Morphology and ultrastructure of the pygidial gland of the ant Dinoponera australis (Hyemenoptera, Formicidae).

8 Pages·1995·0.32 MB·English

by  Billen, J.

B'.den, T. i:fxX8rani5o,C.R.r Paiv/a Rv.S.
1995.
Papeis Avulsos de Zoologia
MUSEU DE ZOOLOGIA DA UNIVERSIDADE DE SAO PAULO
ISSN0031-1049
Papeis Avulsos Zcxdl,S.Paulo. 39(9)209-216 20.VII.1995
MORPHOLOGY AND ULTRASTRUCTURE OFTHE PYGIDIAL
GLAND OFTHE ANTDINOPONERA AUSTRALIS
(HYMENOPTERA, FORMICIDAE)
JOHANBiLLEN '
CarlosRobertoF. Brandao^
RiCARDO V. S. Paiva^
Abstract
Thepygidialglands o/Dinoponera australis appearastwo verylarge
cell clusters underneath the anterior margin on either side ofthe seventh
tergite. Thepolygonalsecretorycellsare associatedwith slenderduct cells,
thatcarrythe secretion into thereservoir, which isformedbythe invaginated
intersegmental membrane between the 6th and 7th tergites. Ultrastructwal
examinationrevealstheoccurrenceofavesicularsmoothendoplasmicreticu-
lum, a well developed Golgi apparatus and abundant mitochondria. These
characteristics maycorrespondwith the elaboration ofapheromonal secre-
tion. Thepygidialglandinthisspeciesisprobablyinvolvedinitsgeneralized
recruitmentsystem.
Keywords: Dinoponera australis, morphology, pygidial gland, ultrastructure.
1.ZoologicalInstitute,UniversityofLeuven,Naamsestraat59,B-3000Leuven(Belgium).
2.MuseudeZoologia,UniversidadedeS5oPaulo,C.P.7172,01064-000SSoPaulo,SP(Brasil).
Trabalhorecebidoparapublica(3oem01.11.1994eaceitoem 11.04.1995.
210 PapeisAvulsosdeZoologia
Introduction
Social insectsin general andants inparticulararecharacterizedbyan
overwhelming varietyofexocrineglands thatarefoundall overtheirbodies,
andthatamounttoatotalof39differentglandsfortheFomiicidaeonly(Billen,
1994). Among the abdominal glands, one group is associated with the sting
apparatus, another is formed by glands that are associated with the tergites
andstemites. Additional,butmuchsmallerintersegmentalglands,canbeclas-
&
sified as tergostemal, dorsolateral and lateroventral in position (lessen
Maschwitz, 1983). Thepygidialglandisthemostconspicuoustergalglandin
ants, and occurs as a paired structure that opens through the intersegmental
membranebetween the6thand 7th tergites. It isextremelydevelopedamong
&
theDolichoderinae (Pavan Ronchetti, 1955).
The pygidial glands in general are involved in the secretionofphero-
monalsubstances,althoughthereisnocommoncharacteristicfunctionforthe
Formicidae in general. Among the several known pheromonal functions are
&
theelaborationofalarmsubstances(Pavan Ronchetti, 1955; Kugler, 1979),
&
trailpheromones(Simon Hefetz, 1991),recruitmentpheromones(Maschwitz
&Schonegge, 1977),sexpheromones(HOUdobier&Haskins, 1977),andsmear-
ing substances (lessen & Maschwitz, 1983). A survey ofthe general appear-
&
ance ofthe pygidial gland in ants is given by HSlIdobler Engel (1978),
illustrating itswidespread occunence in members ofall subfamilies, includ-
ingtheFormicinae, where itwaspreviouslythought notto occur(Hfilldobler,
1984). Ultrastructuraldatadealingwiththepygidialglandsofararerestricted
toadescription ofthegland in Dolichoderinae (Billen, 1986).
Queenlessness isawidespreadphenomenon in ponerineants, and has
recently received intense attention, especially as to the reproductive differen-
tiation and social organization (see revision in Peeters, 1991). The role of
exocrineglandsinthebiologyofqueenlessspecies, however, ispoorlyknown.
Oldham et al. (1994) compared the volume and contents ofthe mandibular
glandsofall membersofacolonyofDinoponeraaustraliswiththereproduc-
tivestatusoftheworkers, notingalargedifferenceintheamountofsecretion
between thegamergate (matedworker) and its non-matednestmates.
