The identity of Doris (s.l.) species MacFraland, 1966 (Mollusca, Nudibranchia, Discorididae): a persistent mystery from California solved

11 Pages·2001·4.4 MB·English

by  David W Behrens

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Volume52, No. 15,pp. 183-193, 7figs., 1 table. August21,2001
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The Identity ofDoris (s.l.) Species MacFarland, 1966
(Mollusca, Nudibranchia, Discodorididae): A Persistent Mystery
from California Solved
by
DavidW. Behrens and Angel Valdes'
DepartmentojInvertebrateZoologyandGeology, CaliforniaAcademyofSciences,
Golden GatePark, San Francisco, California 94118
TheCaliforniandoridnudibranchspecies,previouslyreferredtobyseveralauthorsasDo-
ris{s.l.) species, based upon its original reference in MacFarland (1966), is a synonym of
Diaululasandiegensis(Cooper, 1863).ThesinglespecimenexaminedbyMacFarland,and
otheranimalscollectedfromsouthernCalifornia,matchingtheexternalcolorationofDo-
ris (s.i.) species, have been examined and their internal anatomy is identical to that of
Diaulula sandiegensis. Some variation has been observed in the shape ofthe outermost
radularteeth ofthisspecies. Theobscureandpoorlydescribed species Dorisodonoghuei
Steinberg, 1963 (=DorisechinataCDonoghue, 1922) isprobablya synonym oiDiaulula
sandiegensisaswell.
Themonographicwork"StudiesoftheOpisthobratichiateMoilusksofthePacificCoastofNorth
Ameiica"byF. M.MacFarlandwaspublishedposthumouslyin 1966.Thisworkiscomposedofase-
riesofunpublishednotesthatMacFarlandhadbeenpreparingatthetimeofhisdeath. Oneofseveral
ofthe undescribed species included was referred to as Doris {s.l.) species. MacFarland frequently
usedLatin abbreviationsinhisnotesandmanuscripts, andinthisinstance"s.l."referredtotheLatin,
sensulato, inthebroadersense. MacFarland (1966)didnotprovideaspecificname forthisanimal,
whichhas similarexternal morphologyandcoloration to Diaululasandiegensis(Cooper, 1863). He
examinedonlyonespecimenofDoris(.?./.)species(Fig. I).collectedfromArchRockPool,Newport
Bay,California,butheneverstudieditanatomically.ThenameDoris{s.l.)hasbeencarriedinthelit-
erature in numerouspublications(Sphon andLance 1968; Behrens 1980; McDonaldandNybakken
1981; McDonald 1983), and it is normally used for dorid nudibranchs similar to Diaulula
sandiegensisbuthavingpaledorsal spots.Otherauthorsreferredtothisanimal asDorissp.(McDon-
ald and Nybakken 1981; McDonald 1983) orDiaulula sp. 1 (Behrens 1991, 1992). All these refer-
ences arebasedonMacFarland'sdescriptionsandnewlycollectedspecimensaswell. However, the
question ofwhetherthis animal constitutes a different species from Diaulula sandiegensis remains
unresolved.
PriortothepublicationofMacFarland's(1966)memoir, aspecieswith similarexternal charac-
teristics was described as Doris echinata by O'Donoghue (1922). Later, Iredale and O'Donoghue
(1923)reassignedthisspeciestoDoridigitatad'Orbigny, 1839andchangedthename(withoutexpla-
nation)toDoridigitatamaculata. Steinberg(1963)notedthatbothO'Donoghue'snameswerepreoc-
cupiedbyDorisechinataLoven 1846andDorismaculataGarstang 1896,respectively,andproposed
anewname, Doris odonoghueiforthis species. Additionally, Steinberg (1963) questionedwhether
1Currentaddress:DepartmentofMalacology,MuseumofNaturalHistoryofLosAngelesCounty,900ExpositionBoule-
vard,LosAngeles,California90007.
183
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theplacementofthisspeciesinthegenusDorisisaccurateandsuggestedthatfurtherstudywasneces-
sary.
