The genus Thuridilla (Opisthobranchia: Elysiidae) from the tropical Indo-Pacific, with a revision of the phylogeny and systematics of the Elysiidae

54 Pages·1995·20.5 MB·English

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Vol 49, No. 1, pp. 1-54, 40 figs., 3 tables. December 12, 1995
THE GENUS THURIDILLA (OPISTHOBRANCHIA: ELYSIIDAE)
FROM THE TROPICAL INDO-PACIFIC, WITH A REVISION OF
THE PHYLOGENY AND SYSTEMATICS OF THE ELYSIIDAE
By
Terrence M. Gosliner
DepartmentofInvertebrate Zoology, California Academy ofSciences,
Golden Gate Park^, San Francisco, California 94118
> > phicInstitution
JAN 6 Wto
1
Abstract: This paper reviews the systematics and phytogeny of the sacoglossan genus
Thuridillafrom the Indo-Pacific tropics.Theanatomy ofseven previously determined species
is described. Nine newspecies are named and described anatomically.Theseare: 7\ carlsoni
sp. nov., T. kathae sp. nov., T.flavomaculata sp. nov., T. hoffae sp. nov., /. albopustulosa sp.
nov., T. undula sp. nov., 7. neona sp. nov., T. indopacifica sp. nov. and /. multimarginata sp.
nov.
Phylogenetic analysis of the Elysiidae, presented here, demonstrates the monophyly of
Thuridillaand itsrelationshiptoitssistertaxonPlacobranchus.Continued usageofthegenera
Elysiella, Plattyclaya, Tridachia and Tridachiella renders Elysia paraphyletic. For this reason
the four genera are united with Elysiato preserve monophyly. Bosellia is also placed within
the Elysiidae, as it possesses several synapomorphies with other members ofthe clade.
Anatomical data from these species, in addition to all other described members of the
genus, were used to construct a phylogeny ofThuridilla.
ExaminationofbiogeographicalrelationshipsofThuridillaindicatesthatvicariancepatterns
ofIndo-Pacific sisterspecies have been largely masked by subsequent dispersal.
Received February 14, 1995. Accepted June 16, 1995.
Introduction in association with their specific algal food.
Other derived morphological features differen-
The genus Thuridilla Bergh, 1872, has re- tiate Thuridilla from Elysia.
cently been recognized as being distinct from Ofthe thirteen describedspecies now placed
ElysiaRisso, 1818(Jensen, 1992).Theanatomy in Thuridilla, eleven are found in the Indo-Pa-
of several species was described and thirteen cific tropics. Ofthe remaining two species, one
species wereregardedasmembersofthis genus is found in the Caribbean, East Atlantic and
by Jensen. Mediterranean while the other is restricted to
Species of Thuridilla are unlike most other the Mediterranean. Several of the Indo-Pacific
members of the Elysiidae in that they are species are known only from their original de-
brightly colored and are found crawling out in scriptionand theanatomy ofonly afew species
the open rather than being cryptic and found has been described.
[1]
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During the course of surveying the opistho- May 1990, P. Fiene-Severns. CASIZ 099057, one
branch fauna ofseveral Indo-Pacific localities, specimen, radula removed, pinnacle, G. Buoy,
16 species ofThuridilla were collected, includ- KwajelinAtoll,MarshallIslands,6mdepth,5 March
1994, S. Johnson.
ing 9 undescribed species. In addition, a spec-
Specimens with coloration resembling that de-
imen of Thuridilla picta (Verrill, 1901), from scribed forT. ratna: CASIZ 078470, one specimen,
the Bahamas, and two specimens of Thuridilla dissected, Sapi Island, off Kota Kinabalu, Sabah,
hopei (Verany, 1853), from the Strait of Gi- Borneo, Malaysia, 16m depth, 24 July 1991, T. M.
braltar were examined. This paper further Gosliner. CASIZ 072917, one specimen, jetty,
amplifies the morphology ofpreviously named Christensen Research Institute, Madang, PapuaNew
species and describes the new taxa. Guinea, 13 mdepth, 3 October 1986,T. M.Gosliner.
