Table Of ContentPROC. BIOL. SOC. WASH.
104(3), 1991, pp. 613-619
A SCANNING ELECTRON MICROSCOPE STUDY OF
THE BUCCAL COMPLEX OF METAPENICULUS
ANTOFAGASTENSIS (COPEPODA: PENNELLIDAE)
Raul Castro Romero and Heman Baeza Kuroki
Abstract.—Thebuccalcomplexforthecopepodite, chalimusandadultstages
ofMetapeniculus antofagastensis Castro & Baeza, 1985 is examined and de-
scribed with the aid ofthe scanning electron microscope (SEM). Thejunction
between the labium and labrum ofthe buccal cone at the copepodite stage is
shown to be affected by the insertion ofthe edges ofthe former between the
dorsal and the ventral plates derived from the latter and linked together by a
vertical bridge. The formation ofthe proboscis, followingthe process ofmeta-
morphosis, results in the displacement of the buccal area from the ventral
surface ofthe cephalothorax and from the second maxillae, which remain in
their original position on that surface. The intrabuccal armature is described,
as is the mandible at different developmental stages. Differences in the mor-
phology of the buccal region of Peniculus and Metapeniculus are described.
Reference is made also to the genus Ophiolernaea.
Thebuccalareaofthecopepodsparasitic is very small anddifficultto studyin detail,
on fishes is still inadequately known. Ka- specially in the pennellid copepods.
bata (1974) described the structure of the Intheirsearch for some structural details
buccaltubewithitsassociatedmusculature, thatcouldthrownewlightonthetaxonomy
aswellastheoralappendagesandthemode ofthe Pennellidae, the authors studied the
&
of feeding of Caligus (Caligidae), an ecto- buccal complex ofMetapeniculus Castro
parasite genus. A similar description was Baeza, 1985 and compared it with that of
published for the genus Lepeophtheirus by PeniculusvonNordmann, 1832.Thispaper
Boxshall(1984).Severalauthorsstudiedthe illustrates and discusses the results ofthis
oral region ofmesoparasitic (Kabata 1979) study.
copepods belonging to the family Pennel- Methods.—S^QcirciQns of M. antofagas-
lidae. Gooding & Humes (1963) described tensis, copepodites,chahmusandadult,were
the buccal area ofHaemobaphes cyclopteri- collected from their host fish (Anisotremus
na and John & Nair (1973) that of Ler- scapularis), both juvenile and adult. Some
naeenicushemirhamphianddiscussedtheir fish were taken from their natural environ-
functionalmorphology. ICabata(1979)gave ment, while others were reared in a labo-
a general account of this area in Poecilo- ratory. The copepods were washed in sea
stomatoida and commented also on the water that was filtered through a millipore
structure ofthe buccal tube ofPennellidae. filter. They were rinsed in IM urea to re-
Recently, Chandran & Nair (1988) gave an move fish mucus from the attached speci-
accountofthefiinctionalmorphologyofthis mens, fixed in gluteraldehyde (4%). They
area in Pseudocharopinus narcinae. were dehydrated in ethanol, critical point
In spite ofthese publications, the buccal dried and then coated with gold or silver,
tube and the intrabuccal armature is still observed and photographed under an Au-
inadequately known, because this structure toscan or Jeol Scanning Electron Micro-
614 PROCEEDINGSOFTHEBIOLOGICALSOCIETYOFWASHINGTON
scope at 20 Kv. Lightmicroscopydrawings Adult (Figs. 8-11).—The peribuccal area
were made with the aid ofa camera lucida. ischangedduetothedevelopmentofapro-
boscisthatpushesthesmallbuccalconeand
Results tube away from the surface of the cepha-
Copepodite(Figs. 1, 2).—Thebuccaltube lroetdhuocreadx(aFnidg.s8i).mpTlhee, lwahberruemasistnhoewlgarbeiautml,y
(Fig. 1) is formed by both the labium and whichformsmostofthebuccaltube,consist
labrum. The former forms most ofthe cir-
of three heavily sclerotized rings and is
cumference ofthe tube and bears a fringe
armedwith a distalringofsetules. The dis-
of setules at its distal end. The latter is a
tolateral surface of the buccal cone bears
subtriangular plate, connecting with sub-
cylindrical plate by means of a vertical several microvellosities (Fig. 9, mi). The
bridge. Two intrabuccal stylets are present mandibleisdifficulttostudyduetoitssmall
size. As far as can be seen, in the adult co-
on the inner surface ofthe labrum near its
distal end. The stylets are short, robust and pepod it is a simple stylet, devoid ofden-
tition. The second maxilla remains at its
surmounted by a single setiform process.