Inthepresentpaper,wereportonthemorphologyandultrastructureof
thisgland in the queenlessponerineantD. australis.
MaterialandMethods
A nest ofDinoponera australis was excavated at Itirapina, SP, Brasil,
andthepygidialglandsofallindividualsfound(thegamergateand 12workers)
Vol. 39(9), 1995 211
were fixed in 2% cold glutaraldehyde, buffered at pH 7.3 in 50 mM Na-
cacodylate and 150 mM saccharoseandpostfixed in 2%coldosmium tetrox-
ideinthesamebuffer. Afterdehydrationinagradedacetoneseries,theglands
wereembeddedinaralditeandsectionedwithaReichertUltracutEmicrotome.
Sections were stained in a LKB 2168 Ultrostainer and examined in a Zeiss
EM900 electron microscope. Semithin sections were stained with methylene
blueandthionin. Glandsforscanningmicroscopywerefixedinthesameway
astissuesfortransmission microscopy, afterwhichtheyweredehydrated ina
graded ethanol series and critical point dried in a Balzers CPD 030 instru-
ment, andviewed in aPhilips SEM515 microscope.
Results
ThepygidialglandinDinoponeraaustraliscomprisesaleftandaright
very largeelongate cluster ofpolygonal secretory cells (diameterapprox. 40-
50 /jm) with rounded nuclei, underneath the anterior margin ofthe 7th ab-
dominal tergite, bilaterally disposed (Fig. 1). Each cluster measures approx.
800 //m on an abdominal cross section, by 150 //m on a longitudinal section
(Fig. 2). A rough count leads to an estimate ofapproximately 300 secretory
cellspercluster. Theglandularcellsare individuallyconnectedthroughasso-
Fig. 1. SchematicaldrawingofaDinoponeraaustralisworkershowingthepositionoftheleftpy-
gidialglandcluster(arrow).Scalebar0,5cm.
212 PapeisAvulsosde2)oologia
sc
Vol. 39(9), 1995 213
ciatedductcellswiththepygidialglandreservoir(Figs. 3, 4),whichisformed
by an invagination ofthe intersegmental membranebetween the 6th and 7th
abdominal tergites. Asthis invagination is rathernarrow, however, the reser-
voir has a relatively small volume. There is no muscular supply associated
with thegland nor with its reservoir.
Each secretorycell ischaracterizedby the intracellularendapparatus,
which consistsofa microvillarsheath surroundingthecentral cuticularduct,
which hasan internal diameterofapprox. 0.4//m. Thecuticular liningofthe
ductischaracterizedbyadiscontinuouselectron-denseepicuticle(Fig.5). The
microvillarpattern maydisplayanorderly arrangement(Fig. 5) ormay show
conspicuous extracellular spaces that force the microvilli to occur in a more
loosepattern (Fig. 6). Thecytoplasm ischaracterizedbyanabundance ofmi-
tochondriaandawell developedGolgi apparatus(Fig. 7), aswellasanelabo-
rate smooth endoplasmic reticulum ofthe vesicular type (Fig. 6). Spherical
lamellar inclusions with adiameteraround 1 /im canbe observed, especially
in theregion oftheendapparatus, wheretheyoccurinbetweenthe microvilli
(Fig. 5). Theductcells arecharacterizedbya much reducedcytoplasm, anda
continuouscuticularductwithaninternaldiameteraround 1//mandacuticu-
lar lining ofappro.x. 0.2 jum (Fig. 8).
Wewerenotabletofindanysignificantdifferencebetweentheglandand
reservoir ofthe gamergate and the non-mated workers. In the laboratory and
fieldconditions,weobservedseveraltimespairsofworkersintandem,thatis,a
workerfollowingaleaderworker, keepingphysical contactwithitbymeansof
slightandrepeatedtouchesoftheantennaetothegasterdorsumofthe leader.
