Setation And Setal Groups On Antenna 1 Of Ridgewayia Klausruetzleri, Pleuromamma Xiphias, And Pseudocalanus Elongatus (Crustacea : Copepoda

13 Pages·1998·4 MB·English

by  F D Ferrari

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111(1):209-221. 1998.
Setation and setal groups on antenna 1 ofRidgewayia klausruetzleri,
Pleuromamma xiphias, and Pseudocalanus elongatus (Crustacea:
Copepoda: Calanoida) during the copepodid phase
oftheir development
FrankD. Ferrari and AdamBenforado
(FDF)DepartmentofInvertebrateZoology,NationalMuseumofNaturalHistory,
SmithsonianInstitution,Washington, D.C. 20560U.S.A.;
(AB)2634WoodleyPlace,FallsChurch,Virginia22046,U.S.A.
—
Abstract. Setae added to the antenna 1 ofthree species ofcalanoid cope-
pods during copepodid development are allocated to setal groups present on
the adult antenna 1. Development ofthese setal groups is not homogeneous;
foragiven setal groupthe copepodidstage atwhichthefirst setaappearsand
at which setal addition is completed varies; whetherthe setal group is trithek
orquadrithek in adult males also varies. These variations suggest several sets
ofsetal groups as candidates for the presumed extra groups added duringthe
adaptionofan ancestral calanoidcopepodtothepelagicenvironment.Among
these, a set oflate developing setal groups is preferred. A model for adding
setal groups during copepodid development assumes three source groups are
responsiblefor adding 16 progeny groups.
Antenna 1 ofcalanoid copepods usually [Ps. elongatus]. We analyze setation pat-
consistsof25articulatingsegmentsinadult terns of antenna 1 during development of
females (Giesbrecht 1892) although 27 ar- thesethreecalanoids.Weallocateeachseta
ticulating segments have been found in ateach copepodid stageto asetal groupto
someadultfemaleepacteriscids(Fosshagen which the seta will be associated in the
1985). A calanoid antenna 1 with 27 artic- adult female antenna 1, and derive devel-
ulatingsegmentshasbeenexplainedinone opmental patterns foreach setal group. We
oftwo ways. The 27 segmented antenna 1 also discuss whether a homogeneous pat-
maybeastateforcalanoidswhichhasbeen ternofsetationispresentfromwhichallof
derived by fusion ofthe ultimate and pen- the setal groups in an ancestral 28-seg-
ultimate segments from an ancestral cope- mented appendage can be inferred, or
pod state with 28 segments (Huys & whetherseveralpatterns arepresentamong
Boxshall 1991). Alternatively, it may be a which is a pattern unique to a set of setal
state derived throughthe acquisitionofex- groupswhichcanbeidentifiedastheextra,
tra segments, as the result of adaption by derived setal groups of calanoids. Finally
an ancestral calanoid to pelagic habitats, wepresentamodelfortheadditionofsetal
fromanancestralcopepodstateofabout20 groups to antenna 1 during copepodid de-
segments (Stock 1991). velopmentofthe three calanoids.
Here we examine these two hypotheses
using data derived from the copepodid de- Methods
velopment of the calanoids Ridgewayia
klausruetzleri Ferrari 1995, Pleuromamma Ferrari(1995)describedantenna1during
xiphias (Giesbrecht 1889) [=Pl. xiphias] the copepodid phase ofdevelopment ofR.
andPseudocalanuselongatus(Boeck1865) klausruetzleri; Ferrari (1985) describedthe
.