In this paperwe attempt to determine the identity ofDoris (s.l.) species based on the study of
MacFarland'soriginalmaterialandadditionalspecimensdepositedattheDepartmentofInvertebrate
ZoologyandGeologyoftheCaliforniaAcademyofSciences(CASIZ).Inaddition,thestatusofDoris
odonoghueiis discussed.
Materialand Methods
For this paper several species matching the external coloration described for Diaulula
sandiegensis and Doris (s.l.) species were examined. Table 1 summarizes the material sources and
collectionlocalities. Specimensweredissectedbydorsalincision.Theirinternal featureswereexam-
inedanddrawn underadissectingmicroscopeusingacamera lucida. Partsofthedorsum havebeen
critical pointdried forscanning electron microscopy(SEM) ofthecaryophyllidia. Special attention
waspaidtothe morphology ofthe reproductive system anddigestive system, including the radulae,
which have been prepared forexamination on SEM. Features ofliving animals wererecorded from
photographs ornotes ofcollectors.
Descriptions
—
External Morphology. The living animals measured up to 53 mm in length. The back-
groundcolorvaries from translucentwhitetotan (Figs. I; 2A, B). Thenotal surface is coveredwith
brown specks and bears numerous irregular oval brown spots. In most specimens the centerofthe
brown spots is lighterin color, surroundedbyadarkring. Awhiteband, composed ofminute white
specksoccursalongthenotalmargin.Thebodyisoval,highestalongitsmidline,slopinggraduallyto
themargins.Thenotalsurfaceisdenselycoveredwithvarioussizedcaryophyllidia(Fig.3D).Thegill
iscompletelyretractileintoabranchial pit. Thesixtripinnatebranchial leavesareupstandinganddo
notspreadtotheedgesofthenotum.Thebranchial leavesarewhitetocreamincolorandaredensely
sprinkled with brown specks. The anal papilla is located at the center ofthe branchial plume. The
rhinophoresareperfoliatewith 12-18 lamellaeandareretractileintoshortuprightsheaths.Thecolor
oftherhinophoresissimilartothatofthebranchialplume.Ventrally,thefootisgroovedandnotched,
wide,taperingposteriorlyintoaroundend.Theposteriorendofthefootextendsonlyslightlybeyond
theposteriormargin ofthe notum. The oral tentacles are slenderandpointed distally (Fig. 5C).
—
Anatomy. Thelabial cuticleissmooth. Theradularformulais 14 x 16.0.16 ina 10-mm-long
specimen (CASIZ 060977), 15x23.0.23 in an 18-mm-long specimen (CASIZ 025880) and
22 X 27.0.27 in a 46-mm-long specimen (CASIZ 068277). There is no trace ofrachidian teeth. The
lateral teeth (Figs. 3A, B; 4A, B) are simple hamate increasing in size from thecenteroftheradular
ribbontotheninthandtenthtooth,thendecreasingtothemargin.Theoutermosttwolateral teethare
veryelongate andaresmooth (Fig. 3C), orhaveonetothree small denticles (Fig. 4C, D),depending
on the specimen.
Thereproductive system is triaulic (Fig. 5A, B). The ampulla is tubularandconvoluted. Itnar-
rowsintoashortthintubeandconnectstotheoviductandprostaticportionofthevasdeferens. Imme-
diately afterbranching, the oviduct enters the massive female gland mass. The vas deferens is long
and slightlythinnerthan the ampulla, until it expands into two wide and large, contiguous prostatic
portions. A long, thinductemerges from theprostaticportion andbecomeshighly convoluted in the
ejaculatory segment, priorto enteringacommon genital atrium with thevagina. The vaginal duct is
thick, normally straight and connects to the large, round bursa copulatrix. A separate duct from the
bursa copulatrix connects to the smaller, spherical seminal receptacle. A short, thin uterine tube
•
BEHRENSANDVALDES: IDENTITYOFDORIS{S.L.) 185
B
^
:*\ m
* »
Figure 1.SpecimenidentifiedbyMacFarland(1966)asDoris(s.l.)species(CASIZ025880).A. Photographoftheliving
animaltakenbyG.E.MacGinitie. B,C. DrawingspublishedbyMacFarland(1966,pi.25,figs. 1,2).
emergesneartheconnectionofthisductandthenconnectstheseminalreceptacletothefemalegland
nearthe genital atrium.
