Defining a clade by morphological, molecular, and toxinological criteria: distinctive forms related to Conus praecellens A. Adams, 1854 (Gastropoda: Conidae)

2010·12.2 MB·English

by  Jason S Higgs

"
TIIE NAUTILUS 124(1):1-19, 2010 Page 1
Defining a clade by morphological, molecular, and toxinological
criteria: distinctive forms related to Conus praecellens
A. Adams, 1854 (Gastropoda: Conidae)^
Jason S. Higgs* Maren Watkins*
UniversityofGuam Marine Laboratory, UOG Station Patrice Showers Corneli
Mangilao, GU 96923 USA Baldoinero M. Olivera1
and DepartmentofBiology, Universityof Utah
DepartmentofBiology, UniversityofUtah Salt Lake City, UT84112 USA
SaltLakeCity, UT84112 USA
ABSTRACT INTRODUCTION
WecarriedoutadefinitionoftheConuspraecellens A. Adams, The evolutionary histories of biodiverse Conus lineages
1854, species group using a combination of comparative are a challenge to elucidate. In part this is because the
morphological data, molecular phylogeny based on standard genus is so speciose (about 700 species) but also because
genetic markers, andtoxinological markers. Priorto this work. most prior data in the literature is morphological. The
Conuspraecellenswasgenerallypostulatedtobelongtoaclade usual approach is to characterize each species in the
ofsimilarlyhigh-spired, smallerspecies suchas Conuspagoclus lineage based on its shell morphology and to evaluate
Kiener, 1845, Conus memiae (Habe and Kosuge, 1970) and
phylogenetic relationships using additional anatomical
Conus arcuatus Broderip and Sowerby, 1829. The molecular
phylogenyandtoxinologicaldatademonstratethattheseearlier data, when available.
hypothesesareincorrect, andthatinstead. Conuspraecellens is Prior attempts to divide Conus into subgeneric groups
in a branch of Conus that includes Conus stupa (Kuroda, have been based largely on shell morphology. In this
1956), Conus stupella (Kuroda, 1956), Conus acutangulus work, we focus on one particular branch of Conus that
Lamarck, 1810, and surprisingly, some species that are mor- includes the species known as Conus praecellens. Sev-
phologically strikingly different. Conus mitratus Sowerby, eral previous attempts to determine which species are
1870, and Conus cylindraceus Broderip and Sowerby, 1830. most closely related to Conus praecellens have grouped
A more careful analysis of the morphologically diverse forms C. praecellens with other high-spired forms (Figure 1)
amsatseirginaeldatlooCneo,ntuhserpreaaerceelaltelnesasstugtghersetesatdhdaittifornoamlstpheeciPehsilnieppwinteo stpheactiafriec cporliloerctheydpointhdeeseepsotfhfasthohraevleocbateieonns.prSoopmoeseodftahree
science. Conus andremenezi. Conus miniexcelstis, and Conus
rizali. A reevaluation ofprotoconeh/earlyteleoconcii morphol- summarized in Table 1.
ogy also strongly suggests that Conus excelsus Sowerby III, In the most comprehensive modem treatise on Indo-
1908, is related to these species. Together, the different data Paeifie Conus species (Rockel et ah, 1995), Conus
suggest a clade including the 10 species above that we desig- praecellens is regarded as most closely related to Conus
natetheTurriconus (ShikamaandHabe, 1968)clade;thereare acutangulus. In most of the schemes shown in Table 1
additional distinctive formswithin the cladethat maybe sepa- (Marsh and Rippingale, 1964; Okutani, 2000), Conus
rableatthespecies level. Thephylogeneticdefinitionusingthe praecellens is grouped together with Conus acutangulus
multidisciplinaryapproach described hereinprovides a frame- inthesubgenus Conasprella Thiele, 1929. The designated
wanoirmkalfso,rscuocmhprasehtehnesciovneelysnianilvse.stigating biodiverse lineages of type of Conasprella is “C. cancellatus (= C. pagodus).
Another species generally thought to belong to this
Additional keywords: Neogastropoda, Turriconus, 12SrRNA subgenus is the Eastern Pacific Conus arcuatus. In one
sequences,phylogeneticanalysis, exogenes ofthe proposals (da Motta, 1991), Conus praecellens and
Conus acutangulus are in two different subgeneric
groups: Conus praecellens in Conasprella and Conus
acutangulus in Kerniasprella Powell, 1958 (which this
author regards as a subgenus of the genus Profuncliconus
Kuroda, 1956). Among the species included with Conus
Support for this work was provided by grants from the
NII4GMS POl GM048677 (to BMO) andthe NIHGMS Diver- acutangulus in Kerniasprella are forms such as Conus
sitySupplement Fellowship3POl GM048677-13S1 (to JSB) memiae and Conus nereis (Petuch, 1979), the latter
; To whom correspondence should be addressed: olivera@ regarded by Rockel et ah, 1995 as a form of Conus
biology,utah.edu wakayamaensis (Kuroda, 1956). Thus, the high-spired
,
