Previously undocumented diversity and abundance of cryptic species: a phylogenetic analysis of

112 Pages·2011·23.08 MB·English

Zoological Journal of the Linnean Society, 2011, 161, 245–356. With 88 figures
Previously undocumented diversity and abundance of
cryptic species: a phylogenetic analysis of Indo-Pacific
Arminidae Rafinesque, 1814 (Mollusca: Nudibranchia)
with descriptions of 20 new species of Dermatobranchus
D
o
w
TERRENCE M. GOSLINER1* and SHIREEN J. FAHEY2 n
lo
a
d
1California Academy of Sciences, 55 Music Concourse Drive, San Francisco, CA 94118, USA ed
2University of the Sunshine Coast, Maroochydore DC QLD 4558, Australia fro
m
Received 11 May 2009; revised 6 November 2009; accepted for publication 16 December 2009 http
s
://a
c
a
d
The phylogenetic relationships amongst theArminidae were analysed based upon morphological characters of 58 em
presently described species or nudibranchs, including 35 previously described Arminidae and 20 new species of ic
.o
Dermatobranchus. From the literature review and anatomical examinations, 43 characters were considered for 78 u
p
taxa. These characters were polarized using Berthella canariensis as the outgroup taxon and the type species of .c
o
several other genera identified from recent publications. The resulting phylogeny supports the monophyly of m
Arminidae, Dermatobranchus, Doridina, and Proctonotidae. The paraphyly of the Arminina is further demon- /zo
o
strated in this study. Two previously described, but poorly known, species of Indo-Pacific Armina are redescribed, lin
Armina magna Baba, 1955 and Armina paucifoliata Baba, 1955. The anatomy and taxonomic status of nine ne
a
previously described species of Dermatobranchus were examined in this study. The anatomy of Dermatobranchus n
/a
pspuesctuimloesnu.sI(tviasnreHdaessscerlitb,e1d8a2n4d) hitassrbaenegneoisveerxloteonkdededsitnoceseBveerraglhn(e1w88l8o)cailliltuisetsraintedthtehweersatdeurnlaPoafcivfiacn. DHearsmsealtto’s- rticle
branchus pulcherrimus Miller & Willan, 1986 is considered here as a new synonym of Dermatobranchus rubidus -a
b
(Gould, 1852). The following 20 species of Dermatobranchus are new and are described in the present paper: stra
Dermatobranchusalbineussp.nov.,Dermatobranchusarminussp.nov.,Dermatobranchuscaesitiussp. c
nov.,Dermatobranchuscaeruleomaculatussp.nov.,Dermatobranchuscymatilissp.nov.,Dermatobran- t/1
6
chus dendonephthyphagus sp. nov., Dermatobranchus diagonalis sp. nov., Dermatobranchus earlei sp. 1/2
nov., Dermatobranchus fasciatus sp. nov., Dermatobranchus funiculus sp. nov., Dermatobranchus /2
4
kalyptos sp. nov., Dermatobranchus kokonas sp. nov., Dermatobranchus leoni sp. nov., Dermatobran- 5
/2
chus microphallus sp. nov., Dermatobranchus oculus sp. nov., Dermatobranchus phyllodes sp. nov., 7
3
Dermatobranchuspiperoidessp.nov.,Dermatobranchusrodmanisp.nov.,Dermatobranchussemilunus 20
7
sp.nov.,andDermatobranchustuberculatussp.nov.EighteenofthesenewtaxaarefoundintheIndo-Pacific 4
b
tropics and two are found in temperate South Africa, D. albineus and D. arminus. Unique combinations of y
morphologicalcharactersdistinguishtheseasnewspeciesofDermatobranchus.Severalspeciesthatareexternally gu
e
similar have radically divergent internal morphology, are members of different clades of Dermatobranchus, and s
represent cryptic species. Especially important is the radular morphology, which shows remarkable diversity of t on
form, probably related directly to the diversification of feeding of members of this clade on various octocorals. 06
A
p
©doi2:01101.1T1h11e/jL.1in09n6e-a3n64S2o.c2i0e1ty0.o0f06L4o9n.dxon, Zoological Journal of the Linnean Society, 2011, 161, 245–356. ril 2
0
1
9
ADDITIONAL KEYWORDS: Arminina – biodiversity – biogeography – Indo-Pacific – systematics – trophic
diversification.
