The cephalic sensory organs of Acteon tovnatilis (Linnaeus, 1758) (Gastropoda Opisthobranchia) - cellular innervation patterns as a tool for homologisation

2007·0.98 MB·

by  Staubach, Sid

© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
Bonnerzoologische Beiträge Band 55 (2006) Hcfl 3/4 Seiten 311-318 Bonn, November2007
The cephalic sensory organs ofActeon tovnatilis
-
(Linnaeus, 1758) (Gastropoda Opisthobranchia)
cellular innervation patterns as a tool for homologisation*
Sid Staubach & Annette Klussmann-Kolb"
^^Institute for Ecology. Evolution and Diversity ~ Phyiogeny and Systematics,
J. W. Goethe-University, Frankfurt am Main, Germany
*Paperpresented tothe 2nd Intemational Workshopon Opisthobranchia,ZFMK, Bonn, Germany, September20th to 22nd, 2006
Abstract. Gastropoda are guided by several sensory organs in the head region, referred to as cephalic sensoi"y organs
(CSOs). This study investigates the CSO structure in the opisthobranch,Acteon lonuitiliswhereby the innervation pat-
terns ofthese organs aredescribed usingmacroscopic preparations andaxonal tracingtechniques.
Abipartite cephalic shield and a lateral groove along the ventral side ofthe cephalic shield was found in A. toniatilis.
FourcerebralnervescanbedescribedinnervatingdifferentCSOs:Nl: lip,N2:anteriorcephalicshieldandlateralgroove,
N3 andNclc: posteriorcephalic shield. Cellularinnervation patternsofthecerebral nervesshowcharacteristic andcon-
stantcell clusters in theCNS foreach nerve.
Wecompare these innervation patterns oíA. tonuitilis with those described earlier forHaminoea hydatis (Staubach et
al. inpress). Previously established homologisation criteria are used in order to homologise cerebral nerves as well as
the organs innervatedby thesenerves. Evolutionary implicationsofthishomologisationarediscussed.
Keywords.Haminoea hydatis, Cephalaspidea, axonal tracing, homology, innervation patterns, lip organ, Hancock's
organ.
INTRODUCTION
1.
Gastropoda are guided by several organs in the head re- phylogenetic position of Acteonoidea within Opistho-
gion which are assumed to have primarily chemo- and branchia unsettled. Acteonoidea are characterised by the
mechanosensory functions (Audesirk 1979; Davis & presence ofaprominentcephalic shield. This structure is
Matera 1982; Bicker et al.1982; Emery 1992; Chase alsopresent inCephalaspidea and hasbeenconsideredto
2000; Croll et al. 2003). In Opisthobranchia, these beanapomoiphieoftheCephalaspidea(Schmekel 1985).
cephalic sensoryorgans (CSOs) present an assortment of However,thestructureofthecephalic shieldsdifferscon-
forms including rhinophores, labial tentacles, oral veils, siderably in CephalaspideaandActeonoideawith the lat-
Hancock'sorgansandcephalic shields. Recentinvestiga- terpossessingtwodistincthemisphereswhilethecephal-
tions ofCSOs in Opisthobranchia have focussed prima- ic shield intheCephalaspideapossesses unifomi structure.
rily on functional aspects (Croll 1983; Boudko et al. Therefore, common origin of both types of cephalic
1999; Croll et al. 2003) while homology ofthe differ- shieldsandthushomology isquestionable. FurtherCSOs
enttypes ofCSOs in differenttaxahas neverbeen inves- have been described in Acteonoidea and Cephalaspidea
tigatedindetail. Wewanttoclarifytheirhomology in sep- such as lip organ and Hancock's organ (Rudman 1971a;
arate evolutionary lineages so as to elucidate key ques- RuDMAN 1971b; Rudman 1972a, b; Rudman 1972c;
tions regarding character evolution and phyiogeny. Edlinger 1980).
Acteon tornatilis belongs to the subgroup Acteonoidea, Since the presence of these organs in members of the
formerly ascribed to the basal Cephalaspidea (Odhner genus Acteon has been disputed by different authors
1939, Burn & Thompson 1998). However, recent inves- (Edlinger 1980; Schmekel 1985), absolute clarification
tigations have either excluded the Acteonoidea from the iscertainlynecessary .The intentionofthisstudyistode-
Opisthobranchia (Mikkelsen 1996) or proposed a sister scribe the structure emphasizing the innervation of the
grouprelationshipofActeonoideaandthehighlyderived CSOs in the acteonid A. tornatilis. Our descriptions fo-
Nudipleura (Vonnemann et al. 2005) thus, rendering the cus on the cellular innervation patterns reconstructed for
.
