Tropical western Atlantic species of Diaulula Bergh, 1878 (Mollusca, Nudibranchia), with the description of a new species

2004·6.4 MB·English

by  Angel Valdes

Tropical Western Atlantic Species oe Diaulula
Bergh, 1878 (Mollusca, Nudibranchia),
New
WITH THE Description oe a Species
Angel Valdes^
ABSTRACT. The genus Diaulula is represented in the tropical western Atlantic by two species: Diaulula
greeleyi, a trans-Panamian species also reported from the Pacific coasts of Mexico and Costa Rica, and
Diaulula farmersi, a new species from the Florida Keys. Differences in color and anatomy separate these
two species as D. farmersi has a yellowish background color, a white gill, and the bursa copulatrix and
prostate are proportionally smaller. Examination of specimens ofdifferent sizes ofD, greeleyi, as well as
a review of the literature from other geographic regions, reveals that this species shows little anatomical
variability, supporting the separation of D. farmersi. Two further sympatric species that are superficially
similar to D. greeleyi, Discodoris mortenseni and Discodoris phoca, differ from members ofDiaulula in
having jaws and in other anatomical features.
INTRODUCTION bearing dorids, which, according to these authors,
The genus Diaulula was originally introduced by are a monophyletic group. Valdes and Gosliner
(2001) restricted the use of the name Diaulula to
Bergh (1878) based on Doris sandiegensis Cooper,
1863, from California. Themaincharacteristicsde- species with elongate caryophyllidia, a large pros-
tate with two differentiated portions, penis andva-
fined by Bergh (1878) for this genus were the pres-
gina unarmed, labial cuticle smooth, and radular
ence of a villous, silky dorsum, notched and
teeth hamate and smooth. Additionally, anatomical
grooved anterior border of the foot, tripinnate
examination of specimens of Doris punctuolata
branchial leaves, absence of jaws, presence of a
large prostate, and unarmed penis. d’Orbigny, 1837 (the type species of Anisodoris
Subsequently, Bergh (1905, 1907) introduced Bergh, 1898), revealed that it has the same features
as members ofDiaulula, so these two genus names
four additional species ofDiaulula: Diaulula rubra
were regarded as synonyms. This newclassification
Bergh, 1905 (fromthe Philippines),Diaululagigan-
implies that a number of species ofcaryophyllidia-
tea Bergh, 1905 (from Indonesia), Diaulula capen-
bearing dorids that have been described in various
sis Bergh, 1907, andDiaulula morosa Bergh, 1907,
genera probably belong to the genus Diaulula,
wobfhoittchhhef,seraoscmpceoScriodeuistnhigsAtufonrciVecaralt.daeiTsnh,e(e2x0gc0ee2np)et,rificsoriadDes.nytgniitogynaynotfmeaaol,fl wanaghlnilocyshitshisooupfgrhDotib.aaubFllouyrlaai,nmsCtuaacnmchaec,lhaofro-gleGlraorcwcliiandagetathnhedannVeaowrlidgdeiis--
Sebadoris nubilosa (Pease, 1871). Eliot (1907) and
Marcus (1959) transferredthe SouthAmericanspe- (2003) transferred the tropical Atlantic species Pel-
todorisgreeleyiMacFarland, 1909toDiaulula, and
cies Doris vestita Abraham, 1877, and Doris his-
at the same time synonymized the tropical eastern
pida d’Orbigny, 1837, respectively, toDiaulula. Be-
Pacific species Peltodoris nayarita Ortea and Llera,
cause of the uncertain placement of the tropical
Indo-Pacific and South African species, the genus 1981 with it. They also transferred the Panamic
Diaulula was thought to be restricted to cold wa- species Discodoris aurila Ev. Marcus, 1976 to
Diaulula. Additionally, Valdes and Muniain (2002)
ters in North and South America.