INTRODUCTION
Recent surveys of several localities throughout the
Indo-Pacific tropics and from temperate southern
*Corresponding author. E-mail: [email protected] Africa have produced an abundance of specimens of
Re-use of this article is permitted in accordance with the
Dermatobranchus species. Few of these specimens
TermsandConditionssetoutathttp://wileyonlinelibrary.com/
onlineopen#OnlineOpen_Terms canbeidentifiedaspreviouslydescribedtaxaandthe
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356 245
246 T. M. GOSLINER and S. J. FAHEY
majority of specimens represent undescribed species. new characters or combination of characters can
Specimens from these collections representing 20 further elucidate the phylogeny of the group. Field
undescribed species are here described, doubling the work over the last two decades has produced a rich
knowndiversityofthetaxon.Manyofthesetaxahave diversity of new taxa from many localities in temper-
similar external anatomy, but radically divergent ate South Africa and tropical localities in South
internal anatomy and are therefore considered to Africa,Madagascar,ReunionIsland,Oman,Malaysia,
represent cryptic species. Detailed comparison of Philippines, Papua New Guinea, Indonesia, and
these species provides critical new information for Okinawa.TwentynewIndo-PacificandSouthAfrican
discerning these taxa. Dermatobranchusspeciesaredescribedandcompared
Six genera have traditionally been recognized toknownspecies.Aphylogeneticanalysisispresented
D
withintheArminidae:ArminaRafinesque,1814,Der- that incorporates the newly described species along o
w
matobranchus Hasselt, 1824, Histiomena Mörch, with Arminidae from other geographical localities. n
lo
1859, Linguella Blainville, 1823, Pleurophyllidiella Outgrouptaxawerechosenfromothercloselyrelated a
d
e
Eliot, 1903, and Pleurophyllidiopsis Tchang-Si, 1934 andmorebasallysituatednudibranchgroupsinorder d
(Kolb & Wägele, 1998). However, some recent publi- to gain a better perspective of the evolution within fro
m
cations (see for example Willan, 1997) suggest that and amongst the Arminidae. h
only three genera should be included in the Armin- ttp
s
idae (Armina, Dermatobranchus, and Heterodoris). MATERIAL AND METHODS ://a
Early authors presented summaries of the charac- ca
teristics that distinguish the genera of Arminidae MORPHOLOGICAL ANALYSIS de
m
(Odhner, 1934; Pruvot-Fol, 1937; Odhner, 1939; Mac- Type material and additional nontype material were ic
.o
Farland, 1966; Marcus & Marcus, 1966). However, obtained from the California Academy of Sciences u
p
someofthecharactersthattheseauthorscitedarenot (CASIZ) and the South African Museum (SAM A). .co
m
unique to the group, but are also found in other Specimens were drawn from microscopical examina- /z
nudibranch taxa. These characters included for tion using a camera lucida attached to a dissecting oo
exampletheshapeoftherhinophoresandthepresence microscope. Following dissection that began with a linn
e
ofhyponotallamellae.Kolb&Wägele(1998)followed dorsal or ventral incision, the internal anatomy was a
n
these early authors with a table of characters, along examinedanddrawneitherbycompoundorscanning /a
with a discussion of those characters and a phyloge- electron microscope (SEM). External features were rtic
le
neticanalysisofthefamilywithadetaileddiscussion examineddirectlywhenspecimenswereavailable,by -a
b
of the history of the classification. Kolb (1998) com- photographs, or by literature review (see Table1). In stra
pletedathoroughexaminationofthemorphologyand cases involving new species, where more than two c
t/1
histologyoffourspeciesofArminaandmadecompari- specimens were available for study, at least two indi- 6
1
sons to other species of Armina. Her results showed viduals were dissected for full anatomical study to /2
/2
littlevariationamongstspecieswithregardtoexternal determine intraspecific variation. In instances where 4
5
characters such as number of notal ridges, caruncle onlytwoindividualswereavailableforstudy,onewas /2
7
shape, and number of rhinophoral lamellae. Other fullydissectedandthesecondwasexaminedforexter- 32
0
characters that had historically been considered to nal anatomy, thereby retaining an intact holotype. In 7
4
distinguishamongstspecies,suchasrowsofjawrods caseswhereonlyasingleindividualwasavailable,the b
y
and ampulla morphology were also shown to provide specimen was fully dissected and the parts preserved gu
e
littlephylogeneticinformation.Kolb&Wägele(1998) asadissectedholotype.Inafewinstances,suchasin s
concluded that only two morphological characters Dermatobranchusrodmani,Dermatobranchussemilu- t on