Jensen (1992) described the two portions of CASIZ 078471, Kapas Island, off Marang, s. of
theradularribbon asascendinganddescending. Kuala Terengganu, Malaysia, 4m depth, 28 July
1991,T.M.Gosliner.CASIZ083866, onespecimen,
In the portion that she refers to as descending
Twin Rocks, sw end ofCalumpan Peninsula, w. of
the cutting edge ofthe teeth is actually ascend- Batangas Bay, Luzon Island, Philippines, 10m
ing. Owing to this ambiguity, the two portions depth, 26 February 1992, T.M. Gosliner. CASIZ
are here referred to as dorsal and ventral. The 086663, two specimens, Maragajong, Flores, Indo-
ventral portion corresponds to Jensen's de- nesia, under rock, 1 m depth, 27 April, 1992, P.
scending limb and the dorsal portion to the as- Fiene-Severns.CASIZ070318,onespecimen,Banne
cending limb. The ventral portion contains the de Gorgone, Nosy Be, Madagascar, 15 April 1989,
older teeth and the dorsal portion the more T. M. Gosliner. CASIZ 071294, one specimen, w.
newly formed ones. point ofCoror Island, wreck offishing boat, Philip-
A review of the known morphology of the pines, 10-13 m depth, 5 June 1988, R. Van Syoc.
CASIZ 099058, one specimen, radularemoved, reef
genuspermitsapreliminaryanalysisofthephy- near M. M.D.C, Palau Koror, 10m depth, M.T.
logeny ofthe genus and comparison with other
Ghiselin.
members of the Elysiidae.
—
DISTRIBUTION. Specimens with T. bayeri
Species Descriptions coloration are known from the Maldives
(Yonow, 1994), the Marshall Islands (Marcus,
1. Thuridilla bayeri (Marcus 1965) 1965; Johnson and Boucher, 1983), Guam
(Carlson and Hoff, 1978; Jensen, 1992), ? Fiji
Elysia bayeri Marcus, 1965: 270, figs. 5, 6; Carlson (Brodie and Brodie, 1990), Papua New Guinea
and Hoff, 1978:91, figs. 4, 5b, 6a, b. (presentstudy), Indonesia(presentstudy), Aus-
Thuridilla bayeri (Marcus) Jensen, 1992: 273, figs. tralia (present study). Specimens with color-
14e, 15f, 16g-i, 17c, 18c. ation resemblingT. ratna areknown fromPalau
Elysia ratna Marcus, 1965: 270, figs. 7, 8; Carlson (Marcus, 1965; present study), Guam and Po-
and Hoff, 1978: 107, figs. 5e, 16d, e, 18. nape (Carlson and Hoff, 1978), Marshall Is-
Thuridilla ratna (Marcus) Jensen, 1992: 270, figs. lands (Johnson and Boucher, 1983; ScottJohn-
14b, 15d, 16a-c, 17a, 18b;WellsandBryce, 1993:
son, pers. comm.), eastern and Western
64, fig. 66.
— Australia (Jensen, 1992; present study), Thai-
Material Examined. Specimens with color- land(Jensen, 1992),Philippines(presentstudy),
ation more similarto T. bayeri: CASIZ 065743, one Indonesia (present study), Malaysia (present
sNpeewcimGeuni,nedai,sse1c0temd,dhepatrhb,or15whaJrafn,uaMrayda19n8g8,,PTa.pMu.a study), Madagascar (present —study).
Gosliner. CASIZ086385, one specimen, barrierreef External Morphology. mThme living an-
wnw of Rasch Passage, 4 m depth, 14 June 1992, imals (Fig. 1A, B) are 12-20 in length.