Thompson (1975) andMcDonald (1983) regard- regarded Diaulula vestita as a probable synonym
of Diaulula punctuolata.
ed Diaulula as a synonym of Discodoris, based on
the similar size, shape, mode of life, radula, and Recentfieldwork inthe Florida Keysrevealedthe
presence ofanadditionalspecies ofthegenusDiau-
reproductive organs ofbothgenera. Behrens (1991)
did not agree with that synonymy and maintained lula in the Caribbean. The presentpaperdealswith
this species and provides up-to-date descriptions
the usage ofDiaulula as a valid genus for Diaulula
and classifications for western Atlantic species of
sandiegensis.
Diaulula.
Valdes and Gosliner (2001) reconstructed the
phylogenetic relationships of the caryophyllidia- MATERIAL AND METHODS
1. Malacology, Natural History Museum of Los An- ThematerialexaminedisdepositedattheNaturalHistory
geles County, 900 Exposition Boulevard, Los Angeles, MuseumofLosAngelesCounty(LACM).Specimenswere
California 90007. Email: [email protected]. dissected by making a dorsal incision. The internal fea-
Contributionsin Science,Number 501, pp. 1-7
Natural HistoryMuseum ofLos Angeles County, 2004
2 Contributionsin Science, Number 501 Valdes: TropicalWestern Atlantic Diaulula Species
Figure 1 Living animals: A, Diaululagreeleyi (MacFarland, 1909), Key Largo, Florida, (LACM2003-41.4).B,Diaulula
farmersin. sp., holotype. Key Largo, Florida, (LACM 3016)
tures were examined and drawn using a dissectingmicro- SPECIES DESCRIPTIONS
scope with a camera lucida. A portion ofthe mantlewas
Discodorididae Bergh, 1891
critical point dried for the Scanning Electron Microscope
(SEM). The buccal mass was removed and dissolved in Diaulula Bergh, 1880
10% sodiumhydroxideuntiltheradulawasisolatedfrom
the surroundingtissue. The radula was thenrinsedinwa- Diaulula greeleyi (MacFarland, 1909)
ter, dried, and mounted for examination with the SEM. Figs. lA, 2-3
Eeatures of living animals were recorded from field pho-
tographs and notes. Peltodoris greeleyi MacFarland, 1909:84-88, pi.
Contributionsin Science, Number 501 Valdes: TropicalWestern AtlanticDiaulula Species 3
Figure2 Diaululagreeleyi (MacFarland, 1909), Key Largo, Florida, (LACM2003-41.4), scanningelectronmicrographs
of radula and dorsum: A, Innermost lateral teeth, scale bar = 50 /xm. B, Midlateral teeth, scale bar = 30 /xm. C,
Outermost lateral teeth, scale bar = 50 /xm. D, Caryophyllidia, scale bar = 100 /xm
15, figs. 77-82; Marcus, 1955:137-140, pi. 14, and Valdes, 2003:71-75, text figs. 1C, 4A-D,
figs. 126-132; MarcusandMarcus, 1967:72-74, 5A-D.
text figs. 94-98; Eyster, 1980:588.
Peltodoris nayarita Ortea and Llera, 1981:47-51, TYPE MATERIAL. Holotype. Alagoas, Riacho
mm
text figs. 1-4 (also cited as Anisodoris); Bertsch Doce, Brazil, 28 July 1899, 1 specimen, 9 pre-
et al, 2000:100. served length, leg. A.W. Greeley (California Acad-
Diaulula greeleyi (MacFarland): Camacho-Garda emy of Sciences 21021).
4 Contributionsin Science, Number 501 Valdes: TropicalWesternAtlantic Diaulula Species
copulatrix. Another duct, which connects to the
seminal receptacle and the uterine duct, leads from
the bursa copulatrix. The bursa copulatrixis about
twice as large as the seminal receptacle (Fig. 3A).
GEOGRAPHIC RANGE. This species has been
reported from Brazil (MacFarland, 1909; Marcus,
1955), Florida (Marcus and Marcus, 1967), South
Carolina (Eyster, 1980), the Pacific coast Baja Cal-
ifornia (Bertsch etal, 2000), southernMexico (Or-
tea and Llera, 1981), and Costa Rica (Camacho-
Garcia and Valdes, 2003).