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
312 Sid Staubach & Annette Klussmann-Kolb: Cephalic sensory organ inAceton
thecerebralnerves usingaxonaltracing. Inanearlierstudy ed on an objective slide dorsal side up in Entellan (VWR
(Staubach et al. inpress) these cellular innervation pat- International)andcoveredwithacoverslip.Tenreplicates
terns were shown to be more adequate in homologising were prepared for each cerebral nerve ofA. tornatilis.
cerebral nerves than ganglionic origins ofnerves (Huber Sampleswithonlyapartial stainingofthenervewerenot
1993). By comparising the innervation patterns inA. tor- usedbecauseofpossible incomplete innervationpatterns.
natilis to previously published data on H. hydatis Ourcriterion forawell-stainedpreparationwasadarkblue
(Staubach etal. //;press), wewanttosurveywhetherthe stainednerveindicatingintactaxons(Fredman 1987).The
preliminaiycharacteristic cell clusters in thecentral nerv- Ni-Lys tracings were analysed by light microscopy (Le-
ous system (CNS) ofboth taxa can be identified by ho- icaTCS4D). Cameralucidadrawingsweredigitalisedfol-
mologising cerebral nerves across taxa. Basedon the ho- lowingthemethodofColeman (2003)adaptedforCorel-
mologisation ofthenerves innervatingtheCSOswewant DRAW 11. The somata in the innervation scemes occurs
toclarify ifA. toriiatilis has homologous structuresto the in all replicates. Somata only occurring in single samples
CSOs ofCephalaspideans. It is ourintent interest that we arenotconsideredpartoftheschematics.Theaxonalpath-
shed light on the phylogenetic position and evolutionary ways are estimated over all replicates. Additionally, we
historyofActeonoideawithintheOpisthobranchiaforfu- tested for asymmetries making axonal tracings (n = 2 to
ture studies. 3) for each cerebral nerve ofthe left cerebral ganglion.
2.3. Scanning electron microscopy studies
MATERIALSAND METHODS
2.
The specimens were relaxed by an injection of7 % Mg-
2.1. Specimens CIt inthe foot. Thereafter, theentireheadregionwasdis-
sected from the rest ofthe animal. The CSOs were fixed
% % M
A. tornatilis (Fig. lA) were collected in the wild at St. in 2,5 glutaraldehyde, 1 parafonnaldehyde in 0,1
Michel en Greve(Brittany, France).Theywerethen stored phosphate buffer (pH 7,2) at room temperature. For the
alive at our lab in Frankfurt. Fourty specimens measur- SEM, the fixed CSOs were dehydrated through a graded
ing a shell length between 15 and 20 mm were traced di- acetoneseries followedbycritical pointdrying(CPD030.
rectly (5 to 15 days after collecting) and five were fixed BAL-TEC). Finally, theywere spatteredwith gold(Sput-
for SEM. ter-Coater, Agar Scientific) and examined with a Hitachi
S4500 SEM.AllphotographsweretakenusingDISS(Dig-
2.2. Tracing studies ital Image Scanning System - Point Electronic) and sub-
sequently adjusted forbrightness and contrastwith Corel
Animals were relaxed with an injection of 7 % magne- PHOTO-PAÍNT
1 1
sium chloride. The central nervous system consisting of
the cerebral, pleural and pedal ganglia was removed and
placed in a small Petri dish containing filtered artificial 3. RESULTS
seawater (ASW; Tropic Marin, Rebie-Bielefeld; GER-
MANY). We then followed the procedures from Croll 3.L Organisation and innervation ofthecephalicsen-
& Baker (1990) for Ni2+-lysine (Ni-Lys) tracing ofax- sory organs
ons. Briefly,thenervesoftherightcerebral ganglionwere
dissectedfree from theconnectivetissue. Thenei"veswere A. tornatilispossessesaprominentbipartitecephalicshield
cut and the distal tip was gently drawn into a glass mi- (cs) inwhicheach hemisphereofthisshieldisdividedin-
cropipette using suction provided by an attached 2.5 ml to an anteriorand aposteriorlobe (Figs. 1Aand B). Eyes
syringe. Subsequently, the saline in the micropipette was areembeddeddeeplywithinthetissueoftheshield.Along
replaced by aNi-Lys solution (1.9g NiCl-óH^O, 3,5 g L- the lateralmarginoftheanteriorlobeofthecephalicshield
Lysine freebasein20ml doubledistilled H^O). Theprepa- agroove ispresent(Fig. IB,2A). Hiddenunderthecsand