0
unitetheArminidae,thepresenceofmarginalsacsand nus,andDermatobranchustuberculatus,theholotype 6
A
rhinophores with longitudinal lamellae. wasalsodissected,withtheradularemoved.Thiswas p
Several recent publications have contributed con- carried out to ensure that these individuals were ril 2
0
siderablytotheknowledgeoftheArminina(Gosliner, conspecific with other material in instances where 1
9
1981; Miller & Willan, 1986; Gosliner & Behrens, cryptic species were difficult to identify from external
1996; Jensen, 1997; Kolb, 1998; Ardila & Valdés, morphology alone. In the Material examined section,
2004). This species-rich group of nudibranchs has a all specimens indicated as dissected were dissected
worldwide distribution, with species described from duringthepresentstudy.Specialattentionwasgiven
all oceans (see Kolb & Wägele, 1998 for a discussion tothereproductiveanatomy,assomeofthesefeatures
of the biogeographical distribution and map). were infrequently or cursorily described in the litera-
The present study builds on the previously pub- ture.Inordertoseetheampullaandbursacopulatrix
lished studies of the Arminidae by further examina- it is necessary to dissect the nidamental glands as
tion of several morphological characters. We expand these structures are situated inside the folds of the
the morphological character list to test whether any female gland mass.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
SYSTEMATICS AND PHYLOGENY OF DERMATOBRANCHUS 247
Table1. Sources of morphological data for described species studied
Additional
material
Species Distribution Literature examined
Outgroup
Berthella canariensis Cervera Canary Islands Cervera etal., 2000
etal., 2000
Doridina
D
Actinocyclus verrucosus Ehrenberg, Red Sea,Australia, Valdés, 2002 o
w
1831 Hawaii n
lo
Bathydoris hodgsoni Eliot, 1907 Weddell Sea Wägele, 1989 a
d
Calycidoris guentheri Abraham, AlaskanArctic Abraham, 1876; Fahey & e
d
1876 Valdés, 2005 fro
Diaphorodoris luteocincta Sars, Mediterranean, north and Portmann & Sandmeier, 1960; m
h
1870 eastAtlantic Schmekel & Portmann, 1982; ttp
Fahey & Valdés, 2005 s://a
Dendronotina Tritoniidae c
a
d
Marionia echinomuriceae Jensen, Hong Kong Jensen, 1994 e
m
1994 ic
Tritonia bollandi Smith & Okinawa, Indonesia Smith & Gosliner, 2003 .ou
p
Gosliner, 2003 .c
o
Tritonia hombergi Cuvier, 1803 North-east Europe Odhner, 1922; Pruvot-Fol, 1937, m
1954; Thompson, 1961; /zo
o
Thompson & Brown, 1984; lin
Gosliner & Ghiselin, 1987 ne
a
n
Arminina Dironidae /a
Dirona picta MacFarland in West coast of North Cockerell & Eliot, 1905; Marcus, CASIZ 144725 rtic
Cockerell & Eliot, 1905 America 1961; MacFarland, 1912, 1966 le-a
b
Arminina Heroidae s
Hero formosa Lovén, 1841 Scotland Bergh, 1888; Thompson & trac
Brown, 1984 t/1
6
1
Arminina Heterdorididae /2
Heterodoris antipodes Willan, 1981 New Zealand Willan, 1981 /24
5
Heterodoris robusta Verrill & NorthAtlantic Verrill & Emerton in Verrill, /2
7
Emerton, 1882 1882; Odhner, 1926; Bouchet, 3
2
1977; Willan, 1981 07
4
Arminina Madrellidae b
y
Madrella ferruginosa (Angas, 1864) Eastern Mediterranean Alder & Hancock, 1864; Angas, CASIZ 115754 g
u
e
Okinawa, South-east 1864; Thompson etal., 1990 CASIZ 115806 s
Australia, Madagascar t o
n
0
Arminina Pinufiidae 6
A
Pinufius rebus Marcus & Marcus, Western Pacific, Maldives Marcus & Marcus, 1960a; p
1960 Rudman, 1981a ril 2
0
Arminina Proctonotidae 19
Bonisa nakaza Gosliner, 1981 West and east South Gosliner, 1981
Africa
Caldukia affinis (Burn, 1958) South-eastAustralia Burn, 1958; Burn & Miller, CASIZ 071914
1969
Caldukia albolineata Miller, 1969 New Zealand Miller & Willan, 1986; Miller,
1970
Caldukia rubiginosa Miller, 1969 New Zealand Miller, 1970
Galeojanolus ionnae Miller, 1971 New Zealand Miller, 1971
Janolus australis Bergh, 1884 Arafura Sea Bergh, 1884; Gosliner, 1981
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
248 T. M. GOSLINER and S. J. FAHEY
Table1. Continued
Additional
material
Species Distribution Literature examined
Janolus capensis Bergh, 1907 West and east South Gosliner, 1981
Africa
Janolus hyalinus (Alder & Australia, New Zealand, Alder & Hancock, 1854, 1855;
Hancock, 1854) Europe, Mediterranean Bergh, 1888; Eliot, 1906;
Schmekel, 1970; Gosliner, D
o
1981; Schmekel & Portmann, w
n
1982; Thompson & Brown, lo
a
1984; Miller & Willan, 1986 de
d
Janolus longidentatus Gosliner, East coast of SouthAfrica Gosliner, 1981 fro
1981 m
h
ArmininaArminidae ttp
Ar1m9i8n6a aoteana Miller & Willan, New Zealand Miller & Willan, 1986 s://ac
a
Armina cf. babai (Tchang-Si, 1934) Hong Kong Baba, 1949; Jensen, 1997 d
e