T.M. Gosliner. CASIZ 072919, one specimen, Specimens with coloration typical of T. bayeri
Daphne's Reef, between Wongat and Sinub Islands, are dark brown to black with a series of 6-10
15 mdepth, 1 October, 1986,T. M.Gosliner.CASE cream to yellow longitudinal lines on the head
071469,onespecimen,dissected, SaintCrispinReef, and parapodia. The edge of the parapodia may
nw of Port Douglas, Queensland, Australia, 15-20 be lined with an orange to red-orange line (a
m depth, 9 December 1984, M.L. Gosliner. CASIZ single specimen from Papua New Guinea), an
0la8n7d1,23M,anoandeo,speScuilmaewne,siunIdnedornersoicak,, 3Momntedehpatghe, I1s7- aofbsaenrcoewooffobtlhaecrkpsipgomtsen(tspgeicviinmgentshefriommprGeussaimo)n
GOSLINER: THURIDILLA
FlGURE 1. Living animals. A. Thuridilla bayeri (Marcus, 1965), Madang, Papua New Guinea, 20mm in length. B.
Thuridillabayeri(Marcus, 1965),withcolorationtypicalofT.ratna Marcus, 1965,NosyBe,Madagascar, 15mminlength.
C. Thuridilla livida (Baba, 1955), Sodwana Bay, South Africa, 17mm in length. D. Thuridilla lineolata (Bergh, 1905),
Manado,Indonesia,photographbyPaulineFiene-Sevems,20mminlength. E.Thuridillasplendens(Baba, 1949),Okinawa,
photobyRobertF. Borland,25mm inlength. F. Thuridillamoebii(Bergh, 1888),SodwanaBay,SouthAfrica, 12mmin
length.
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Volume49, No. 1
or bluish green patches (specimens from the the footisredororange. The insideofthepara-
MarshallIslands).Otherspecimenslackanyad- podia is usually brownish with scattered tur-
A
ditional pigment along the margin of the para- quoise blue pigment. thin, white marginal
podia. Red-orange pigment may be present at band is present and a broader, orange submar-
the posterior junction of the parapodia. Six to ginal band may be prominent or absent. —
seven bright blue, ovoid spots are found sub- Pericardium and Dorsal Vessels. In
marginally along the length of each parapod- specimens with coloration typical of T. bayeri,
ium. The head mayalso havea mid-dorsal blue the pericardium is ovoid (Fig. 2A-C). From its
mark or paired spots between the rhinophores. sides, are two lateral vessels which bifurcate
Basally, the rhinophores are the same color as terminally or remain undivided. From the pos-
the generalbody, with cream longitudinal lines. terior end of the pericardium are two other
These lines expandand unite into a large trans- blood vessels, that arejoined basally. They are
verse white band. This band may continue to bifurcate or slightly more highly branched.
the apex ofthe rhinophores ormay be followed The branching of the dorsal vessels was ex-
by a red band or streaks. A single specimen amined in four specimens with coloration typ-
from the Solomon Islands (ScottJohnson, pers. ical ofT. ratna (Fig. 2D-G). In all cases, there
comm.) has an additional apical black ring dis- are both lateral and posterior vessels. In one
tal to the red ring. In specimens from the Mar- individual,onlytheleftlateral branch waspres-
shall Islands, there is considerable variation in ent, but a secondary right branch was situated
the presence of the white and red pigment on off the side of the right posterior branch. The
the rhinophores. Only white pigment may be lateral branches are undivided orcontain bifur-
presentorthere may be longitudinalredstreaks cateormorehighlybranchedtips. Theposterior
that merge with the white band. The anterior vessels have a common origin from the peri-
margin of the foot is red, often with opaque cardium. They may entirely lack branches or
white. Blue spots may also be present on the have a few secondary branches.—
anterior portion of the foot. In specimens with Buccal Mass and Radula. The buccal
heavy blue spotting, the inside ofthe parapodia mass (Fig. 3A) contains a round pharyngeal
has a narrow white marginal band, a broad or- pouchandrelativelylarger,moremuscularpha-
ange band, and a broaderblackarea. Inside the ryngeal portion. There is no morphological dif-
black band is an area of bright blue pigment. ference between specimens of different color
The coloration of the inside of the parapodia patterns. In two specimens with coloration typ-
is not known from specimens with little blue ical of T. bayeri, the radula contains 24-26
pigment. teeth. There are 7-8 teeth in the dorsal portion
In specimens with coloration typical of T. of the radula, 7-8 in the ventral portion and 9
ratna, the animal is dark brown with eight to arranged in a spirally coiled fashion. No loose
ten white or cream lines along the outer side teeth were contained in the ascus. Each tooth
of the parapodia and on the head. The internal (Fig.4) iselongateandarched.Thereare 17-18
margin ofthe parapodia is usually orange. The coarse denudeson eitherside ofthe tooth. The
posteriorjunction oftheparapodia maycontain denticles continue as faint striae on the dorsal
some orange pigment. The head is the same surface of the teeth.