ration was then incubated for 12-24 hours at 8" C to al- above the foot, the mouth opening is situated at the me-
low transport ofthe tracer. The micropipette was then re- dian frontal edge (Fig. 2B) suiroundedbythelip(notvis-
moved and the gangliawere washed inASW three times. ible in Figure 2B). We found four nerves innervating the
TheNi-Lyswasprecipitatedbytheaddition offiveto ten CSOs (Fig.IB). The Nl (Nervus oralis) provides inner-
drops ofa saturatedmbeanic acid solution in absolute Di- vation to the lip and small median parts ofthe anterior
methylsulfoxide (DMSO). After 45 minutes the ganglia cephalic shield. ThebifurcatedN2 (Nervus labialis/labio-
%
weretransferredto4 paraformaldehyde(PFA)andfixed tentacularis) innervates the complete anterior cephalic
for4-12 hours at4°C. Thereafterthe gangliawere dehy- shield whereby the groove at the ventral anterior lobe of
drated in an increasing ethanol series (70/80/90/99/99% thecephalic shield isespecially inner\'ated. ThesmallN3
10 minutes each), cleared in methylsalicylateand mount- (Nervus tentacularis/rhinophoralis) innervates a little re-
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
Bonnerzoologische Beiträge 55 (2006) 313
gion ofthe posterior cephalic shield. The Nclc (Nervus For the Nl (n = 10) we identified six cerebral clusters
clypei capitis) innervates the largest hind part ofthe pos- (Cnocl-6) and one pedal cluster (PdnocI) in each sam-
teriorcephalic shield. Wecouldnotdetectaliporgan(Fig. ple (Fig. 3A). The variation between the samples was re-
2B),whichaccordingtoEdlinger(1980)shouldcomprise strictedtoveryfew somata in someclusters. Thecerebral
two small lobes on the cephalic shield above the mouth. clustersweredistributedoverthewholecerebral ganglion.
AHancock's organ described by Edlinger (1980) for.4. ThepedalclusterPdnocI was locatedontheanteriormar-
Tornatilis, here a folded structure separated from the ginofthepedal ganglionabovethepedalcommissure.The
cephalicshieldwas likewisenotfoundinthepresentstudy. innervationpatternoftheN2 (n=10)consistsoffivecere-
bral clusters (Cnlcl-5) and three pedal clusters (Pdnlcl-
3.2. Tracing studies 3) (Fig. 3B). The cerebral clusters show distinct spatial
separationsandareeasyto identify.The thirdtracedcere-
Byconductingtheaxonal tracing studies we were ableto bral nerve(n= 10)wastheN3. Sixcerebral (Cnrcl-6)and
reconstructcellularinnervationpatternsforthefourcere- three pedal clusters (Pdnrcl-3) were identified (Fig. 3C).
bralnervesofA. tonmtilis. Tenreplicatetracingswereper- We foundan additional singlecluster(Cc/z/rc/)anda sin-
formed each for the Nl N2, N3 and Nclc using only the gle soma in the left cerebral ganglion (see arrows in Fig.
nerves ofthe right cerebral ganglion. The characteristic 3C). The contralateral cluster was located at the base of
patternsoflabelledsomataforall nervesareshown in Fig- the N2 whereas the single soma was found at the root of
ure 3A-D, including the approximate pathways of the the cerebral commissure. We observed slight intraspecif-
stainedaxons.The identifiedclusterswerenamedwithab- icvariabilitybetweentheten sampleswhich amountedon-
breviations signifying the ganglion in which they are lo- ly to very few somata in some clusters. In the Nclc, the
cated, the nerve filled and a number indicating the order innei"vation(n= 10)patternconsistedoffivecerebral clus-
oftheirdescription(forexample, Cnlc3: CerebralNervus ters (Cnccl-5) and a single soma at the lateral margin of
labialis cluster 3). Nerve cells are grouped in clusters on the cerebral ganglion above the pedal connective (Fig.
the basis oftheir close positioning in the ganglia and the 3D). Additionally we found four pedal clusters (Pdnccl-
tightfasciculation oftheiraxonsprojecting intothe filled 4) The Nclc had the highest amount ofpedal clusters in
.
nerve. Asymmetries for tracings ofthe left nerves could all investigatednerves.Thenumberofpedalsomata,how-
not be detected. ever, was comparable to the number ofpedal somata for
the N2 innervation pattern (Fig 3B).