Armina bayeri Marcus & Marcus, WestAfrica Marcus & Marcus, 1966 m
ic
1966 .o
u
Armina californica (Cooper, 1863) Gulf of Panama, Mexico, Cooper, 1863; Marcus, 1961 CASIZ 171955 p
.c
western USA o
m
Armina columbiana O’Donoghue, Oregon, British Columbia O’Donoghue, 1921; Marcus, /z
o
1924 ,to Panama 1961 o
lin
Armina comta (Bergh, 1880) Hong Kong Jensen, 1997 n
e
Armina cordellensis Gosliner & Cordell Bank, California Gosliner & Behrens, 1996 CASIZ 105717 an
Behrens, 1996 /a
Armina elongata Ardila & Valdés, Columbia Ardila & Valdés, 2004 rticle
2004 -a
b
Armina gilchristi (Bergh, 1907) SouthAfrica Bergh, 1907; Marcus & Marcus, CASIZ 087273 stra
1966; Gosliner, 1987 CASIZ 087388 c
Armina joia Marcus & Marcus, WestAfrica Marcus & Marcus, 1966 t/16
1
1966 /2
Armina juliana Ardila & Diaz, Colombia Ardila & Diaz, 2002; Ardila & /2
4
5
2002 Valdés, 2004 /2
7
Armina loveni (Bergh, 1860) Norway, Britain, Denmark Pruvot-Fol, 1954; Marcus & CASIZ 074516 3
2
Marcus, 1966; Kolb, 1998; 0
7
Ardila & Diaz, 2002 4 b
Armina maculata Rafinesque, 1814 Mediterranean, Portugal, Pruvot-Fol, 1937, 1954; Marcus y g
u
Angola & Marcus, 1966; Schmekel & e
s
Portmann, 1982; Kolb, 1998 t o
n
Armina magna Baba, 1955 Japan, Philippines Baba, 1955 CASIZ 173357 0
6
CASIZ 174127 A
Armina mülleri (Ihering, 1886) Brazil MaMrcaurcsu&s &MaMrcaurcsu,s1,916966;0b, pril 2
0
1967; Ardila & Diaz, 2002; 19
Ardila & Valdés, 2004
Armina neapolitana (Delle Chiaje, Mediterranean Pruvot-Fol, 1937, 1954; Marcus CASIZ 068478
1824) & Marcus, 1966; Kolb, 1998
Armina papillata Baba, 1933 Hong Kong Baba, 1933; Baba, 1955; Jensen,
1997
Armina paucifoliata Baba, 1955 Japan Philippines CASIZ 171415
CASIZ 174128
Armina punctulata Lin, 1990 Hong Kong Jensen, 1997
Armina semperi (Bergh, 1861) Sagami Bay, Singapore, Baba, 1955
Philippines
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
SYSTEMATICS AND PHYLOGENY OF DERMATOBRANCHUS 249
Table1. Continued
Additional
material
Species Distribution Literature examined
Armina tigrina Rafinesque, 1814 Mediterranean, Portugal, Pruvot-Fol, 1937, 1954; Marcus CASIZ 87181
Senegal, Sargasso, Gulf & Marcus, 1966; Thompson
of Mexico etal., 1990; Kolb, 1998; Ardila
& Diaz, 2002
Armina variolosa (Bergh, 1904) Hong Kong Bergh, 1904; Baba, 1949; D
o
Jensen, 1997 w
n
Armina xandra Marcus & Marcus, WestAfrica Marcus & Marcus, 1966 lo
a
1966 de
d
Dermatobranchus albus (Eliot, Okinawa Eliot, 1904; Edmunds & CASIZ 087896 fro
1904) Thompson, 1972 CASIZ 105263 m
Dermatobranchus fortunatus EasternAustralia, Bergh, 1888; Marshall & CASIZ 065771 h
(Bergh, 1888) Okinawa, Kerama Willan, 1999 ttps
Island ://a
c
Dermatobranchus gonatophora Indonesia, Okinawa, Bergh, 1887, 1905; Gosliner, CASIZ 105299 a
d
e
(Hasselt, 1824) SouthAfrica Behrens & Williams, 1996 m
Dermatobranchus marginlatus Lin, China Lin, 1981 ic.o
1981 up
Dermatobranchus multistriatus China Lin, 1981 .co
m
Lin, 1981 /z
Dermatobranchus ornatus (Bergh, Sagami Bay, Okinawa, Baba, 1949; 1976 CASIZ 159387 oo
1874) Thailand CASIZ 144033 lin
n
CASIZ 144008 ea
n
CASIZ 156334 /a
Dermatobranchus otome Baba, Sagami Bay Baba, 1992 CASIZ 082031 rtic
le
1992 CASIZ 082033 -a
CASIZ 082065 bs
Dermatobranchus primus Baba, Sagami Bay Baba, 1976 tra
c
1976 t/1
6
Dermatobranchus pulcherrimus New Zealand Miller & Willan, 1986 CASIZ 105696 1
/2
Miller & Willan, 1986 /2
4
Dermatobranchus pustulosus Indonesia, Philippines Hasselt, 1824 CASIZ 069306 5
/2
Hasselt, 1824 CASIZ 157212 7
3
CASIZ 083865 20
7
CASIZ 085963 4
b
CASIZ 096293 y
g
CASIZ 083798 u
e
CASIZ 085904 st o
Dermatobranchus rubidus (Gould, Hawaii Gould, 1852; Kay, 1979 CASIZ 116909 n
0
1852) 6
A
Dermatobranchus semistriatus Sagami Bay, Baba, 1949, 1976 CASIZ 104706 p
Baba, 1949 ril 2
0
Dermatobranchus striatus (Hasselt, Sagami Bay, Indonesia Baba, 1949, 1976, 1992; Bergh, CASIZ 170101 1
9
1824) 1905 CASIZ 086314
Dermatobranchus tongshanensis China Lin, 1981
Lin, 1981
Histiomena convolvula (Lance, Gulf of California to Mörch, 1860; Lance, 1962 CASIZ 074274
1962) Panama CASIZ 020300
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
250 T. M. GOSLINER and S. J. FAHEY
PHYLOGENETIC ANALYSIS RESULTS
TAXONOMIC SECTION
Fifty-fivespeciesofArminidaewereconsideredforthe
SPECIES DESCRIPTIONS
presentanalyses.Allofthesespecieswereincludedin
the final analysis. Six additional species of Dermato- FAMILY MADRELLIDAE VAYSSIÈRE, 1909
branchus were excluded from the analysis owing to GENUS MADRELLA ALDER & HANCOCK, 1864
lack of sufficient morphological information. Forty-
Type species: Madrella ferruginosa Alder & Hancock,
three morphological characters were considered for
1864, by original designation.