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developmentofcopepodid (C)II-VIofPL ses of Andronov (1974) and Park (1985),
xiphias; andOberg(1906)describedanten- which revealed these relationships, used
na 1 for CI-IV ofPs. elongatus. Here we some of the same characters but neither
add descriptions ofantenna 1 ofCI ofPI. analysisincludedasacharacterthenumber
xiphiasandofCV-VIofPs.elongatus,and ofsegments ofantenna 1
redescribe the morphology of all of the
stageswhilecomparingthethreecalanoids. Results
The setose edge of antenna 1 has been
calledanterior(thedirectionofantenna1 is At CI, antenna 1 of all three calanoids
held in calanoids) (Hulsemann 1991) but has ten articulated segments. The setation
wenotethatamongtheremainingcopepod ofR. klausruetzlerifromtheproximalseg-
appendages, most setae are found on the mentis 3, 2, 1, 2,0, 1, 1, 3,2,7 (Figs. 1A,
ventral edge (in descriptive work usually 2E), and for PI. xiphias and Ps. elongatus
notedasmedial)ofanendopod;afewsetae it is 3, 2, 1, 2, 0, 1, 1, 2, 2, 7 (Figs. 3A,
arefounddorsally(usuallynotedaslateral). 4D, 5A, G).
Ifthe distal segments ofantenna 1 are en- AtCII,antenna 1 ofR.klausruetzlerihas
dopodalthentheanterioredgeofantenna 1 17 articulated segments with 1, 4, 0, 1, 0,
is ventral in copepods. The trithek/quadri- 2, 0, 1, 0, 1, 2, 1, 1, 1, 3, 2, 7 setae (Figs.
thekgroupingsofsetaeonantenna 1 (Gies- IB, 2D). Antenna 1 ofPI. xiphias has 15
brecht 1892) refers to the following set of articulated segments with two poorly ex-
setae: in the adult female a pair of setae pressed arthrodial membranes within the
originate close together often immediately third segment; there are 3, 4, 1, 2, 0, 1, 0,
proximaltoanarthrodialmembrane;oneis 1, 2, 1, 1, 2, 2, 2, 7 setae (Figs. 3B, 4E).
a simple seta and the second, usually a Antenna 1 ofPs. elongatus has 16 articu-
modified, poorly sclerotized seta often is lated segments with one poorly expressed
called an aesthetasc. A third simple setais arthrodial membrane within the first seg-
located proximal to the pair. In the CVI ment; there are 5, 0, 1, 0, 2, 0, 1, 0, 1, 2,
male a fourth, poorly sclerotized seta or 1, 1, 2, 2, 2, 7 setae (Fig. 5B, H).
aesthetasc maybepresentnearthelocation At CIII, antenna 1 of R. klausruetzleri
ofthe above-mentionedpair. has 24articulatedsegmentswith 1, 2, 1, 2,
Phylogenetic relationships among the 0, 1, 0, 2, 0, 1, 1, 1, 2, 1, 1, 1, 1, 3, 1, 1,
269 calanoid genera have not been pro- 2, 3, 2, 7 setae (Figs. 1C, 2C). Antenna 1
posed. The 43 calanoid families are ofPI. xiphias has 20 articulated segments
grouped into 11 superfamilies and phylo- withtwopoorlyexpressedarthrodialmem-
genetic relationships among eight or 10 of branes within the sixth segment; there are
thosesuperfamilieshavebeenhypothesized 5, 1, 2, 0, 1, 2, 1, 2, 2, 1, 1, 1, 1, 3, 1, 1,
respectively by Andronov (1974) andPark 2, 3, 2, 7 setae (Figs. 3C, 4F). Pseudoca-
(1986). Ridgewayia klausruetzleri [Ridge- lanuselongatushas 19articulatedsegments
wayiidae,threegenera]belongstothePseu- with poorly expressed arthrodial mem-
docyclopoidea [three families], one of the branes within the first, fifth, sixth and sev-
two presumed oldest superfamilies, along enth segments; there are 6, 2, 0, 1, 2, 1, 2,
with Epacteriscoidea; PI. xiphias [Metridi- 2, 1, 1, 1, 1, 2, 1, 1, 2, 2, 2, 7 setae (Fig.
nidae, three genera] belongs totheArietel- 5C, I).