Fig. 1. A: Photograph ofActeoii tornatilis with the cephalic shield visible. B: Schematic illustration ofthe CNS, the fourcere-
bralnerves(excludingtheoptical nerve)andthecephalicsensoryorgansofHaminoeahydatisandActeoiitornatilis. Onlytheright
cerebral nerves are shown. Nl Nervus oralis, N2 Nervus labialis,N3 Nervus rhinophoralis, Nclc Nervus clypei capitis, eyeye, gr
groove, al anterior lobe, pi posterior lobe, sh shell, cs cephalic shield, ffoot.
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
314 Sid Staubach &Annette Klussmann-Kolb: Cephalic sensory organ inAceton
Fig. 2. A. Lateral SEM photography ofthe groove at the ventral surface ofthe cephalic shield ofActeon tomatilis. cs cephalic
shield,grgroove. B. Frontal SEM photography ofthemouth regionoíActeontomatilis. cs-cephalicshield,mo-mouth, f-foot.
4. DISCUSSION missing inA. tofiiatilis. Hence, weexpectedconsiderable
differences in the cellularinnervation pattems fortheN3
The present study demonstrates theconstancy ofnervous ofthesespecies. However, thesedifferencesweremargin-
structures in the opisthobranch tnoUusc. Throughout our al and only amounted to the lack ofone single cell soma
investigation ofseveral individualsoftheí\c{QO\\\á,Acteoi) in the cerebral ganglion of.4. toiitatilis. This implies that
tomatilis we found uniform innervation pattems of the basic innervationpattemsoftheN3 areprobablythe same
headregion via fourcerebral nerves, which can be attrib- inboth species.Additional functions oftheN3 processed
uted to characteristic neuronal cell clusters in the CNS. intherhinophoral ganglion canbeproposedfor//, hydatis.
These cellular innervation patterns in A. torinitilis show These functionsareprobablyrelatedtotheHancock'sor-
an extremely high congruence with the cellular innerva- gan, which is innervated by nerves originating in the
tion patterns described for the four cerebral nerves of rhinophoral ganglion (Staubach etal. inpress). Wewere
Haiiiiiioeu hychitis (Staubach et al. in press). unable to locate such an organ in A. tornatilis in contrast
to earlier descriptions (Edlinger 1980).
in the Nl, the number ofcerebral clusters as well as the
position ofthese clusters to each other is the same in A. Upon comparing the innervation pattems presented here
tofiiatilis and H. hydatis. However, we found some dif- for A. tornatilis with those for H. hydatis (Staubach et
ferences in the size and numberofsomata when compar- al. in press) we find constant features ofthese pattems
ingboth species.Additionally,wecould notdetectapleu- across species. This is congnaent with otherfindings that
ral, a parietal and a pedal cluster in A. toniatilis. which neuronal stmctures in the central nervous system ofmol-
weredescribed forH. hydatis. Thismaybeduetothedif- luscsandotherinvertebrates seemtobehighlyconserved
ferences in the peripheral innervation area ofthe Nl. In (Croll 1987;Areas 1991; Hayman-Paul 1991; Kutsch
A. toriiatilis itonly provides forthe lipandvery small parts & Breidbach 1994; Newcomb et al. 2006). Hence, we
ofthe median cephalic shieldwhereas inH. hydatis. it in- postulate the Nl oíA. tornatilis to be homologous to the
nervates the lip and large parts ofthe anterior cephalic N1 (Nervusoralis)describedby Huber(1993) forCepha-
shield. Forthe second nerve, theN2 (Nervus labialis), we laspideans. Additionally, we postulate homologies ofthe
nearly fotmdnodifferencesbetween thepresenceanddis- N2 and the N3 oíA. tornatilisto the N2 (Nei-vus labialis)
tributions ofthe cell clusters for both species. The only andN3 (Nervus rhinophoralis) ofChepalaspideans. This
ostentatious difference was the lack ofa single pedal so- is congruentto the assumption ofHoffmann (1939) that
ma and its contra-lateral analogue in A. toriiatilis. In the thec3 (afterVayssiére 1880)of//, hydatisrepresentsthe
Nclc (Nervus clypei capitis), the difference between the Nei"vus labialis and the c4 represents the Nervus tentac-
two species was also reduced to the presence ofa single ularis, herea synonym fortheNervus rhinophoralis (Hu-
cerebral soma in A. tornatilis. In contrast to the three ber 1993). OurdatacannotsupportEdlinger's(1980)de-
nervesdescribed above,we found a prominentdifference scription ofindependent nerves for the lip organ (Nl af-
in the structure of the N3 when comparing .4cteoii and ter Edlinger 1980) and the anterior Hancock"s organ (N2
Hamiiioea. On the other hand, in H. hydatis the N3 ter- afterEdlinger 1980).TheNclc of^. tornatilisalsoseems
minates in a rhinophoral ganglion. Such a ganglion is tobehomologoustotheNclc ofCephalaspideans(Huber
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
Bonnerzoologische Beiträge 55 (2006) 315
A
B
NI NI
Fig.3. Schematic outline ofcell clusters providing the Nl (A), N2 (B), N3 (C) and Nclc (D) oíActeon tornatilis. The size and
position ofthe somata were digitalized from a camera kicida drawing, the distribution ofthe axons are averaged from all replica-
tes. Nl Nervus oralis, N2 Nervus labialis, N3 Nervus rhinophoralis, Nclc Nervus clypei capitis, N. opt. Nervus opticus, CG cere-
bral ganglia, RhG rhinophoral ganglia, PIG pleural ganglia, PdG pedal ganglia.