Discussion
After the anatomical study of the material of Doris {s.l.) species examined by MacFarland
(CASIZ025880),ofadditionalspecimenswithasimilarexternalcolorationfromsouthernCalifornia
(CASIZ 060976), and of specimens matching the original description of Diaiiliila sandiegensis
(CASIZ 068277; CASIZ 071641), we wereunable to find anyconsistentdifferences. It is clearthat
Doris{s.l.) speciesconstitutes acolorvariation ofDiaululasandiegensis. Theexternal coloration of
thisspeciesisextremelyvariable. Itranges fromwhiteorcreamtoyellow,withbrownringsorsolid
spots, sometimes surroundedbyan opaquewhitering(Fig. 2). Specimens fromCanada,Alaska,and
the Russian fareastgenerallyhave the dorsum covered with numerousverydark spots (Fig. 2E, F),
whereas in southern Californiaand Mexicothe spots are lighterand less common. Specimens from
central andnorthern California, Oregon, and Washington match the original description by Cooper
(1863).
The reproductive system ofall the specimens examined has two large and distinctprostatic re-
gions inthevasdeferens. There is a long,thick, straightvaginal duct. The oviduct,vasdeferens and
uterineductall enterthefemaleglandmassinthesameproximity,nearthegenital atrium(Figs. 5A,
B; 6A, B).
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BEHRENSAND VALDES: IDENTITY OFDORIS
(S.L.) 187
Figure2. LivinganimalsofDiaululasandiegensis(Cooper, 1863). A. SpecimenfromSanDiego,California, originally
identifiedasDoris(s.l.)species;B.SpecimenfromOrangeCounty,California,originallyidentifiedasDoris(s.l.)species;C.
SpecimenfromSanLuisObispo,California;D.SpecimenfromtheChannelIslands,California;E.SpecimenfromVancouver
Island, British Columbia, Canada; F. Specimen from Vancouver Island, British Columbia, Canada. Photograph lA by J.
Hamann,othersbyD. Behrens.
Camera lucida drawings based on light microscopy of the radula of Doris {s.l.) species
(MacFarland 1966; McDonald 1983, 1997; Behrens 1992) suggests that the species has smooth,
hamate,outerlateral teeth. Scanningelectron microscopyofthespecimen seenbyMacFarland(Fig.
4C, D) showsthepresenceofdenticleson theoutertwo lateral teeth. Thischaracteris notpresent in
other examined specimens with the same color pattern collected from southern California (Fig.
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Figure3.Diaululasandiegensis(Cooper,1863),scanningelectronmicrographsofaspecimenoriginallyidentifiedasDoris
(5./,)species(CASIZ060977).A.Innerlateralteeth;B.Lateralteethfromcentralportionofhalf-row;C.Outerlateralteeth;
D.Caryophyllidia.
BEHRENSAND VALDES: IDENTITY OFDORIS
(S.L.)
Figure4.Diaululasandiegensis(Cooper, 1863),scanningelectronmicrographsofaspecimenidentifiedbyMacFarland
(1966)asDoris{s.I.)species(CASIZ025880).A.Innerlateralteeth;B.Lateralteethfromcentralportionofhalf-row;C.Outer
lateralteeth;D. Detailofthedenticlesontheouterlateralteeth.