loidea [eight families], the next most de- At CIV, antenna 1 of R. klausruetzleri
rived superfamily and presumedly the old- has 25 articulatedsegmentswith2, 3, 1, 2,
est superfamily of pelagic calanoids; Ps. 1, 2, 1, 1, 3, 1, 1, 3, 2, 2, 2, 3, 2, 2, 3, 1,
elongatus [Clausocalanidae, seven genera] 1, 2, 3, 2, 7 setae (Figs. ID, 2C). Antenna
belongs to the Clausocalanoidea [11 fami- 1 ofPI.xiphiashas23 articulatedsegments
lies] the youngest superfamily. The analy- withtwopoorlyexpressedarthrodialmem-
VOLUME111,NUMBER 1
Fig. 1. Proximalsectionofantenna1ofRidgewayiaklausruetzleri.A,CI;B,CII;C,CIII;D,CIV;E,CV;
E CVI female. Illustrations not to scale; proximal isdown; proximal section includes setal groups 1-20, if
present:setalgroupsarenumbered.
branes withinthe eighthsegment; thereare 3, 1, 1, 2, 3, 2, 7 setae (Figs. 3E, 4F). An-
7, 1, 2, 1, 2, 1, 1, 4, 1, 3, 2, 3, 2, 3, 2, 2, tenna 1 ofPs. elongatushas 23 articulated
3, 1, 1, 2, 3, 2, 7 setae (Figs. 3D, 4F). An- segmentswithtwopoorlyexpressedarthro-
tenna 1 ofPs. elongatus has 22 articulated dial membranes within the first segment;
segmentswithtwopoorlyexpressedarthro- there are 10, 3, 2, 3, 2, 2, 4, 1, 1, 3, 2, 3,
dial membranes within the first segment 1, 1, 1, 2, 2, 1, 1, 2, 2, 2, 7 setae (not il-
and one poorly expressed arthrodial mem- lustratedbut seeFig. 5E, I).
brane within the fourth segment; there are AtCVI,thefemaleantenna1 ofR.klaus-
7, 2, 1, 3, 1, 3, 1, 1, 3, 1, 3, 1, 1, 1, 2, 2, ruetzleri has 26 articulated segments with
1, 1, 2, 2, 2, 7 setae (Fig. 5D, I). 2, 5, 2, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3,
AtCV,antenna 1 ofR.klausruetzlerihas 3, 2, 2, 3, 1, 1, 2, 3, 2, 7 setae (Figs. IF,
26 articulated segments with 2, 4, 1, 3, 2, 2C). Antenna 1 ofPLxiphiashas 22 artic-
3, 2, 3, 2, 3, 2, 2, 3, 2, 2, 2, 3, 2, 2, 3, 1, ulated segments with three poorly ex-
1, 2, 3, 2, 7 setae (Figs. IE, 2C). Antenna pressed arthrodial membranes within the
1 ofPLxiphiashas23 articulatedsegments seventhsegment;thereare 10, 3, 3, 3, 3, 3,
withtwopoorlyexpressedarthrodialmem- 12, 3, 3, 3, 3, 3, 3, 3, 3, 3, 1, 1, 2, 3, 2, 7
branes withintheeighth segment; thereare setae (Figs. 3F, 4F). Antenna 1 ofPs. elon-
9, 2, 3, 2, 3, 2, 3, 7, 3, 3, 3, 3, 3, 3, 3, 3, gatushas 24 articulated segmentswithone
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Fig.2. Antenna 1 ofRidgewayiaklausruetzleri.A,proximalsectionofCVImale;B,distalsectionofCVI
male;C,distalsectionofCIII(distalsectionofCIV,CV,andCVIfemaleisidentical);D,distalsectionofCII;
E,distalsectionofCI.Distalsectionincludessetalgroups21-27;remainingexplanationasforFig 1.