I
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
316 Sid SiAUBACii &Annette Klussmann-Kolb: Cephalic sensory organ inAceton
1993). Hoffmann (1939)describedthe same nerveasthe datis: and 3. the posterior Hancock's organ has second-
Nervus proboscidis. We define this nerve however, as arily been reduced inA. tornatilis.
Nervus clypei capitis according to Huber (1993).
The first hypothesis is rather implausible since we found
Considering the homologisation ofthe cerebral nerves in adistinctN3 with conserved cellularinnervationpatterns
light of their neurological origin, neuro-anatomics and in the central nervous system. Ifthe ancestor ofA. tor-
nervous innervation patterns, we postulate hypotheses of natilis neverhad a posterior Hancock's organ, this nerve
homologies respective ofthe organs innervated by these andassociatedneural structures shouldbelacking. More-
nerves. Thus, weconsiderthe lipofA. tomatiUs tobeho- over, a Hancock's organ has been described for other
mologous to the lip of Cephalaspideans (Huber 1993) Acteonoidea(Rudman 1971a,b; Rudman 1972a,b; Rud-
since both organs are innervated by the Nl. The same MAN 1972c). If we consider the second explanation for
holdstrueforthesmall medianpartsofthecephalic shield lack ofa posterior Hancock's organ in A. tornatilis. we
in Acieon and the anterior cephalic shield ofHaiiiinoea. implythattheposteriorcephalic shield inthisspecies, in-
Wecould not finda lip organ inA. tonmtilis asdescribed nervated by the N3, presents a sensory organ as the Han-
byEdlinger(1980),butwedetectedagrooveattheven- cock's organ in Cephalaspidea. However, immunohisto-
tral side ofthe anteriorcephalic shield. This groove is in- chemical and ultrastructural investigations ofthe respec-
nervated by the N2 as isthe lip organ ofCephalaspideans tiveepitheliainA. tornatilisdonotindicateasensoryfunc-
(Huber 1993). Therefore, we postulate this groove to be tion at all (S. Faller, Frankfurt, pers. comm. 2007;
homologous to the lip organ. This hypothesis is also sup- Göbbeler & Klussmann-Kolb inpres.s). We reject this
ported by data on immunorcactivity against several neu- hypothesis ofhomology ofthe posterior cephalic shield
rotransmitters. In the groove ofA. tornatilis as well as in in A. tornatilis and posterior Hancock's organ in H. hy-
the lip organ ofH. hydatis, characteristic sub-epidermal datissincewe foundnoevidence forafunctionofthepos-
sensoi7 neuronscontainingcatecholaminescould be found teriorcephalic shieldasanolfactorysensoryorgan. More-
in high density indicating that both organs are involved over,theposteriorcephalic shieldismostly innervatedby
in contact chemoreception (S. Faller, Frankfurt, pers. the Nclc and not by the N3. The third hypothesis regard-
comm. 2007). ing the reduction ofa Hancock's organ seems to be the
most plausible when the habitat and the food sources of
The N2 oí'Haiiiiiioea is divided into two branches which A. tornatilis in comparison to H. hydatis are considered.