thepresentstudyandallcharacterswereincludedin
thefinalanalysis.Table1containsalistofsourcesof
D
material for previously described species included in o
the phylogenetic analysis. The character matrix is MADRELLA FERRUGINOSA ALDER & HANCOCK, 1864 wn
lo
shown in Table2. Phylogenetic analyses were per- Material examined: CASIZ 115806, two specimens, a
d
formed using the program PAUP v. 4.0 (Swofford, 10–12mmalive,onedissected,TenganPier,Ishikawa ed
2002) using the heuristic algorithm (tree bisection- City, Okinawa, Japan, collected 25.vi.1995 by R. fro
m
reconnection branch swapping option), set at Bolland (3218-D), 12m depth. CASIZ 121200, one h
maximum parsimony. One hundred replicates were specimen, 5mm preserved, dissected, Bigej-Mack ttp
s
run with starting trees obtained using stepwise addi- Reef, Kwajalein Atoll, J. Johnson, 10.x.1995, 35m ://a
tion. Characters were unordered and were polarized depth. CASIZ 099104, seven specimens, 3–9mm ca
d
using the following outgroup species: Actinocylus ver- alive, Tengan Pier, Ishikawa City, Okinawa, Japan, e
m
rucosus Ehrenberg, 1831, Bathydoris hodgsoni Eliot, collected 5.iii.1994 by R. Bolland (3218), 12m depth. ic
.o
1907, Berthella canariensis Cervera etal., 2000, u
p
based on Valdés’ (2002) and Fahey & Valdés’ (2005) .co
Geographicaldistribution:Thisspeciesisknownfrom m
analyses of the Onchidorididae, Bonisa nakaza Gos- /z
liner, 1981, Caldukia affinis (Burn, 1958), Caldukia India(Alder&Hancock,1864),Japan(Baba,1949,as oo
albolineata Miller, 1970, Caldukia rubiginosa Miller, M. sanguinea; present study), South Africa (Fraser, linn
2001), the Marshall Islands (present study), and e
1970, Calycidoris guentheri Abraham, 1876 based on a
n
Millen & Martynov’s (2005), Valdés’ (2002), and Madagascar (present study). /a
Fahey & Valdés’ (2005) analyses of the Onchidorid- rtic
le
idae, Diaphorodoris luteocincta (Sars, 1870) based on -a
Buccal armature: The jaws are large and thickly b
theanalysisoftheGoniodorididaebyGosliner(2004), cuticularized with a thick masticatory margin and stra
Valdés’(2002)andFahey&Valdés’(2005)analysesof c
two to three rows of long, pointed denticles. The t/1
the Onchidoridae, Dirona picta MacFarland in Cock- 6
radular formula of CASIZ 121200 is 48¥1.1.1.1.1. 1
erell & Eliot, 1905, Galeojanolus ionnae Miller, 1971, /2
The rachidian teeth are claw-shaped with a thick, /2
Hero formosa Lovén, 1841, Heterodoris antipodes 4
projecting, pointed central cusp that has six pointed, 5
Willan, 1981, Heterodoris robustus Verrill, 1882, /2
Janolus australis Bergh, 1884, Janolus capensis flankingdenticlesoneachside.Thenextlateraltooth 732
isalsoclaw-shapedwithtenshorter,pointeddenticles 0
Bergh, 1907, Janolus hyalinus (Alder & Hancock, 7
1864), Janolus longidentatus Gosliner, 1981, thatdecreaseinsizetowardstherachidiantooth.The 4 b
Madrella sanguinea (Angas, 1864), Marionia echino- next lateral tooth is a long pointed hook with no y gu
denticles. e
muriceae Jensen, 1994, Pinufius rebus Marcus & s
Marcus, 1960a, Tritonia bollandi Smith & Gosliner, t on
0
2003,andTritoniahombergiCuvier,1803.Inaddition 6
totheoutgrouptaxon,thesetaxaincludefourspecies FAMILY DIRONIDAE ELIOT, 1910 Ap
of Doridina, three species of Dendronotina and 15 GENUS DIRONA MACFARLAND IN COCKERELL & ril 2
0
outgroup members of the Arminina not traditionally ELIOT, 1910 19
included in the Arminidae. All three Dendronotina
Typespecies:DironapictaMacFarlandinCockerell&
were members of the Tritoniidae as members of this
Eliot, 1905, by original designation.
familyhavebeentraditionallyconsideredasthemost
basal Dendronotina (Odhner, 1939).
