Ihe temperature was tow ihul duv \< thedivisionol'labourauiouu the workersby inhibiting
.'0 ( i. and bees were eetieially less active at ovarian development,
lower icmpetatuies However, these obscivaitous During this ,>mdy ^uardine, behaviour wa> not llic
<lid not eo\er the period ol maximal ggg prodttelMHi same us thatobserved in Held studiesol h >ritkiitahi.
and slundtl be treated vvith eautiim. i.e. with (he abdomen curled anil used lo block Ihe
Ai!.yiessi\e 'u-havioi i has ma been reported ftw entrance bom predators such as ane> 11hirst unpub.i
othet allodapine bees except iarcl> bnwceti /; This may be related lo the I'ael that there was no
nu\hi and its sivial pufitsilcH. htliasi**-(Halta i I <'' piodalion prepare- in die shade house environmeiiu
l'*o :a and inlreLiuently lot A, &-\viiWHi and />'. fmvithi unlike studies 011 /•.. bfytyfai coudueicd in shade
(Mastnt IVSX). The agonistic behaviour described houses where anK were a problem *Mli1M;1liustrj
loi these species mainly consisted ofnudpiiiL!. buine However, females lhat were •juardiii'j ueie alw-ivs
t»l legs and hndies an.l blocking passa.u^ bin alsi: facine the boitom ol Ihe nest which su^'cMs rh.ii
f>i / STBKNa M.r sciiwak/
they wan* in a position 10 block the ncsi if the need all similui lothose lound lorotherspecies, su;jeesiimj
arose. lhal such behaviours are likely lo be ancestral and
I lophallavis to altruistic behaviour. foraiUTN that development ol' novel behavioural elements is
ungate in energetically cosily ttitd risky behaviour Id not necessary Tor social ot^amsalion lo evolve bom
obtain tooJ which they relinquish to others. small family groups,lolaoiegroups with uioipholoyical
Trophulluxis is important in the social organisation ililleieniiahnii amoiiL! colony metnbers.
ol many social insects (Wilson ls>7! ). In allodapines However, unlike oilier allodapines. I triJathtta
llictv may he differences in the way in which exhibits frequent and overt agonistic behaviours
ttophallavis is performed. £xfiWtiUM ht<i>l<>r have auKtin; nest mates Such agonistic behaviour has
been observed to engage in solicitation behaviour often been associated with more prinitlivcly social
lietore Irophallasis occurs (Melna& Sehwaty l*W.H species, According lo Wilson's i 1971 1 criteria, E
Sulii,ilUlion mw>kcd individuals rapidly slrokiny triifi'iuttrn can be classed as highly eusocial because
each olhci's antennae prior 10 huccal contact. dierc is female morphological dimorphism as.sociaud
Trophallasis in E, hia>io? can also involve one with reproduclive division of laboni Ihctcloic. /:.
(inMdeilvniadua&l pSrocfhfvcrviatiijv.' Wa$gBl|o,bull'erototletilui,qiu>idoltogalnoobtuhleesr nthualtlntaHghrtedsosesino'nt cwointhlionnualcooWliolnsyoncsan( 1b**e71rtespul;a±cueesdliho\n
was not observed in £ IrittwUtiUt and ifsolicitation "penile despotism" as sociality involves larger jjtoup
occurred, il was loo last to be identified. However, tl size and requires a greater decree of intCettlUOll
is likely that individuals which enc-aged in "blk'etiJ Most i>ihcr highly eosoeutl species display diMinct
couiael" where nectar flow was observed, weiv moi'phs which are directly associated with diseivle
Irequcntly emj.aimj in tiophallaxts. Ttophallaxis bchavioural castes, involving minimal ornoagression
allows ietuales lo Iced without leaving llie nesL. The Considering lite presence of aijeressive interactions
presence ol trophalla*is in li tmlrntata thereioie within /.. iri</cnnifti colonies, it would seem (bat
allows behavioural specialisation where only some taCt&JtftfCl colony si/c and the dcvclopmciil o| moi
ol ihe lemalcs have lo lotape and other females can |tholi'tgiiii1 dilferenliation amone colons members
perform oilierduties ill lite nest. need not be accompanied by decreased levels .-!
f,\cnrurn iiHiciiialu exhibits asimilarrepertoire ot overt intra colony agression.
behaviours lo other allodapines (Macta ci nl. WW;
Hana «•/ at. IVW; Melna & Sehwar/ 1993).
Arknowlt'dijiiu'ni's
Hcbaviours reeouled in this study, including adult
adult interactions and adull-biood interactions, are
We would like to thank friends and laboraloiv
members who assisted with field work and N. Bull.
1 lIiJti aMn.ANn.Ot-I.ahIaMnW4A)lloI.'tuaspoiunaelihloyc,mitfakWltiCelattilVilaMnidwfpoolp'ulStaltliilolnl Sr.efeRreeyeess.forI*.adIvluircsel.onJ.thettimradnuasncrdipttw.oThainsorneysmeaorucsh
(ApislUtt. \vIneopnuH11. BSl (lions) thesi*. I linuViy was partially funded by grants from Lhe Australian
1 IaI'Inl*likvAemrussitlr)ValoifaSnSouA[tlhlWoAtdliustpiiaRnlekepirloluduuuop.cuht)i/..vetythhif"til'nUrchhiufriSth'iun DRUeIseatrvfcthh Tto>ncrnieudisslioonM,fFr'.oSm. lIihceldSwoourtkh wAausslcraarhraiietd
Strutli (Amliophoinlae, XyTOvOpMflC}, US' illnnM Dcparlrncnl ol linviioiimenl ami Natund Resources,
iin'M', I a fwihu I Into' rally innimh), permit no. Q23256-fljf. issued lo M. I'. S.