color as the parapodia, without any additional The radula of two specimens with coloration
pigment. Basally, the rhinophores are the same typicalofT. ratnaconsistedof26-27teeth (8-9
color as the remainder of the body. In some in the ventral limb, 8-9 in the dorsal limb and
specimens, the white orcream lines widen dis- 9 to more than 10 loose teeth in the ascus).
tally and form a transverse band. In most spec- The teeth (Fig. 5) are triangular with the ser-
imens, some red orred-orange pigment may be rated portion longer than the basal one. The
presentontherhinophores.Thismaybepresent cutting margin bears 16-18 coarsedenticlesper
as a series ofred longitudinal linesoradistinct side of the tooth.
transverse band. An apical transverse black Reproductive System (Fig. 3B-D).
band may also be present on the rhinophores. The reproductive morphology is complex and
Its presence is independent of the presence of appears complicated, due to the diffuse distri-
red pigment. The margin ofthe anterior end of bution of the ovotestis, prostatic cells and al-
GOSLINER:THURIDILLA
Figure 2. Thuridilla bayeri (Marcus, 1965). A-C. Variation in branching ofpericardial vessels in specimens with
colorationtypicalofT.bayeri.D-G. VariationinbranchingofpericardialvesselsisspecimenswithcolorationofT.ratna,
scale=4.0mm.
bumen gland throughout the parapodia. The albumen glands join together into a pair of
system is basically triaulic. The ovotestis con- ducts that join the female gland mass im-
tains lobate acini. They connect via a pair of mediately anterior to the junction of the her-
elongatehermaphroditicducts.Theseductsjoin maphroditic ducts. The female gland mass con-
immediately anteriorto theround, shortstalked sists ofseveral distinct lobes, the largest forms
ampulla.Theprostateconsistsofapproximately thebulkofthemucousgland.Neartheposterior
sixelongatefinger-shapedglands.Thealbumen end ofthe mass a spherical receptaculum semi-
gland consists of numerous digitiform ducts nisjoins the gland mass via a thin, moderately
with lateral glandular bodies. The prostate and long duct. Near the anterior end of the gland
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Figure 3. Thuridilla bayeri (Marcus, 1965). A. Buccal mass, pp=pharyngeal pouch, scale=0.25 mm. B. Entire
reproductivesystem:al=albumengland,am=ampulla,be=bursa copulatrix,fa=femaleaperture,fg=femaleglandmass,
o=ovotestis, p=penis, pr=prostate glands, rs=receptaculum seminis, scale= 1.0mm. C. Distal reproductive organs of
specimenwithcolortypicalofT.bayeri,Australia.D.DistalreproductiveorgansofspecimenwithcolortypicalofT.ratna.