poorly expressed arthrodial membrane 12th segments. Segment 12 bears distally
within the second segment; there are 3, 7, a segmental attenuation which appears
3, 2, 3, 2, 2, 4, 1, 1, 3, 2, 3, 1, 1, 1, 2, 2, similartotwostiff,poorly-articulatedsetae
1, 1, 2, 2, 2, 7 setae (Fig. 5E, I). found proximally on the segment; there
At CVI, the right male antenna 1 ofR. also is a stiff, poorly-articulated seta on
klausruetzleri has 24 segments with 2, 5, segments 10 and 11 (Fig. 4C). The right
2, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 3, 2, male antenna 1 of Ps. elongatus has 19
2, 5, 2, 3, 2, 7 setae (Fig. 2A, B); thereis segmentswith 12,4, 3,4, 3,4, 11, 2, 3, 2,
a geniculation between the 19th and the 2,2,3,2,2,2,2,2,7setae(Fig.5F);there
20th segments. The right male antenna 1 is no articulation. Morphology ofthe left
ofPI. xiphias has 15 segments with three antenna 1 ofthe CVI male is identical to
poorly expressed arthrodial membranes in that of the CVI female for all three cal-
the sixth segment and one in the seventh anoids.
segment;there are 12,4, 3,4, 3, 14, 10, 6, There is a posterior seta on each ofthe
3, 2, 3, 5, 5, 2, 7 setae (Fig. 4A, B); there lastfoursegmentsofallthreespeciesatall
is ageniculationbetweenthe 11th andthe six copepodid stages.
Fig. 3. Proximalsectionofantenna 1 ofPleuromammaxiphias. A,CI;B,CII;C,CIII;D,CIV;E,CV;F,
CVIfemale.Dottedlinesindicateincompletelyformedarthrodialmembranes;remainingexplanationasforFig1.
Discussion development, setae usually are conserved
The presence ofa proximal and a distal (an exception is the loss ofa setaby setal
arthrodial membrane delimiting a group of group 1 ofR.klausruetzleriduringthemolt
setaetraditionallyhasbeenusedtoidentify to CII); new setal groups usually bear one
pthreessseiognmenotfstohefaanrttehnrondaia1l. Vmaermibatriaonnesin,exa-s gsertoaup(sex1,ce3p,t2i1o,ns2:5,R2.6,kl27a;usPrLuextizplheiraissseettaall
described below, has led us to assign all groups 1, 3, 21, 25, 26, 27; and Ps. elon-
setae present at each stage ofdevelopment gates setal groups 1, 21, 25, 26, 27); ar-
to one of 27 setal groups present in the throdial membranes may establish the lo-
adultfemaleantenna 1 (Tables 1-3)without cation ofa setal group before the first seta
regard to the presence of arthrodial mem- ofthatgroup is formed (setalgroups 8, 10,
branes. Assignment of setae during cope- 12, 19, 22 of all three species); and setae
podiddevelopmenttoasetalgroupisbased are added to a group so that the trithek/
on the following four assumptions: during quadrithek groupings are conserved (a tri-
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Fig. 4. Pleuromammaxiphias. A, proximal sectionofrightantenna 1 ofCVImale (curvedarrowunites
setalgroup6withsetalgroup7);B,distalsectionofrightantenna1ofCVImale;C,detailofsetalgroups19-
23onCV(toright)andCVI(toleft)malerightantenna1 (longarrowneararticulationoftheproximalsetaof
setalgroup20;arrowheadsnearpoorlyarticulatedsetaeofsetalgroups 19-21;openarrownearattenuationof
segmentbearingsetalgroup22);D,distalsectionofCI;E,distalsectionofCII;F,distalsectionofCHI(distal
sectionofCIV,CV,andCVIfemaleisidentical).ExplanationsasforFig2.
thek/quadrithek grouping is not the out- taegenerallyagreeamongthethreespecies.
come for setal group 1). Theresultingadultfemaleseriesalignswith
Aside from truncations of setal addition the28-segmentedadultantenna1presumed
(Tables 1-3), developmentalpatternsofse- for the ancestral copepod by Huys &
VOLUME 111,NUMBER 1
Fig.5. Antenna 1 ofPseudocalanuselongatus.A,proximalsectionofCI;B,proximalsectionofCII;C,
proximal section ofCHI; D, proximal section ofCIV; E, proximal section ofCVI female (arrow indicates
arthrodialmembraneabsentinCV;otherwiseCVidenticaltoCVIfemale);F,CVImale;G,distalsectionofCI;H,
distalsectionofCII(distalsectionofOil,CIV,CV,andCVIfemaleisidentical).ExplanationsasforFig2.