Figure 3 Diaululagreeleyi (MacFarland, 1909), KeyLar- REMARKS. Diaulula greeleyi was originally de-
go, Florida, (LACM 2003-41.4), anatomy: A, Reproduc- scribed from Brazil (MacFarland, 1909) and was
tive system, scale bar = 500 ixm. B, Ventral view of the subsequently reported from several other Atlantic
mouth area, scale bar = 2mm.Abbreviations: am - am- localities. Camacho-Garcia and Valdes (2003) re-
pulla; be = bursa copulatrix; dd = deferent duct; fg = garded the eastern Pacific species Peltodoris nay-
female glands; ot = oral tentacle; pr = prostate; sr = arita Ortea and Llera, 1981 as a synonym, based
seminal receptacle; v ~ vagina on the examination of specimens from the Pacific
coast of Costa Rica. These authors also provided
illustrations of the reproductive system and radula
ofthis species based on Pacific material. Thenewly
MATERIAL EXAMINED. Shore in front of the collected specimens from the Florida Keys are an-
Bayside Resort (mile marker 99.5), Key Largo, atomically identical to the specimens from Costa
Monroe County, Florida, 13 July 2003, 1-2 m Rica, confirming thatthe populations on bothsides
depth, 3 specimens, 5-13 mmpreservedlength,leg. of the Isthmus of Panama belong to the same spe-
A. Valdes (LACM 2003-41.4). cies.
EXTERNALMORPHOLOGY.The bodyisoval Two other Caribbean species are Discodoris
to elongate (Fig. lA), with the posterior end ofthe mortenseniEv. Marcus and Er. Marcus, 1963,orig-
foot covered by the mantle. The dorsum is covered inallydescribedfromCurasaoandTobago(Marcus
with caryophyllidia about 100 {jum long (Fig. 2D). andMarcus, 1963), andDiscodorisphocaEv. Mar-
The body is pale yellow to orange or brown. The cus and Er. Marcus, 1967, originally described
dorsum is coveredwith a numberofbrownpatches from Biscayne Key, Florida (Marcus and Marcus,
distributed regularly all over the surface. The rhin- 1967). The reproductive system ofDiscodorismor-
ophoral sheaths areelevated and inflated. Therhin- tenseni was subsequently 'described by Bertsch
ophores are dark brown with the apex white. The (1975). These two species have a pinkishorbrown-
gill is composed of 12 unipinnate branchial leaves, ish dorsum with darker spots. Differences between
which are yellow to dark brown. Near the edge of these two species and Diaulula greeleyi include the
the mantle there is a row of opaque white mantle presence of jaws with jaw elements and dorsal
glands. white spots in Discodoris mortenseni and Disco-
The anterior border of the foot is grooved and doris phoca. Additionally, the radular teeth ofDis-
notched (Fig. 3B). The oral tentacles are short and codoris phoca are more angular and the outermost
triangular. teethofDiscodorismortensenihavesmalldenticles.
ANATOMY. The labial cuticle is smooth. The According to Marcus and Marcus (1963, 1967),
radular formula is 45 X (50.0.50) in a 13 mm pre- both Discodoris mortenseni and Discodoris phoca
served length specimen (LACM 2003-41.4). Rach- have caryophyllidia, and the latter also has the
idian teeth are absent (Fig. 2A). The lateral teeth prostate divided into two portions. Thus, thesetwo
are hamate, having a single cusp and lacking den- species should be removed from Discodoris Bergh,
ticles (Fig. 2B). The teeth increase in size gradually 1877, whichincludesspecies lackingcaryophyllidia
towardthe medial portionofthehalf-row.Theout- (Valdes, 2002). Valdes and Gosliner (2001) diag-
ermost teeth are also hamate and lacking denticles nosed Diaulula as lacking jaws, but the systematic
(Fig. 2C). positionofspecieswithjawsandcaryophyllidiahas
The reproductive system is triaulic (Fig. 3A).The not been investigated. Therefore the status of Dis-
ampulla is longandconvoluted. Itentersthefemale codoris mortenseni and Discodoris phoca remains
glands near their nidamental opening. The prostate uncertain until comprehensive phylogenies of car-
is large and granular. Itis divided intotwodifferent yophyllidia-bearing dorids at the species level be-
portions that are clearly distinguishable by their come available.