C,D.,letteringsameasinB.,scale=1.0mm.
mass, the thin vas deferens emerges and joins of the parapodia that are absent in T. bayeri.
the simple unarmed penis. A saccate bursa Based on the similarity ofcolorpattern, Bro-
copulatrix emerges to the outside of the body die and Brodie (1990) considered T. bayeri and
wall near the female gonopore. The female T. ratnaassynonymous.Others (Marcus, 1965;
gonopore exits into the lateral ciliated groove, Carlson and Hoff, 1978; Jensen, 1992) have
adjacent to the anus. The penis exits below the considered them to be distinct species. Carlson
rightrhinophore. The reproductive morphology and Hoff, and Jensen emphasized the distinct-
was examined in three specimens with color- nessofthecolorpatternofT. bayeri, blue spots
ation typical of T. bayeri and two with color- along the parapodia and black spots along the
ation characterist—ic of T. ratna. parapodial margin. Carlson and Hoff (1978)
Discussion. Thuridilla bayeri is similar also noted differences in the coloration of the
in appearance and appears closely related to inner surface of the parapodia in specimens
two other species, T. ratna and T. splendens. from Guam. In T. bayeri, the margin of the
All three species are similar in having a uni- inner portion of the parapodia is white, fol-
formly dark blackish body with numerous lon- lowed by a red-orange band, an area of black,
gitudinalyelloworwhite lines. In T. bayeri and followed by a large area of steel blue. In T.
T. splendens, there are bluish markings and ratna, the submarginal red-orange band is usu-
spots on the head and parapodia. In the latter ally absent and the inside of the parapodia is
species, there are yellow spots on the surface brownish, with scattered white and blue mark-
GOSLINER: THURID1LLA
Figure4. RadularteethofspecimenwithcolortypicalofT.bayeri.A.DorsalviewoftoothfromspecimenfromKwajelin,
CASIZ099057, scale=15\xm. B. Ventral view ofteeth from same radula, scale=15|im. C. Lateralview oftooth from
specimenfromAustralia,CASIZ071469,scale=15\xm.D. Lateralviewofteethfrom specimenfromPapuaNewGuinea,
CASIZ065743,scale= 15pjn.
ings. Two specimens with external coloration specimens examined in this study further blur
matching thatofT. ratna, from Guam and Ma- the distinctness of T. bayeri. Most specimens
laysia, have a prominent red submarginal band of T. bayeri have blue pigment on the dorsal
and some bluish pigment in the pericardial re- surface of the head between the rhinophores
gion. This pigment appears to be somewhat in- and additional blue on the anterior portion of
termediate between the two species. Several the foot. One specimen from Papua New
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Figure5. RadularteethofspecimenwithcolortypicalofT.ratna.A,B.DorsalviewoftoothofspecimenfromPalau,
CASIZ099058.A.scale=15um.B.scale=7.5urn.C.VentralviewoftoothofspecimenfromBorneo,CASIZ078470,scale
= 15um.D.VentralviewoftoothofspecimenfromPalau,CASIZ099058,scale=10um.
Guinea (CASIZ 072919) examined had faint podia, but lacked any trace ofblue on the head
blue markings on the parapodia and head, but or foot. One specimen having no trace ofblue
lacked any trace of blue on the foot. Another markings has been found in the Indian Ocean
specimen from Australia (CASIZ 071469) and (Yonow, 1994). Only a single specimen having
the specimen from the Maldives illustrated by coloration similar to T. ratna has been found
Yonow (1994), had faintblue lines on thepara- from the western Indian Ocean. Thuridilla
GOSLINER:THURIDILLA
ratna isconsidereduncommon inWestern Aus- this basis, Thuridilla ratna is regarded as aju-
tralia (Wells and Bryce, 1993) and, together nior synonym of T. bayeri. Both species were
withJensen's (1992)recordfrom Thailand,rep- described in the same paper (Marcus, 1965),
resents the only other record ofthis color form but T. bayeri appears first in the text and is,
from the Indian Ocean. therefore, regarded as the senior synonym.