Boxshall (1991) with the exception ofour occurs between homologous setal groups
distal setal group, which is represented by 20 and 21, as suggested for calanoids by
segmentsXXVIIandXXVfflinthe28-seg- Huys & Boxshall (1991) for their equiva-
mented adult ancestor. As a result of this lent segments XX and XXI. However, our
alignment,thegeniculationonantenna1for alignmentdoesnotmatchthatsuggestedby
themaleofR.klausruetzleriandPI.xiphias Oberg (1906) for CI-CIV of Ps. minutus
216 PROCEEDINGSOFTHEBIOLOGICALSOCIETYOFWASHINGTON
r~ r— r^ r— r~ r-— r— for which the four setae on the proximal
sectionofCIaresetalgroups9, 11, 16and
N N (N N N N (N 20, andnot setal groups 1, 7, 11 and 16 as
en m m m m proIpnocsoemdplheetree (aTrtahbrloedi3a)l. membranes vary
N N N (S among the stages of PL xiphias and Ps.
elongatus studied here. However, in all
cases the section of the arthrodial mem-
brane that was present was much thinner
than a complete arthrodial membrane, and
(N tN en m m tthhreodsieacltomreomfbtrhaenesegwmaesntabisnenwthiaclhwatyhse ianr--
cludedtheanteriorface.Theabovehypoth-
esized setal allotments result in a compli-
cated association of setal groups with ar-
throdial membranes. Earlyindevelopment,
m m m m arthrodialmembranesarenotexpressedbe-
tweensetalgroupsthatlaterindevelopment
"8 * becomeseparatedbyarthrodialmembranes;
e.g., setal groups 7 and 11 at CI, and setal
groups 3 and 7 at CII of all three species
cn <n m m are not separated by an arthrodial mem-
brane. Development ofPI. xiphias is more
complicated. There is no arthrodial mem-
brane between setal groups 3 and 7 at CII,
but there is an arthrodial membrane be-
tween setalgroups 1 and3. AtCIIIthelat-
ter arthrodial membrane is not expressed,
butanewarthrodialmembraneisexpressed
between setal groups 3 and 7; thus setal
o o —' fN group 3 becomes associated with setal
>—6 <oc» pgrreosuspio1n.Fiasilmuorreeofcaortmhmroodnialinmeamdublrtamnaeleesx;-
e.g., compare adult male and female setal
groups 3-4, 14-15, 16-17, 21-22, 22-23
cn <N tN m m m and 24-25 ofPL xiphias; setal groups 21-
E I 22 and 22-23 ofR. klausruetzleri; orsetal
groups 3-4, 10-11, 11-12, 12-13, 13-14
— <N m m m tahnrdee2c2a-l2a3noiodfs,Psf.aileulroengoaftuasrt.hrAodmioalngmetmh-e
brane expression proximal to one setal
group coupled with a new membrane ex-
rN eN m rn m m pression distalto the same setal groupdur-
ing immature copepodid development is
found only in PL xiphias. However, this
patternmayexplainthephenomenonofse-
tae that appear to jump across article
H B ft B C > > > b(oGurnydgaireires199a4t).molts in other crustaceans
VOLUME 111,NUMBER 1 217
r-~ r~- r- r» r- r- r~ There is no evidence from the setal de-
velopmentpatterns ofthesethreecalanoids
for a homogenous pattern of setal devel-
opment for all ofthe setal groups. The ad-
dition ofthe first seta to a setal group ex-
hibits little variation; an exception is setal
group2ofR.klausruetzleriwhosefirstseta
appears at CV, rather than CIV as for the
other two species (Table 4). However, not
allsetalgroupsbeginwithasinglesetaand
(N (N f^t^ m n(^ tnhoitrdallsesteatadlurgirnogupsconatdidgutohueisrmsoelctosn.dTahnids
(N co co m lack of homogeneity may result from the
additionof16setalgroupsduringonlyfive
O —' cn co co (N copepodidmolts, unlikethethoracopodsin
which up to three setal groups are added
during five copepodid molts. Alternatively
these groups may not be homogeneous in
theirdevelopmentbecausethey arenotev-
olutionarily equivalent; ifthe ancestral co-
pepodpossessedfewerthan27setalgroups,
thendifferentsetsofsetalgroupsmayhave
been added to antenna 1 at different times
co co co co during evolutionto the calanoids.