original position close to the base of the
The first maxilla (Fig. 2) is located at the proboscis. Theintrabuccalstructurehasthe
baseofthelabium.Ithastheusualpennellid
appearanceoftwolong,widelaminae(Figs.
structure. Its exopod is a single seta with a
robustbase,whereasitsendopodcarriestwo 3, 10, 11)arisingfromthebaseofthelabium
(that is starting from the buccal cone area)
long setae. Posteromedial and close to the
with some folding near their tips (Fig. 10,
first maxilla is the mandible, which is an ia), and reaching the buccal opening when
unsegmented stylet with a bifid apex (Fig.
2). Thesecondmaxillaisbi-segmented, and the buccal tube is contracted.
is situated posterior to the labrum. Its first
Discussion
segment (=lacertus) and second segment
(=brachium) are unarmed. The distal claw ThebuccalapparatusofPennellidaecon-
carries several spines apically. sistsoftheconeandtube,theformerformed
Chalimus I and III (Figs. 3-7).—At the bythefusionofthelabrumandlabium(Ka-
firstchalimus stages(Fig. 3)theanteriorin- bata 1979). Ithasnowbeenrecognizedthat
ner surface ofthe labium is produced into the labrum produces a ventral plate (cutic-
two prominent plate-like swellings (Fig. 3). ular process of Gooding & Humes 1963;
At the third chalimus stage (Figs. 4, 5) the dorsal plaque ofKabata 1979). Gooding &
structure of the buccal cone and tube ap- Humes (1963), suggested that the plaque
proaches its definitive condition; the la- fused with the labium. This would prevent
brum and labium are linked at their distal thetubefromtelescopingtoanyappreciable
ends. The upper margin ofthe labium are extent, although Kabatapostulatedthatthe
inserted between the subtriangular dorsal pennellid tube can telescope. The structure
plate (dp) andsubcircularventralplate (vp) of the buccal tube of Metapeniculus sup-
(Fig. 6). At this stage the projections ofthe portsKabata'sassertion. Thetelescoping(of
inner surface ofthe labium and the intra- thebuccaltube)is madepossibleduetothe
buccal armature ofthe tube reach their de- lose insertion ofthe distal upper margin of
finitive shape (Fig. 7) (Chalimus III is the the labium, between the dorsal and ventral
juvenile stageforthisgenus). The mandible plates derived from the labrum, allowing
enters the buccal tube through an opening free movement ofthe labium. The buccal
at the junction ofthe labium and labrum. tube, supported by three incomplete scler-
Other appendages retain their original po- otized rings, is common for all genera of
sition. Pennellidae. While in the majority ofthese
VOLUME 104, NUMBER 3 615
Figs. 1-3. Copepodite andchalimus I ofMetapeniculusantofagastensis. 1. Copepodite, frontal view ofthe
buccalarea, showingthelabium, andthedorsalandventralplates. 720x (LA = labium, DP = dorsal plate, IS
= intrabuccalstylet, SA = secondantenna, VP = ventral plate, RI = rim).
2. Copepodite,detailofthefirstmaxillaandmandible. 1730x (fm = firstmaxilla,M = mandible). 3. Chahmus
I, detailofthe labium, showingthe plate-like swellings. 600x (A = plate-like swellings, LA = labium).