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Figure5.Diaululasandiegensis(Cooper,1863),anatomyofaspecimenoriginallyidentifiedasDoris(s.l.)species(CASIZ
060977). A. Reproductivesystem,scalebar= 1 mm; B. Detail ofseveralorgans,scalebar= 1 mm; C. Ventral viewofthe
moutharea,scalebar= 1 mm.Abbreviations:am,ampulla;be,bursacopulatrix;dd,deferentduct;fg,femaleglandmass;ot,
oraltentacle;prl,proximalprostaticregion;pr2,distalprostaticregion;sr,seminalreceptacle;v,vagina.
3A-C), SOitisclearlydueto intraspecificvariation. OtherspecimensofDiaululasandiegensis have
smooth, sharply-pointed,hamate-shapedteethacrosstheentirerow(Fig. 7A-C),identicaltothoseof
Doris (s.l.) species.
Scanning electron microscopy of Diaulula sandiegensis clearly indicates the presence of
caryophyllidia(Fig. 7D),whichareidentical insizeanddensitytothosepresentinDoris(s.l.)species
(Fig. 3D).
O'Donoghue's(1922)descriptionofDorisechinatawasbrief,stating simplythatthedorsumis
coveredwith spiculatepapillaeandthecolorisopaquewhitewithfromadozento fortysmall brown
spots scattered irregularlyoverthesurface. Theradulawasdescribedas simply hamate, 16-18 rows
of 13-15 lateral teeth per half-row. A description ofthe reproductive system is lacking, except for
mentionthatthepenisisunarmed.O'Donoghue(1922)statedthatthoughhefeltthattheclassification
ofthe familywas unsatisfactory, Doris echinata falls within its definition.
In proposing the name Doris odonoghuei to rectify the preoccupancy issue discussed earlier,
Steinberg(1963) examinedtwo specimens from thecollectionofthe FridayHarborMarine Labora-
tories. Questioningthe assignmentofthe species to Doris, she dissected the smallerofthe two, but
cametonosatisfactoryconclusion. Recentreviewofherpersonalnotes(J. Steinberg,pers.commun.,
Jan. 2001) revealedno furtherevidence to assist in itsplacement.
BEHRENSAND VALDES: IDENTITY OFDORIS(S.L.) 191
Figure6.Diaululasandiegensis(Cooper,1863),anatomy(CASIZ068277).A.Reproductivesystem,scalebar= 1 mm;B.
Detailofseveralorgans,scalebar= 1 mm;C.Ventralviewofthemoutharea,scalebar= 1 mm.Abbreviations:am,ampulla;
be,bursacopulatrix;dd,deferentduct;fg,femaleglandmass;ot,oraltentacle;prl,proximalprostaticregion;pr2,disstalpros-
taticregion;sr,seminalreceptacle;v,vagina.
Sincethattimenopublishedaccountsorcasualobservationshavebeenmadeofthisspecies.San-
draMillen(pers.commun.,April 1982)indicatedthatshehadnevercollectedspecimensintheVan-
couver area, British Columbia, that she could clearly identify as Doris odonoghuei. According to
Millen it is impossible to distinguish Doris odonoghuei from small Diaululasandiegensis.
WhereasthisspecieshasnotbeendefinitelyconfirmedsinceO'Donoghue's(1922)original de-
scriptionandnotypematerialisavailableforexamination,andwhereasthisdescriptioncannotbedif-
ferentiated from Diaulula sandiegensis, we propose that this species be regarded as a synonym of
Diaululasandiegensis.
Acknowledgments
WethankJeffGoddardforcollectionofmaterial,JeffHamannforuseofhisphotographandJoan
Steinberg and Sandra Millen for sharing their field and laboratorynotes. Joan Steinberg made con-
structivecommentsonthemanuscript.Thispaperhasbeen supportedbytheNational ScienceFoun-
dation,throughthePEETgrant(DEB-9978155,"Phylogeneticsystematicsofdoridnudibranchs")to
Terrence M. Gosliner.
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Figure7.Diaululasandiegensis(Cooper, 1863),scanningelectronmicrographs(CASIZ068277).A.Innerlateralteeth;B.
Lateralteethfromcentralportionofhalf-row;C.Outerlateralteeth; D. Caryophyllidia.