Synapomorphies were mapped using the character
trace option in MacClade 4.08 (Maddison & Maddi- DIRONA PICTA MACFARLAND IN COCKERELL &
son,2005)usingthemajorityruletreefromthePAUP ELIOT, 1905
analysis. Material examined: CASIZ 144725, four specimens,
Bremer analyses were performed on the strict con- San Francisco Bay, California, collected 16.ix.1975 by
sensustreetoestimatebranchsupport(Bremer,1994). K. Mauzey, 5m depth.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
SYSTEMATICS AND PHYLOGENY OF DERMATOBRANCHUS 251
Table2. Data matrix of character states in the taxa examined for the phylogenetic analysis ofArminidae
1 10 20 30 35 40 43
Berthella canariensis 000-000200021011000-----00011101----2010000
Actinocyclus verrucosus 010-0100-0000000000----111000000----2011000
Bathydoris hodgsoni 010-0100-10000000010-110000111001---0--0000
Calycidoris guentheri 010-0100-0000000010-----0001111-----2010000
Diaphorodoris luteocincta 010-0100-0000010010-----1001--1-----2010000
Marionia echinomuriceae 1-1-00121002101100102110010111001---21?0000
Tritonia bollandi 1-1-001210021000001101100?0???0000??2111000 D
o
Tritonia hombergi 1-1-001210021000001111100?0???00?0??2?????0 w
n
Dirona picta 1-1-0012000000000110-2101001--001---2000010 lo
a
Hero formosa 1-1-0011-0020??0011102101?0???0002????????0 de
d
Heterodoris antipodes 1-100102000010000110-2000?0???001---2100000 fro
Heterodoris robusta 1-000102000010000111??00??0???001---2010000 m
Madrella sanguinea 1-0-01120002100101111210110---001---???1000 h
ttp
Pinufius rebus 1-0-00120002000001110210------00020?0001000 s
Bonisa nakaza 1-0-0011-00000100111020010000-001---1011010 ://a
c
Caldukia affinis 1-0-0011-00000000110-110000000000---?111010 ad
e
Caldukia albolineata 1-0-0011-0000000011101001000000002--?101000 m
Caldukia rubiginosa 1-0-0011-0000000011101001000000002--?101010 ic.o
Galeojanolus ionnae 1-0-0011-1000010011101001000000002--1000100 up
Janolus australis 1-0-0100-00000100110-200000111001---10?01?0 .co
m
Janolus capensis 1-0-0011-00000000110-000000111001---1010100 /z
Janolus hyalinus 1-0-0011-00000100110-000100111001---1000100 oo
Janolus longidentatus 1-0-0011-0000010011110000001110002211001100 lin
n
e
Armina aoteana 1-10100200111001101101101000000000000000000 a
n
Armina bayeri 1-00100200111011101100101001110000000?????0 /a
Armina californica 1-00100200111001101101100000010000000010010 rtic
le
Armina comta 1-10100201?11011101112101001110000000001000 -a
Armina cordellensis 1-100102?0?11001101112101000110000000001000 bs
Armina elongata 1-10100210111001101112101000000001000001000 tra
c
Armina gilchristi 1-10100200011001101101101?0???0001?00?????0 t/1
6
Armina joia 1-10100200111011101111101000000000000?????0 1
/2
Armina juliana 1-10100200111001101112101000000000000111010 /2
4
Armina loveni 1-10100200111001101101101000000001000010000 5
/2
Armina maculata 1-10010200011001101101101001110000000010000 7
3
Armina magna 1-10100200011001111101101000010000000000000 20
7
Armina mulleri 1-10100200111011101101101000010001000110010 4
b
Armina neapolitana 1-10100200111001101112101000000000000010000 y
g
Armina papillata 1-10100210111001101112101000000000000001000 u
e
Armina paucifoliata 1-10100200011001101101101000010000000010000 st o
Armina punctulata 1-10010200111001101112101000000000000000000 n
0
Armina variolosa 1-10010210111101101111101000110000000001000 6
A
Armina xandra 1-00010200111011101112101100110000000?????0 p
Dermatobranchus albopunctulatus 1-1110020001100000111200100011001---0?????? ril 2
0
Dermatobranchus albus 1-21100200011000011112101211110000100001000 1
9
Dermatobranchus fortunatus 1-21010200011000021111101210000002120011000
Dermatobranchus gonatophorus 1-1110020001100000111110100000001---0001000
Dermatobranchus marginlatus 1-1110020001100000111200100001000000???????
Dermatobranchus multistriatus 1-1110020001100000111201100011001---???????
Dermatobranchus nigropunctatus 1-1110020001100000111201100111001---0??????
Dermatobranchus ornatus 1-1101020001100000111111100111001---0001001
Dermatobranchus otome 1-21100200011000011112101211110000100011000
Dermatobranchus pulcherrimus 1-1110020001110000111200100000000000000000?
Dermatobranchus pustulosus 1-11100200011000001102001000010001100011000
Dermatobranchus rubidus 1-1110020001110000111200100000000000000100?
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
252 T. M. GOSLINER and S. J. FAHEY
Table2. Continued
1 10 20 30 35 40 43
Dermatobranchus semistriatus 1-11100200011000001112101100110002100??????
Dermatobranchus striatus 1-2110020001100001111210121111000010001100?
Dermatobranchus tongashanensis 1-1110020001100000111201100011001---???????