Setal groups can be divided into several
setsthatdifferinthenumberofsetaepres-
entin each group ofthe adult male, orthe
initialconditionofthesetalgroupinitsear-
liestcopepodidstage, orthedevelopmental
patternofthesetalgroup.Wewillexamine
O O —' <N co these sets for evidence of a set of setal
groups that were added secondarily to the
ancestral copepod state as an adaption to
thepelagic environment.
There are no quadrithek setal groups on
themaleantenna 1 ofR.klausruetzleri,per-
haps because these animals spend part of
eachdayinmonospecificswarms(Fosshag-
— (N CO CO emnal1e99r1e,ceFpetrirvaerito19m9a5)t,inwghemraeyfinnodtinrgeqauifree-
searching a significant volume ofwater. If
quadrithek setal groups are an adaption of
M (N <N CO calanoid males to search for receptive fe-
malesinsignificantvolumesofpelagicwa-
ter,quadritheksetalgroupsmaybetheextra
setal groups of calanoids. We do not con-
siderthe first setal group, whichbearsfour
setaeinbothadultmalesandfemalesofPI.
xiphias, to be a true quadrithek. There are
'
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five other setal groups (5, 7, 9, 11, 13) of
the male ofPL xiphiasthatbearfoursetae
N N N N N N N including a distinctive flask-shapedaesthe-
tasc peculiarto the males. However, seven
other setal groups (2-4, 6, 8, 10, 12) with
13 - N N M M only three setae also bear a distinctive,
male-specific, flask-shaped aesthetasc.
§ 8 Males ofPs. elongatus alsohavefive setal
a * groups (5, 7, 9, 11, 14) of four setae, but
seven other setal groups (4, 6, 8, 17-20)
bearing one more aesthetasc than the fe-
male.Differingnumbersofquadritheksetal
—i tN (N (N mgrooluopgsyaonfdsoanmeapseptaarlengtroluapcskboefarsienrgiaqluahdo--
ritheks, or distinctive or extra aesthetascs,
suggests that setal groups with these iden-
tities are unlikely candidates for the set of
extrasetal groups ofcalanoids.
The initial condition of setal groups is
variablebutwecan identifytwo sets: aset
of five groups (8, 10, 12, 19, 22) whose
— —i (N location initially is establishedbythepres-
ence of a proximal and a distal arthrodial
membranebefore the first setaofthatsetal
groupappears; andasetofsixsetalgroups
(1, 3, 21, 25, 26, 27) that initially appear
O O -< — withmorethanoneseta.Eitherofthesese-
tal groups are likely to be the extra set of
h NN N CIn the calanoids.
Setal development patterns also may be
O O — -H , used to identify extra setal groups. In the
caseofadultfemales,therearesetalgroups
that complete development late (those for
whichsetationbecomescompleteatCVIor
thoseforwhichthethirdsetaofthetrithek
h h is is nn ^ is added atCVI), and setal groups thatbe-
gin development late (those for which the
first seta appears at CIV) (Table 4). While
thenumbersofsetalgroupsineachofthese
categories usually differ (Table 5, columns
— C-E), the setal groups, when present, are
(N (N
always homologous among the three spe-
cies and are always found among the fol-
lowing set of setal groups: 2, 4, 6, 8, 10,
and 12. Webelievethis setisthebestcan-
didate for the set of extra setal groups of
u -2 -S calanoids,becausedevelopmentofthesesix
H «£ do. setWalegrhoyupposthiessiinzietitahtaetdsaonmdeteorfmtihneatleadteladtee-.