are described as two single nerves by Edlinger (1980). TheposteriorHancock'sorgan isbelievedtobeanolfac-
The first or inner branch provides the lip organ as de- tory sensory organ (Audesirk 1979; Emery 1992). H. hy-
scribed earlier. The second, outer branch is related to the datis feedson green algae which occurinpatches inopen
anteriorHancock'sorgan (Edlinger 1980; Huber 1993). water whereas A. tornatilis is a predator ofsoft inverte-
hi Acteon we also found two branches ofthe N2: the in- brates living up to ten centimeters in solid sand(Fretter
ner one providing the largest part ofthe groove whereas 1939; YoNOW 1989; own investigations). In such an en-
the outer branch is restricted to a small region between vironment, an olfactoiy sensory organ is not plausible
the anterior and posterior lobe of the cephalic shield. sinceolfactionordistancechemoreception isgenerallyas-
Therefore, this latterregion maybehomologoustothean- sociated with watercuiTcnts, which are not substantial in
terior Hancock s organ of//, hydatis and not to the pos- a sandy substrate habitat. Here, a contact chemoreceptor.
terior Hancock'sorgan asdescribedby Edlinger(1980). which is located near the edge ofthe cephalic shield is
moreplausible. ThiswewitnessedinActeon tornatilisvia
The N3 of^. tuniatilis provides a large part ofthe pos- its display ofa potentially chemoreceptive groove along
terior cephalic shield but no identiFiable posterior Han- the lateral inargin ofthe anterior cephalic shield.
cock'sorgan.Additional immunohistochemical and ultra-
structural investigations could also not detect a posterior Thisassumptionofsecondaryreduction oftheHancock's
Hancock's organ in A. tornatilis (S. Faller, Frankfurt, organ in theendobenthicA. tornatilis isalso supportedby
pers. comm. 2007; Göbbeler & Klussmann-Kolb //; thefactthataHancock'sorganhasbeendescribedforoth-
press).Theposteriorpai1softhecephalic shields inActeon erepibenthicActeonoidea (e. g. Bnllina. Micromelo. Hy-
and Ihiiniiioeu are probably equally homologous as both datina) (RuDMAN 1971a, b; Rudman 1972a, b; Rudman
where innervated by the Nclc. 1972a.b,c).
The lack ofa posterior Hancock's organ in A. tornatilis Despite all discussion, homology ofthe described Han-
might be due to three different reasons: 1. the ancestorof cock's organs to those in Cephalaspidea cannotundoubt-
A. tornatilisneverhadaposteriorHancock'sorgan; 2. the edly be proposed at this stage, particularly since data on
posteriorcephalic shieldofA. tornatilismaybeahomol- innervationpatternsintheseacteonidsare lackingtodate.
ogousstructuretotheposteriorHancock'sorgan of//, hy- Moreover, currentphylogenetichypotheses(Grandeetal.
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
Bonnerzoologische Beiträge 55 (2006) 317
Croll, R. P,Boudko,D.Y,Pires,A.&Hadfifld,M.G. 2003.
2004; VoNNEMANN et al. 2005) regarding Opistho- Transmittercontent ofcells and fibers in the cephalic senso-
branchia propose an independent origin ofActeonoidea 17organsofthegastropodmolluscPlicsiillasily)gac.CellTis-
andCephalaspidea. indicatingconvergentdevelopmentof sue Research 314: 437-448.
these sensory organs in both evolutionary lineages. Fur- Davis,W.J.&Matera,E. M. 1982.Chemoreceptioningastro-
therstudieswill haveusutilizingcellularinnei"vation pat- podmolluscs: electronmicroscopyofputativereceptorcells.
ternsforCSOs inordertocompare severaltaxawhileho- Journal ofNeurobiology 13(1): 79-84.
Edlinger, K. 1980. Zur Phylogenie derchemischen Sinnesor-
mologising the different types of CSOs in Opistho-
gane einigerCephalaspidea
branchia. This procedure will enable us to glean a better (Mollusca,Opisthobranchia). Zeitschrift türZoologie, System-
understanding ofthe evolution ofthese organs. atik und Evolutionsforschung. 18: 241-256.
Emery, D. G. 1992. Fine structureofolfactory cpithcliaofgas-
tropod molluscs. Microscopy Research and Technique 22:
307-324.
Acknowledgements.Marc Hasenbank,PatrickSchultheissand
Fredman, S. M. 1987. Intracellular staining of neurons with
ChristianeWeydigwereconstructiveinlocatingtheActeontor- nickel-lysine. Journal of Neuroscience Methods 20(3):
natilis population at St. Michel en Greve. Thanks to Katrin 181-194.