Dermatobranchus albineus 1-11100200011000021111101210110000120001001
Dermatobranchus arminus 1-11100200011000101111101000010001000001000
Dermatobranchus caeruleomaculatus 1-1110020001100000111201&00111001---0001000
Dermatobranchus caesitius 1-11100200011000011112101210000000100001000 D
o
Dermatobranchus cymatilis 1-21100200011000001102001001110001110011000 w
n
Dermatobranchus dendronephthyphagus 1-1110020001100000102201000111001---0011001 lo
a
Dermatobranchus diagonalis 1-21100200011000011112101211110000200001000 de
d
DDeerrmmaattoobbrraanncchhuuss efaasrcleiaitus 11--211111000022000000111100000000201111111&110011201000001000000020110000000111000000 from
Dermatobranchus funiculus 1-21100200011000021112101210010001000001000 h
Dermatobranchus kalyptos 1-11010200011000001111101000010000100000000 ttps
Dermatobranchus kokonas 1-21000200011000021112101210010002120001000 ://a
c
Dermatobranchus leoni 1-1110020001100000111201100011001---0011010 a
d
e
Dermatobranchus microphallus 1-21100200011000021111101210010002200001000 m
Dermatobranchus oculus 1-21100200011000011112101211100000100001000 ic.o
Dermatobranchus phyllodes 1-11100200011000001112000001110001000001010 up
Dermatobranchus piperoides 1-21000200011000021111101210110001120001010 .co
m
Dermatobranchus semilunus 1-21100200011000001112001001110001100001001 /z
Dermatobranchus rodmani 1-21000200011000021111101210010000120001000 oo
Dermatobranchus tuberculatus 1-21010200011000011112101100010000000001001 lin
n
Histiomena marginata 1-0010021001100110111100000111001---00?0000 ea
n
/a
Datacodes:0,generallythepresumedplesiomorphiccondition;1–3,apomorphicconditionsorinsomespecificinstances rtic
le
cited may represent the presumed plesiomorphic state; -, character not applicable; ?, missing data. -a
b
s
tra
c
t/1
FAMILY ARMINIDAE RAFINESQUE 1814 Geographicaldistribution:Thisspeciesisknownfrom 61
GENUS ARMINA RAFINESQUE, 1814 the west coast ofAmerica, from the Gulf ofAlaska to /2/2
Panama. 45
Typespecies:ArminatigrinaRafinesque,1814,bysub- /2
7
sequent designation by Iredale & O’Donoghue (1923). 3
2
0
External morphology: The external morphology 7
4
PREVIOUSLY DESCRIBED SPECIES EXAMINED AND matchesthedescriptionbyCooper(1863).Thatis,the by
body shape is ovate, rounded in front with approxi- g
INCLUDED IN THE PHYLOGENETIC ANALYSIS u
mately 15 elevated, parallel notal ridges. es
ARMINA CALIFORNICA (COOPER, 1863) t o
n
Pleurophyllidia californica Cooper, 1863: 203. 0
6
Armina californica (Cooper, 1863) Marcus, 1961: 41, Buccal armature: The jaws are large and thickly A
p
Armpli.n8a, ficogluurmesb1ia4n7a–15O0’D. onoghue, 1924: 11, pl. 2, cmuutilctuipllaerizreodw,swoifthtraianthgiuclkar,mpaostinictaetdordyenmtaicrlgeisn. Tanhde ril 20
1
radular formula is 38¥58.1.1.1.58. The rachidian 9
figures13–17.Marcus,1961:43,pl.8,figures151–
teetharebroadlytriangularinshape,withfivelarge,
154. Steinberg, 1963; 64
pointed denticles lengthening towards the sixth,
Armina vancouverensis (Bergh, 1876) Steinberg,
central denticle. The first lateral tooth is bicuspid.
1963: 64.
The next 58 teeth are elongate hooks having narrow,
Armina digueti Pruvot-Fol, 1956: 464, figures8–10.
feathery denticles near the tip. The last three to four
Steinberg, 1963: 64.
of these are smaller than the others.
Material examined: CASIZ 171955, one specimen,
50mm, dissected, Gulf of Alaska, 223m depth, col- Reproductive system: As described and drawn by
lected 22.vi.2001 by K. Palenscar. Marcus (1961) for A.columbiana.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
SYSTEMATICS AND PHYLOGENY OF DERMATOBRANCHUS 253
Remarks:Theridgesor‘stripes’thatCooperdescribed Geographicaldistribution:Thisspeciesisknownonly
do not interconnect at regular intervals on our speci- from Sagami Bay, Japan (Baba, 1955) and Panglao,
mens. O’Donoghue (1924) stated that the arrange- Bohol Island, and Cervera Shoal, Philippine Islands
mentofthenotalridgesisadistinguishingfeatureof (present study).