616 PROCEEDINGSOFTHEBIOLOGICALSOCIETYOFWASHINGTON
Figs. 4-7. Chalimus III and premetamorphosis female ofMetapeniculus antofagastensis. 4. Chalimus III,
buccalarea, lateralview. 400x (BT = buccaltube, BC = buccalcone, FA = firstantenna, FM = firstmaxilla,
SA = secondantenna). 5. Chalimus III, buccaltube, dorsal view, showingthedorsalplate position. 800x (RI
= rim, DP= dorsalplate), 6. ChalimusIII, detailuppermarginoftherim showingtheinsertionofthelabium
betweenthedorsalandventralplates. 400x (ri = margin, vp= ventralplate,dp = dorsalplate, p = bridge). 7.
Premetamorphosingfemale,showingtheintrabuccalarmature.400x (ibs=intrabuccalstylet,lA=intrabuccal
armature, LM = lamina, RI = rim).
VOLUME NUMBER
104, 3 617
Figs.8-11. AdultfemaleofMetapeniculusantofagastensis.8.Adultfemale,cephalicarea,showingtheproboscis
andbuccal area. 52x (PR = proboscis, L = labrum, Sm = second maxilla, N = neck, R = fin ray fragmentof
host fish). 9. Buccal tube detail showing the microvellosities (MI = microvellosities, dp = dorsal plate, Im =
lamina). 10. Detail ofplate-like swelling(= intrabuccal armature) in a buccal tube longitudinal section. 800x
(lA = intrabuccal armature, ibs = intrabuccal stylet). 11. Detail ofthe buccal area, showing the intrabuccal
armatureasseenbytransparence(ia=intrabuccalarmature,bt=buccaltube,be=buccalcone,pr=proboscis,ri
= rings ofthe buccal tube).
genera the buccal area is situated close to velopment of a prominent proboscis, re-
theventralsurfaceofthecephalothorax(i.e., sulting from the activity ofthe oral devel-
a short buccal area in Peniculus and Ler- opment centre (Kabata 1979). The length
naeenicus) in Metapeniculus it is displaced ofthe proboscis is exceeded only by that of
away from it as the consequence ofthe de- OphiolernaeaShiino, 1958. Boxshall(1986)
618 PROCEEDINGSOFTHEBIOLOGICALSOCIETYOFWASHINGTON
pointed out thatPeniculus elongatus shows Thestructureoftheadultmandible,how-
an incipient proboscis, indicative ofa ten- ever, requires further study. In this respect
dencytowardstheelongationofaproboscis also, there exist clear differences between
in this family. Peniculus andMetapeniculus in these mor-
The existence ofa prominent proboscis phologicaldetails. Furtherstudyofthebuc-
inMetapeniculus supports Boxshall's view. cal region might disclose differences of a
Although the genera Peniculus and Meta- similar kind in different genera ofthe fam-
peniculus share similar attachment sites on ily.Theknowledgeofthesedifferencesmight
theirrespective hoststhe relativelengths of lead to a better understanding ofthe func-
theirproboscis differconsiderably. The po- tional morphology ofthis area and of the
sition ofthe second maxilla also varies be- evolutionary trends exhibited by the pen-
tweenpennellidgenera. InMetapeniculusit nellid copepods.
remains at its original position at the base
of proboscis, but in Ophiolernaea it mi- Acknowledgments
grates with the buccal area to the tip ofits
Specialthanksareextendedtothestaff"of
extraordinarily long proboscis close to the
first maxilla (cf. Ho 1966: figs. 25-27). Electron Microscopy ofthe Universidad de
Concepcion, and Universidad Catolica del
The buccal apparatus was hitherto be-
Norte (Sede Coquimbo), fortheir technical
lieved to consist ofthe mandible, first and assistanceandtoallthosepeoplewhohelped
secondmaxiUaeandintrabuccalstylets. This
us collect samples, and to anonymous re-
study disclosed the presence of another
viewerswhoimprovedthefinalmanuscript.
component ofthis apparatus, the two long
This study represents a portion ofa project
plate-like swellings derived from the prox- sponsored by FONDECYT 0069/88.
imalpartofthe innersurfaceofthe labium.