Göbbeler and Simone Faller for their personal commitments. Fretter, V. 1939. The structure and function ofthe alimentary
tReorgnesranCrdolClSOwsa.sWalewaayrse gvreartyefhuellptfouAlnignedliascDuisnsaipnoglit,raAcdirnigepnante- canalofsometectibranchmolluscs,withanoteonextraction.
Transactions of the Royal Society of Edinborough 59:
Jochum andAlen Kristoffortheircomments on an earlierver-
599-646.
sion ofthis manuscript. Göbbeler, K. & Klussman-Kolb,A. 2007. Acomparative ul-
This study was supported by the German Science Foundation,
KL 1303/3-1 and by the Verein der Freunde und Förderer der trastructural investigation ofthe cephalic sensory organs in
Opisthobranchia (Mollusca, Gastropoda). Tissue Cell, doi
Johann-Wolfgang-Goethe Universität.
I0.I016/j.tice.2007.07.02.
Alsothankstoanunknownrefereewhoprovidedvaluablecom- Grande,C,Templado,J.,Cervera,J.L.&Zardoya, R. 2004.
ments on the manuscript. Phylogenetic relationships amongOpisthobranchia (Mollus-
ca Gastropoda)basedonmitochondrialcox tmV,andmiL
: 1,
genes. Molecular Phylogenetics and Evolution 33(2):
378-388.
REFERENCES
Hancock,A. 1852. Obsewations on the olfactory apparatus in
Arbas, E. a. 1991. Evolution in nervous systems. Annual Re- the Bullidae. Annual Magazine ofNatural Histoi^y 2: 9.
view inNeuroscience 14: 9-38. Hayman-Paul, D. 1991. Pedigreesofneurobehavioral circuits:
AUDESIRK, T. E. 1979. Oral mechanoreceptors in Tritonia tracingthe evolution ofnovel behaviours by comparing mo-
diomedea. Journal ofComparative Physiology 130: 71-78. tor patterns, muscles and neurons in members ofrelated ta-
Bicker,G., Davis,W. J. & Matera, E. M. 1982. Chemorecep- xa. Brain Behavioural Evolution 38: 226-239.
tion andmechanoreception in the gastropodmollusc Pleiiro- Hoffmann, H. 1939. Mollusca. I Opisthobranchia. Pp. 1-1248
brancheacaliforiiica. JournalofComparativePhysiology 149: in: Bronns,H.G.(ed.)KlassenundOrdnungendesTierreichs
235-250. III (1). Akademische-VerlagsgesellschafT Leipzig.
Bock,W.J. 1989.Thehomologyconcept: itsphilosophical foun- Huber,G. 1993. On thecerebalnervoussystemofmarine Het-
dationandpracticalmethodology.ZoologischeBeiträge(Neue erobranchia (Gastropoda). Journal ofMolluscan Studies 59:
Folge)32: 327-353. 381-420.
BOUDKO,D.Y., SWITZER-DUNLAP,M. &Hadfield, M.G. 1999. KuTSCH, W. & Breidbach, O. 1994. Homologous structures in
Cellularandsubcellularstructureofanteriorsensoi"ypathways thenervoussystemsofarthropoda.Advancesin InsectPhysi-
in Phestilla sihogae (Gastropda, Nudibranchia). Journal of ology 24: 2-113.
ComparativeNeurology 403: 39-52. Newcomb,J.M., Fickbohm, D.J. & Katz, P.S. 2006. Compara-
Burn, R. & Thompson, T. 1998. Order Cephalaspidea. Pp tivemappingofserotonin-immunoreaetiveneuronsinthecen-
943-959in: Beesley, P L., Ross,G.J. B.&Wells,A.(eds.) tral nervous system ofnudibranch molluscs. The Journal of
Mollusca: The Southern Synthesis. Fauna ofAustralia. Vol. ComparativeNeurology 499: 485-505.
5, PartB. CSIRO Publishing, Melbourne. MiKKELSEN, P.M. 1996. The evoludonary relationships of
Chase, R. 2000. Behavior and its neural control in gastropod Cephalaspideas.l. (Gastropoda:Opisthobranchia): aphyloge-
molluscs. Oxford University Press, NewYork. netic analysis. Malacologia 37: 375^42.