A. californica. He thought that the ridges ‘start at
middle, passing outwards and backwards at an acute
External morphology: The body shape of the living
angle with the mid-dorsal line’. However, the dorsal
animal (Fig.1A) is broad, flattened, and narrows at
ridges of the specimens we examined lie parallel to
the posterior end. The wide foot projects beyond the
the midline and mantle edge. Marcus (1961) thought
distinct mantle margin and has a large ovoid pedal
that, because Bergh in his original description (1890)
glandonitsposteroventralsurfaceinthelargerspeci- D
ofA.californicadidnotmentionobliquedorsalridges, o
men examined. The pedal gland is absent in the w
then this was not a distinguishing feature of this n
smaller specimen. There are up to 22 prominent lon- lo
species. Marcus thought that O’Donoghue actually a
gitudinal dorsal ridges with some additional shorter de
examined specimens of A. columbiana. The specimen d
we examined from the Gulf of Alaska matches the ridgesinbetween,overthesurfaceofthenotum.The fro
blunt oral veil extends forward and is rounded at the m
dexecsecrpitptfoiornosnebynoCtaobolpeedrif(f1e8re6n3c)e.aTnhdeMAlaarsckuasn(s1p9e6c1i-) sides. Behind the oral veil are the closely spaced http
rhinophores. The rhinophores have a series of longi- s
mtheant Mhaasrcnuosnenootfedth.eTh‘cela‘wbr-luikshe’-ltiykpee’ loafterraadlutleaerthteeatrhe tudinal lamellae on the rounded club. The stalk ://aca
widensasitentersthedorsalcavityandthereareno d
present, however. Marcus (1961) thought that the e
lamellae on the stalk. A caruncle is situated just m
specimensexaminedbyBergh(1904)wereactuallyA. ic
posterior to the rhinophores. Marginal sacs are not .o
columbiana O’Donoghue, 1924 because of the pre- u
dominance of brush-like denticles. The presence of vairseib3le6–a5lo6nbgrtahnechmiaanltllaemeedlglae.eUantdtehrethaentmerainotrleenthderoef p.com
bspruecsihe-slikaendor Acl.awco-lliukmebdiaenntaiclsehsouvaldriersemwaitihninasthias thebodyandatleast52–60hyponotallamellaeatthe /zoo
synonym of A. californica. posterior end. The genital opening is situated in the linn
anterior third of the body wall and the anus opening e
a
isapproximatelyhalfwayalongthebody.Theground n
/a
colour of the dorsum and foot is black and the dorsal rtic
ARMINA CORDELLENSIS GOSLINER & BEHRENS, 1996 ridge crests are pale yellow to opaque white. The le
-a
Material examined: Holotype: CASIZ 105717, Cordell mantleedgeisbrightyellow.Therhinophorelamellae bs
Bank, California, collected 20.x.1978, by R. are black and the stalk has black stripes perpendicu- tra
c
Schmeider etal. 23–26 fathoms (fm) depth. lar to the lamellae. The anterior hyponotal lamellae t/1
6
have dark spots and the hyponotal respiratory leaves 1
/2
have dark edges. The ventral surface of the oral veil, /2
4
Geographicaldistribution:Thisspeciesisknownonly the foot sides, and the foot sole has dark mottled 5
/2
from the Cordell Bank, California, USA (Gosliner & blotches and the anterior foot edge is white. 7
3
2
Behrens, 1996). 0
7
4
Buccal armature: The jaws are large and thickly b
y
cuticularized (Fig.2A), with a thick masticatory gu
ARMINA MAGNA BABA, 1955 (FIGS1A, 2, 3) margin and approximately seven rows of pointed es
Armina magna Baba, 1955:22, text figures31, 32, denticles along the entire margin of each jaw t on
0
pl. 11, figures29, 30. (Fig.2B). The radular formula (CASIZ 173357) is 6
A
40¥8.36.1.1.1.36.8 (Fig.2C). The rachidian teeth p
(Fig.2D)arebroadwithalarge,spear-shapedcentral ril 2
0
Material examined: CASIZ 173357, one specimen dis- cusp and four to five flanking denticles on each side. 1
9
sected, 60mm preserved, station (stn) T39, muddy The flanking denticles are all of the same thickness.
sand 100–138m, Cervera Shoal, west of Pamilacan Theinnerlateralteethhaveanarrowbaseandacusp
Island, Bohol, Philippines, collected 6.vii.2004 by T. thatisposteriorlydirected.Thecusphasthreetofour
Gosliner,Y.Camacho,J.Templado,M.Malaquias,M. triangular denticles and two to three smaller second-
Poddubetskaia.CASIZ174127,OT607,onespecimen, ary denticles along its outer side. The next 36 lateral
130mm alive, off San Isidro, Panglao Island Philip- teeth (Fig.2E) are hook-shaped with up to three
pines,9°33.4′N,123°49.6′E–9°33.8′N,123°51.5′E,mud pointed denticles on the under side. The number of
and fine sand, stn T10, 117–124m depth, collected denticles decreases to one denticle on the teeth
15.vi.2004byT.Gosliner,Y.Camacho,J.Templado,M. towards the outer edge of the radula. The outer
Malaquias, M. Poddubetskaia. approximately eight lateral teeth (Fig.2F) are also
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356
254 T. M. GOSLINER and S. J. FAHEY
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/2
/2
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5
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7
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Figure1. Living animals. A, Armina magna Baba, 1955, CASIZ 173357, Panglao, Philippines, photo by Marina
Poddubetskaia. B, Armina paucifoliata Baba, 1955, CASIZ 171415, Panglao, Philippines, photo by T. Gosliner. C,
Dermatobranchus albus (Eliot, 1904), Panglao, Philippines, photo by Marina Poddubetskaia. D, E, Dermatobranchus
albus (Eliot, 1904), CASIZ 174129, Tulear, Madagascar, photos by T. Gosliner. F, Dermatobranchus albus (Eliot, 1904),
CASIZ 068678, Madang, Papua New Guinea, photo by T. Gosliner. G, Dermatobranchus fortunatus (Bergh, 1888), after
Bergh, 1888. H, Dermatobranchus fortunatus (Bergh, 1888), CASIZ 174198, Palmyra Atoll, photo by T. Gosliner.
I, Dermatobranchus fortunatus (Bergh, 1888), CASIZ 074158, Mahe, Seychelles, photo by T. Gosliner.
© 2011 The Linnean Society of London, Zoological Journal of the Linnean Society, 2011, 161, 245–356