different texture and coloration. The deferent duct Diaulula greeleyi differs from D. sandiegensis,
is long and expands into the muscular ejaculatory the type species of the genus, by having a darker
portion. The deferent duct opens into a common background color, lacking dorsal rings on the dor-
atrium with the vagina. There are no penial hooks. sum, having unipinnate branchial leaves, and hav-
Thevagina is longandnarrow. Atitsproximalend, ing larger, more hooked-shaped and smooth out-
the vagina connects to the large and rounded bursa ermost radular teeth. The anatomy and external
Contributions in Science,Number 501 Valdes: TropicalWesternAtlantic Diaulula Species 5
Figure 4 Diaulula farmersi n. sp., holotype (LACM 3016), scanning electron micrographs of radula and dorsum: A,
Innermost lateral teeth, scale bar = 50 /xm. B, Midlateral teeth, scale bar = 50 /xm. C, Outermost lateral teeth, scale
bar = 50 /xm. D, Caryophyllidia, scale bar = 100 /xm
morphologyofD. sandiegensiswasdescribedinde- brown and opaque white spots. The lateral profile
tail by Behrens and Valdes (2001). ofD. aurila is much lower than that ofD. greeleyi
The three other valid species of Diaulula found and the radular teeth are more elongate and ha-
intheAmericasareD. punctuolata, D. hispida,and mate. Both D. punctuolata and D. hispida are
D. aurila (see “Introduction” section). Diaululaau- South American species that clearly differ from D.
rila is also a tropical species redescribed by Ca- greeleyi in their external coloration. Illustrationsof
macho-Garda andValdes (2003) andcharacterized D. punctuolata and D. hispida by Schrodl (1996)
by having a grayish background color with minute revealtwo lightlycolored species, the formerispale
6 Contributionsin Science, Number 501 Valdes: TropicalWestern AtlanticDiaulula Species
of the half-row. The outermost teeth are also ha-
mate and lacking denticles (Fig. 4C).
The reproductive systemis triaulic (Fig. 5A).The
ampulla is long and curved; it enters the female
glands near their nidamental opening. The prostate
is large andgranular; itis dividedintotwodifferent
portions that are clearly distinguishable by their
different texture and coloration. The deferent duct
is long and expands into the muscular ejaculatory
portion. The deferent duct opens into a common
atrium with the vagina. There are no penial hooks.
Thevagina islongandnarrow. Atitsproximalend,
Figure 5 Diaulula farmersi n. sp., holotype (LACM the vagina connects to the large and oval bursa co-
3016), anatomy: A, Reproductive system, scale bar = 1 pulatrix. Another duct, which connects to the sem-
mm. B, Detail ofsome reproductive organs, scalebarlike inal receptacle and the uterine duct, leads fromthe
in A. C, Ventral view of the mouth area, scale bar = 1 bursa copulatrix. The bursa copulatrix is about
mm. Abbreviations: am = ampulla; be = bursa copula- three times as large as the seminal receptacle (Fig.
trix; dd = deferent duct; fg = female glands; ot = oral 5B).
tentacle; pr = prostate; sr = seminal receptacle; v = va- GEOGRAPHIC RANGE. This species is only
gina known from the type locality in the Florida Keys.
ETYMOLOGY. Dedicated to Farmers Insurance
Group for their generous contribution to the edu-
cation and research programs of the Natural His-
tory Museum of Los Angeles County.
cterreaimsicsohm-pwlheitteelwyitwhhitlieg,htabnrdobwonthspohtasveantdritphiennlaatte- REMARKS. A review of the literature revealed
that there are no other species similar to Diaulula
branchial leaves.