They are very difficult to observe with the
aid ofa low magnification and can only be Literature Cited
detected in specimens made translucent by Boxshall, G. A. 1984. The comparative anatomyof
treatmentwithlacticacidandobservedun- the feedingapparatus ofrepresentative offour
der higher magnification. The laminae are orders ofcopepods.—Proceedings of the Sec-
already present in the copepodite stage and ond International Conference on Copepoda.—
Syllogeus 58:158-168.
ccohmalpilmeutse stthaegier. Bdyeveerloodpimnegnttheathotshtetifsisnuael p.en1n9e8l6l.idA(Cnopeewpogdean:usSaipnhdontowsotonmeawtosipdeaci)esanodf
the laminae are probably able to supple- an analysis ofevolution within the family.—
ment the function of the mandible, es- SystematicParasitology 8:215-225.
pecially when the latter is short and weak Castro, R., & H. Baeza. 1985. Metapeniculus anto-
as in Metapeniculus. The shape ofthe ar- fagastensisgen. etsp. nov. (Copepoda: Pennel-
lidae) parasitic on two inshore fishes ofAnto-
mature appears to be different in Metapen- fagasta, Chile, South Pacific—Crustaceana49:
iculus and Peniculus. (Their shape for the 22-29.
latterofthesegeneraisnowbeingexamined Chandran,A., &N. B. Nair. 1988. Functionalmor-
by the authors.) phologyofthemouthtubeofthelemaeopodid
The pennellid mandible is usually bipar- Ppseepuoddao:chaSriopphionnuosstnoamractioniadea)(.Pi—llaHiy,dr1o9b6i2o)lo(Cgoi-a
tite and armed with teeth, e.g., in Lernae- 167:629-634.
ocera (see Kabata 1962) and in Haemo- Ho,J.S. 1966. ThreespeciesofFormosancopepods
baphes (see Gooding & Humes 1963). The parasiticon fishes.—Crustaceana 11:163-177.
mandible ofMetapeniculus, in contrast, is Gooding, R., &A. G. Humes. 1963. External anat-
omyofthefemaleHaemobaphescydopterinaa
unsegmented, bifid at the copepodite stage copepodparasiteofmarinefishes.—TheJournal
and apparently undivided at the apex and ofParasitology49(4):663-667.
devoid ofteeth in the adult. John, S. E., & N. B. Nair. 1973. Structure ofthe
VOLUME 104, NUMBER 3 619
mouthtubeandmethodoffeedinginLernaee- Nordmann,A.von. 1832. MikrographischeBeitrage
nicus hemirhamphiKirtisinghe, a parasitic co- Zur Naturgeschichte der wirbellosen. Thiere.,
pepod.—ZoologischerAnzeiger 190(l/2):35-40. G. Reimer. Berlin 2:1-150.
Kabata,Z. 1962. Themouthandthemouthpartsof Shiino,S. 1958. CopepodsparasiticonJapanesefish-
Lernaeocera branchialis (L), a parasitic cope- es. 17 Lemaeidae.—ReportofFaculty ofFish-
—
pod. Crustaceana 3:311-317. eries,PrefecturalUniversityofMie3(1):75-100.
. 1974. Mouth and mode offeeding ofCali-
gidae (Copepoda), parasites offishes, as deter- Universidadde Antofagasta, Facultad de
mined by light and scanning electron micros- Recursos del Mar, Departamento de Acui-
copy.—JournaloftheFisheriesResearchBoard
ofCanada 31:1583-1588. cultura, Casilla 170, Antofagasta, Chile.
1979. ParasiticCopepodsfromBritishfishes.
.
RaySociety, London, 468 pp.