Discussion
The pygidial gland represents one ofthe most conspicuous exocrine
elementsinthegiantNeotropicalantDinoponeraaustralis.Theglandisformed
bynumerousbicellularunits, eachconsistingofasecretorycellanditsaccom-
panying duct cell, which therefore correspond to the class 3 glandular cells
following theclassificationofNoirot&Quennedey(1974). Thesearecharac-
terized by the presence ofan end apparatus, that represents thejunction be-
tween the secretory cell and the duct cell. Size variation ofthe extracellular
spacethatoccursat thisjunction, duetodifferencesin thearrangementofthe
microvilli ofthe end apparatus, can probably be seen as an expression ofa
different stage in the cell's secretory activity, as has also been observed in
otherexocrineglands(Bazire-Benazet&Zylberberg, 1979). Thepossiblefor-
mation, foreach secretory cell individually, ofan additional reservoir space.
214 PapeisAvulsosdeZoologia
Figs, 5-8 (scalebarl/fln); 5. Detailoftheendapparatus,showingthefenestratedepicuticularlayer
ofthecentralduct,andlamellarinclusions(LI)inbetweenthemicrovilli(mv);6.Cytoplasmwithend
apparatus(EA),mitochondria(M)andwidecisternsofsmoothendoplasmicreticulum(SER);7.Cy-
toplasmicdetailshowingGolgiapparatus(GA)andmitochondria(M).N:nucleus;8.Crosssection
throughductcells.N:nucleus.
allows temporary storage ofsecretory products, which may be important for
glands with a rather small common reservoir, as in the present case ofthe
pygidial gland ofD.australis. In Dolichoderinae, on the other hand, the py-
gidial gland reservoir is extremely enlarged. For this reason, this gland has
Vol. 39(9), 1995 215
&
been erroneously interpreted as an 'anal gland' (Pavan Ronchetti, 1955;
Billen, 1986). In the Myrmicinae, theglandappearsto bemore developed in
the moreadvanced genera (Kugler, 1978).
The cytoplasm ofthe secretory cells contains a very well developed
smooth endoplasmic reticulum and Golgi apparatus, and an abundance of
mitochondria.Thesecharacteristicsaretypicalofpheromoneproducingglands,
where non-proteinaceous molecules oflow molecular weight are elaborated
(Noirot & Quennedey, 1974; Billen, 1991). The lamellarinclusions probably
representthesecretoryproducts, asisalsoillustratedbytheiroccurrencenear
to oreven inbetween the microvilli ofthe endapparatus, wherethey maybe
&
on theirway to the reservoir(Hefetz Orion, 1982; Billen, 1986).
The observation offrequent tandem running, with contacts between
individuals involvingtheplacewherethepygidial glandsare located, theab-
sence ofa muscularsupply associatedwith thegland orits reservoir, and the
absence ofvolatile substances in the gland and its reservoir, suggest that the
pygidial gland in Dinoponera australis may be constantly producing and re-
leasingcontactpheromonesofrelativelylowvolatility, employedintheirgen-
eralized recruitment system. Also the lack ofsignificant differencesbetween
the pygidial gland ofgamergates and non-mated workers suggests that this
gland is not involved in reproduction.
According to HOlldobler and Wilson (1990), the secretions ofthe py-
gidial glands in ponerine ants can function as tandem running pheromones,
recruitmentandtrail pheromones, orsexpheromones, dependingonthe spe-
cies and the behavioural context. In Pachyncondyla obscuricornis, Traniello
and Holldolber (1984) suggested that the secretion ofthe pygidial gland ap-
pears to be transferred to the hindlegs ofa tandem pair leaderby a series of
self-groomingbehavioursthatoccurpriortotheformationofatandempair. In
thisspecies theformationoftandempairs is relatedto nest migration, which
can also be the case ofDinoponera, as observed in D. gigantea by Overal
(1980). In spiteofapresumableinvolvementintheproductionofpheromonal
substances based on the ultrastructural characteristics, however, preliminary
chemical analysisofthepygidialglandsof D. australiscouldnotconfirmthe
presenceofanyvolatilecompounds (Oldham & Morgan, pers. comm.).
Acknowledgements
Weareverygrateful toJ. Cillis,D. CorstjensandE. Schoetersfortheir
help in specimen preparationforscanningandtransmissionelectron micros-
copy. ConselhoNacionaldeDesenvolvimentoCientificoeTecnol6gico,CNPq
andFunda^ao de Amparo kPesquisa do Estado de SSo Paulo, FAPESP, par-
tiallyfunded this study.
216 Papeis AvulsosdeZoologia
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