There are no other species of dorid nudibranchs farmersi in the tropical western Atlantic. The most
from the Atlantic or other biogeographic regions similar species in external morphology and color-
assigned with certainty to the genus Diaulula (see ation is an unnamedanimal fromCapeVerde,West
Africa, illustrated by Ortea (1998:pl. lA), which
“Introduction” section).
differs from D. farmersi only inthe yellowishcolor
Diaulula farmersi new species ofthe gill. Ortea (1998) introducedthenameDoris
hayeki based ontwo uniformlyyellowanimalsalso
Figs. IB, 4-5
collected from CapeVerde. Thephotosoftheliving
TYPE MATERIAL. Holotype. Shore in frontofthe animals show that they clearly belong to two dif-
Bayside Resort (mile marker 99.5), Key Largo, ferent species. One ofthem (from Boavista) hasthe
Monroe County, Florida, 13 July 2003, 1-2 m dorsum covered with caryophyllidia (Ortea, 1998:
mm
depth, 9 preserved length, leg. A. Valdes pi. lA), whereas the other (from Sal) has simple,
(LACM 3016). rounded dorsal tubercles (Ortea, 1998:pl. IB). Or-
EXTERNALMORPHOLOGY.The bodyisoval tea (1998) designated as the holotype the specimen
to elongate (Fig. IB), with the posterior end ofthe from Sal, which is identical to the original descrip-
foot covered by the mantle. The dorsum is covered tion of Doris atypica Eliot, 1906. The generic
with caryophyllidia, about 150 fim long (Fig. 4D). placement and anatomy of the specimen from
The body is yellowish gray and has a number of Boavista is unknown.
minute brown dots all over the surface. The rhin- Diaulula farmersi is clearly distinguishable from
ophoral sheaths are elevated and inflated. Therhin- D. greeleyi by the externalcoloration,whichis uni-
ophores are dark brown with the apiceswhite. The formly yellowish gray with minute brown dots and
gill is composed of 9 bipinnate branchial leaves, white branchial leaves in the former and pale yel-
which are uniformly white. Near the edge of the low to orange or brown with brown patches and
mantle there are 2 rows of opaque white mantle yellow to dark brown branchial leaves in the latter.
glands. The outermost row is composed of small Anatomical differences include the size ofthe bursa
glandsdenselypacked,the innermostrowhasafew copulatrix and prostate, which are proportionally
larger and irregular glands. smaller than in D. greeleyi. Examination of Pan-
The anterior border of the foot is grooved and amic specimens of D. greeleyi by Camacho-Garcia
notched (Fig. 5C). The oral tentacles are short and and Valdes (2003) revealed that the external col-
triangular. oration and anatomy oftheir specimens is virtually
ANATOMY. The labial cuticle is smooth. The identical to that of the Atlantic specimens here
radular formula is 46 X (50.0.50) in the holotype studied. Additionally, verylittlevariabilityhasbeen
(LACM 3016). Rachidian teeth are absent (Fig. observed among specimens of different sizes col-
4A). The lateral teeth are hamate, having a single lected fromthe FloridaKeys. ItisclearthatD.gree-
cusp and lacking denticles (Fig. 4B). The teeth in- leyi has a very conservative anatomy and external
crease in size gradually toward the medial portion coloration; thus, differences with D. farmersi are
Contributionsin Science, Number 501 Valdes: TropicalWestern Atlantic Diaulula Species 7
not due to intraspecific variability or state of ma- chia, Doridacea) from Costa Rica. Proceedings of
turity. the CaliforniaAcademy ofSciences 54:65-79.
Differences between Diaulula farmersi and D. Eliot, C. 1907. Nudibranchs from New Zealand and the
sandiegensis include the presence ofdorsal rings on Falkland Islands. Proceedings ofthe Malacological
the dorsum and tripinnate branchial leaves in the Society ofLondon 7:327-361, pi. 28.
Eyster, L.S. 1980. Distribution and reproduction ofshell-
latter. Also, D. punctuolata and D. hispida are lessopisthobranchsfromSouthCarolina.Bulletinof
much lighter species, having tripinnate branchial MarineScience 30:580-599.
leaves. MacFarland,F.M. 1909.TheopisthobranchiateMollusca
of the Branner-Agassiz Expedition to Brazil. Leland
ACKNOWLEDGMENTS StanfordJunior University Publications, University
Series 2:1-104, pis. 1-19.
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supportedbytheNational ScienceFoundationMRIgrant 49. 36:3-133.
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