Coleman, C. O. 2003. "Digital inking": how to make perfect Odhner, N.H. 1939. Opisthobranchiate Mollusca from thewe-
line drawings on computers. stern and northern coasts ofNorway. Kongelige Norske Vi-
Organisms,DiversityandEvolution3: Electronical Supplement denskabemes Selskabs SkrifterNRNo. 1: 1-93.
14: 1-14. Rudman, W.B. 1971a. The genus Bullina (Opisthobranchia) in
Croll, R. P. 1983. Gastropod chemoreception. Biological Re- New Zealand. Journal ofthe Malacological Society ofAus-
views, Supplement 3, 58: 293-319. tralia 2(2): 195-203.
Croll, R. P. 1987. Identifiedneurons andcellularhomologies. Rudman,W.B. 1971b.ThefamilyActconidae(Opisthobranchia,
Pp. 41-59 in: All M.A. (ed.) Nervous Systems in Inverte- Gastropoda)inNewZealand.JournaloftheMalacologicalSo-
brates. ciety ofAustralia2(2): 205-214.
Croll,R.P.&Baker,M. 1990.Axonalregenerationandsprout- Rudman,W.B. 1972a.Theanatomyoftheopisthobranchgenus
ing following injury tothe cerebral-buccal connective in the Hydatinaandthefunctioningofthemantlecavityandalimen-
snail Achatinafúlica. The Journal ofComparative Neurolo- tary canal. Zoological Journal of the Linnean Society 51:
gy300: 273-286. 121-139.
© Biodiversity Heritage Library, http://www.biodiversitylibrary.org/; www.zoologicalbulletin.de; www.biologiezentrum.at
318 Sid Staubach &Annette Klussmann-Kolb: Cephalic sensory organ inAceton
RUDMAN, W.B. 1972b. Studies on the primitive opisthobranch Vonnemann, v., Schrödl, M.. Klussmann-Kolb, A. &
genera BiiHina Ferussac and Micmiiielo Pilsbry. Zoological Wägele, H. 2005. Reconstruction ofthe phylogeny ofthe
Journal ofthe Linnean Society 51: 105-119. Opisthobranchia(Mollusca,Gastropoda)bymeansof18Sand
RuDMAN,W.B. 1972c.AstudyoftheanatomyofPupaandMax- 28S rDNA sequences. Journal of Molluscan Studies 71:
acteon(Acteonidae,Opisthobranchia),withanaccountofthe 113-125.
breeding cycle ofPupa kirki. Journal ofNatural Histoi'y 6: YoNOW,N. 1989. FeedingobservationsonActeontomatilis(Lin-
603-619. naeus)(Opisthobranchia,Acteonoidae).JournalofMolluscan
ScHMEKEL, L. 1985. Aspects ofevolution within the opistho- Studies 55(1): 97-102.
branchs. Pp. 221-267 in: Truenan, E.R. & Clarke, M.R.
(eds.)TheMollusca.Vol. 10Evolution.Academic Press, Lon-
don.
Staubach, S.E., Schützner, P., Croll, R.P. & Klussmann-
Kolb,A.Innervationpatternsofthecerebral nei^vesinHami-
uoeahyclalis(Linnaeus 1758)(Gastropoda,Opisthobranchia) Author'sadresses: SidStaubach (correspondingauthor)
-Atest forintraspecificvariability.Inpress, Zoomorphology andAnnetteKlussmann-Kolb, InstituteforEcology, Evo-
(2()()7). lution and Diversity - Phylogeny and Systeinatics, J. W.
Vayssiere,a. 1980. RecherchesanatomiquessurlesMoUusques Goethe-University, Siesmayerstraße 70, 60054,Frankfurt
delafamilledesBullidésAnnalesdesSciencesNaturelleZoo- am Main, Germany. E-mail: Staubach(5¿bio.uni-
logie 6: 9. frankfurt.de; Klussmann-Kolbíábio.tmi-frankfurt.de.
ZOBODAT - www.zobodat.at
Zoologisch-Botanische Datenbank/Zoological-Botanical Database
Digitale Literatur/Digital Literature
Zeitschrift/Journal: Bonn zoological Bulletin - früher Bonner Zoologische Beiträge.
Jahr/Year: 2007
Band/Volume: 55
Autor(en)/Author(s): Staubach Sid, Klussmann-Kolb Annette
Artikel/Article: The cephalic sensory organs of Acteon tovnatilis (Linnaeus, 1758)
(Gastropoda Opisthobranchia) - cellular innervation patterns as a tool for homologisation
311-318