Internally, there is little difference between As noted above, specimens of Thuridilla
Thuridilla bayeri, T. ratna and T. splendens. splendens are similar in coloration and internal
All three have paired lateral vessels from the anatomy to T. bayeri. However, specimens of
pericardium andposterior vessels that originate T splendens are consistently different in that
from a commonjunction with the pericardium. they haveyellow spots on the sides ofthepara-
There are fewer lateral branches in most spec- podia and foot which are absent in all variants
imens with the color pattern of T. bayeri, of T. bayeri. In addition, the pharyngeal pouch
though there is considerable overlap in branch- is somewhat proportionately larger in T.
ing pattern with specimens typical of T. ratna splendens. On these bases, T. splendens is re-
and T. splendens. Jensen (1992) indicated that garded as distinct from T. bayeri.
there are slight differences in the size of the
pharyngealpouchandshapeoftheradularteeth
between T. bayeri and T. ratna. No consistent 2. Thuridilla lineolata (Bergh, 1905)
differences in the relative proportions of the
muscular buccal mass and pharyngeal pouch Elysia? lineolata Bergh, 1905: 85, pi. 3, fig. 10, pi.
and theshapeandsizeoftheradularteethcould 13, figs. 25, 26.
be determined in the present material, with one Thuridilla lineolata (Bergh) Jensen, 1992: 277.
—
exception. The pharyngeal pouch of T. Material Examined. CASIZ 070285, one
splendens is slightly largerproportionately than specimen, Manado, Sulawesi, Indonesia, 0.5 m
the pouch of T. bayeri and T. ratna. The con- depth, 21 May 1989, PaulineFiene-Severns. CASIZ
figuration ofthereproductivesystem, including 099059, two specimens, one dissected, Bunaken Is-
the shape of the bursa copulatrix and penial land, Manado, Sulawesi, Indonesia, 3 m depth, 20
May 1990, Pauline Fiene-Severns.
papilla, is virtually identical in the specimens
typical of T. bayeri, T. ratna and T. splendens —
examined in this study. Distribution. Thisspecies isknown only
Color photographs of more than 50 speci- from Indonesia (Bergh, 1905;—present study).
mens of Thuridilla bayeri and T. ratna from a External Morphology. The living an-
broad geographical area were compared in de- imals (Fig. ID) are light blue. The edge ofthe
tail. No consistent difference in pattern could parapodiais linedwith aband ofbrightorange.
be discerned. Thefactthatsome specimens had Immediately inside this band is a narrower
faint blue markings on the parapodia and en- blackband.Twoblacklinesandanorangeband
tirely lacked blue markings on the head and arepresentat thebaseoftheparapodia, as well.
foot, suggests that they are intermediate in col- There is a narrow black band surrAounding the
head, near the level of the eyes. v-shaped
oration between that described for the two spe-
cies. No consistent anatomical differences black band is near the middle of each
rhinophore and the rhinophores are tipped with
could be found in branching of the dorsal ves-
sels, morphology of the buccal mass, radula or orange. Orange pigment is present on the an-
reproductive system that could be correlated terior margin of the foot.
with differences in coloration. All ofthese data Pe—ricardium and Dorsal Vessels (Fig.
6A). There are paired lateral and posterior
strongly suggest that the described differences
between T. bayeri and T. ratnaare simply vari- vessels. These vessels are thin compared to
most other species. The anterior vessels are bi-
ation within a single species that is extremely
variable in its coloration. Johnson and Boucher furcate near their tips. The more posterior ves-
sels have separate origins from thepericardium
(1983) noted that the egg capsule size of T.
bayeri and T. ratna was somewhat different. and give rise to one or two shor—t branches.
Buccal Mass and Radula. The buccal
Possible developmental differences of the two
color forms require further investigation. On mass (Fig. 6B, C) contains a large pharyngeal
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Figure6. Thuridilla lineolata(Bergh, 1905). A. Branchingofpericardialvessels,scale=4.0 mm.B. Lateralviewof
buccal mass. C. Ventral view of buccal mass. B., C. pp=pharyngeal pouch, scale=0.25mm. D. Ventral view ofdistal
reproductiveorgans:am=ampulla,be=bursacopulatrix,p=penis,rs=receptaculumseminis,scale=0.5mm.
Figure 7. Thuridilla lineolata (Bergh, 1905). Radular teeth. A. Lateral view of specimen from Indonesia, CASIZ
099059,scale= 10um.B.Ventralviewofsame,scale=15urn.