KWi'UMCCS
A!ilauiFHinu;,anihtnairs,pSil.itMu.1iu.\iVmC^1rnli|W'i7n+tth1lVeKi.kiaI/)hhnL>dMh«ii<tatmVn\M.il<i>a<iSlHnltofVJltKl.u.pi2uiSd3iKJ7tl\j\-)k<:\>w-7't.»'i-lUlimVduKitiM[vii|'fcMiiJusi1 Iti(.I1.Jtn1aianlsiHVii.imaciJSr.t<,e.eMMWittA»nhiMie/Ui.s.epJiAi>V.i'In.ettli-.I^J.hN'iloa(vKjpiiinvsaio.Alp.ih'rsiicainlvi...jlWY\.\t.iorvJpfiiuf.-.n."ti^'JvlsuyM.A'oi"n*iH,>
(ktltlkvHngiat,nopateisao:ciAarlitlp1oaprla1Mi>treidnein)..U/k-K}iink-wv.I\sliit/lhnHuntmmS",m'- CvnS»ir., ISfI(I,-tS,\vltiMpks fufliisiiv. I' t) i l<WM Itcmistiy and
GivAo-iloiHMstic11 BSciflULLL-v.-miaounh. TrsoVcIi.al$ 1iUnl(Ieia\eVuunJs..i p)a7nKd) (lhlSnlBlMlii.cfitVio.lt'i..Ii\5Uo_i\hisiim-ittasiin;Hliiv,linnielaMiop;ijeliaan:d Apnri.lKiloupchlsoioildaeheii;/..oClhntiun,.
/K/.KlfKtAWM.nVjrSatlxH'iPi'n-.em/lVi/s/avl>i.o2n5,ini5a|pMriUitHiivelv etisocial l^-e ll<»i,i \oookn. K $c S' uw\u/. M. J' tin pivs.vi Ctiiariliiii-
Hroiheis, H. I, £i MitliL-nn. <\ I) lll>74) Inieraeliuns in spatatisalioninptv-ivpmducuvi M^lonu^ot iliealloLlapine
loIoiiii:s iif potitiliselv sot-ial hc*?« III F.llinloniy tl| bet h..\<>ntitr<i hit >*!", Kitti/l t.t'l l:\.>l 10
idilvlivsiinocnnoptnc|ra (Haallliowc*liJaion. 7L.ilfSti»MNpg,lPMlJWhi\,i\'<'t:tlpHhlvmPiUn llohohtMVOSnt liFt.ehlU{Wh|ceMl7i?n)sNrcivltimlll)l;ttm»loMliocvh>ei"t'ei,.l,,/r/L'rm0Mv.iHlhf\t(JSJVI'f.t!
S l/n/_ 101 I I ;
BEHAVIOUR IN AN ALLODAPINE BEE 63
Hurst, P. S. & Schwarz, M. P. (1996) Morphological MiCHENER,C.D.(1965)Thelifecycleandsocialorganisation
differences among females of the eusocial allodapine ofbeesofthegenusExoneura andtheirparasite.Inquilina.
bee, Exoneura tridentata (Hymenoptera: Apidae). Univ. KansasSci. Bull 46, 317-358.
Proceedings of the XX International Congress of (1972) Activities within artificial nests of an
Entomology, Firenze Italy 25-31 August, p. 413. allodapine bee. ./. KansasEntomol. Soc. 45, 263-268.
Jeanne, R. L. (1986)The evolution ofthe organisation of (1974) "The social behaviour of bees: a
Maewtoar,kYi.n,sSoacikaalgainmsie,ctsS..MEon&itMokrehktnooelr,,JtaCl..D2.0,(1191992-)133. cUnoimvpearrsaittiyvePresstsu,dCy"amb(rTihdegeB,eMlaksnsaapchuPsreetstss)o.f Harvard
Laboratory studies on the behaviour and colony (1975) A taxonomic study of African allodapine
Tstariuwcatunre(oHfymBernaoupntsearpai:s hAenwtihttoip,hoariXdyaleo)c,opUinniev.beKeanfsraosm- bees. Bull Amer. Mus. Nat. Hist. 155, 67-240.
Sri. Bull. 54, 289-333. Schwarz, M. P. (1994) Female biased sex ratios in a
Mason.C.A (1988) Divisionoflabourandadultinteractions facultatively social bee and their implications forsocial
i(nHyemuesnoocpitaelrac:olAonntihoepshoorfidtaweo).aJl.lKoadanpsianseEnbteoemoslp.ecSioec.s evoluti&on.OvEevrolhuotlito,n L4.8,A.16(8149-9136)97M.ethods for rearing
61,477-491. allodapine bees in artificial nests (Hymenoptera:
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