Page 2 THE NAUTILUS, Vol. 124, No. 1
Figure 1. High-spired Conus species previouslypostulatedto be related to Conuspraecellens-. Top from left: Conusacutangulus,
“typical form”; Conus acutangulus “deep-water form”; Conus nereis. Middle from left: Conus praecellens, “Aliguay form”; Conus
praecellens, “sowerbii form”; Conus andremenezi new species (Holotype, MSI); Conus pagodus. Bottom from left: Conus
miniexcelsus, new species (Holotype, deposited at MSI); Conus rizali new species (Paratype 2, MSI); Conus arcuatus. All ofthe
specimens shown are from the Philippines, except lorConusarcuatus. MeasurementsprovidedinAppendix 1.
. .
S. Biggs et al., 2010 Page 3
J.
Table 1. Previous taxonomic assignments ofConus praecel- MATERIALS AND METHODS
lens and Conus acutangulus.
Specimen Collection. Most forms in the Conus
Marshand praecellens complex are collected offshore from 30-250
Rippingale (1964): DaMotta(1991): Okutani (2000): meters in depth. The bulk of Philippine specimens
Conasprella Conasprella Conasprella in collections assigned to this species were collected
praecellens praecellens praecellens (together with such species as Tibia fusus (Linnaeus,
pagodas pagodus pagoda 1758) andXenoplioraSolaris (Kosuge and Nomoto, 1072)
arcuatus arcuatus gracatapi around 1960, primarily from a few classical fish trawler
acutangulus acutangulus localities (Maqueda Bay in Samar Is, Tayabas Bay in
wakayamaensis Luzon); atthetime, thesewere mostlyidentifiedas Conus
Kennasprella Endemnoconus sowerbii (see Reeve, 1849; Springsteen and Loebrera,
acutangulus memiae 1986). Because other forms in the praecellens complex
memiae wakayamaensis
are mostly from even deeper water, these were less well
wakayamaensis tone
represented in collections; most specimens available in
nereis
museums are poorly preserved and/or dead-collected.
jaspideus
However, the combination of gill net and hookah collec-
tions in the Cebu/Bohol area ofthe Central Philippines
Conus species including Conus praecellens were either and intensive small trawl collections around the Island
all grouped together in Conasprella, or were divided of Aliguay has increased accessibility to several forms in
into a praecellens/pagodus group (Conasprella) and an the Conuspraecellens complex. Some of these are smaller
acutangulus/memiae group (Kennasprella) specimens that were sparsely represented in earlier col-
These shell morphology-based suggestions can he lections. A range of live-collected specimens with pre-
independently evaluated using molecular data. If only served protoconchs has become available, which has
morphological analyses are used, the resulting systemat- facilitated the reevaluation of the Conus praecellens spe-
ics may not reflect evolutionary trends as the traits may cies complex.
be subjectto selection forces thatdo not reflectcommon
descent. Distinguishing similarity by descent (reflecting Phylogenetic Analysis. We aligned sequences using
the phylogeny) from similarity directed by selection Clustal X (Larkin et ah, 2007) and refined by eye using
(convergence or parallelism) is problematic without MaeClade (Maddison and Maddison, 2005). The tree
independent data corroborating the morphological evi- was inferred using MrBayes (Huelsenbeck et ah, 2001;
dence. Hence a widespread attempt to define biodiver- Ronquist and Huelsenbeck, 2003). The run comprised
sity using molecular markers, notably a segment of the 1,000,000 generations with the first 25% oftMheCsMamCpMleCd
COI gene, has led to the “barcode initiative”. Although generations discarded as burn-in trees. Two
thisinitiativehasbeenwidelyimplemented,workerswho runs (metropolis-coupled Monte-Carlo nrarkov-chain),
needtoidentifyfield specimens require amore seamless using four chains each, were used to thoroughly explore
integrationofthe molecularwith themorphologicaldata. tree space. Convergence of the likelihoods was deter-
Our first goal is to define a phylogenetic tree with mined by comparing the average standard error of the
clades that reflect the branching pattern and in turn the difference (ASED) in split frequencies between the two
evolutionary history of the species. Molecular data pro- runs and by comparing plots of the log-likelihood after
vide independent evidence for such a phylogeny and a the burnin to the end of the runs. Optimality was also
useful organizational framework for in-depth studies of judged adequate when tire PSRL (Potential scale reduc-
species-rich groups. The morphological traits mapped tion factor) for the total tree length and for each model
onto such a tree distinguish the respective roles of com- parameterreached 1.00.
mon descent and selection in the evolutionary process.
In this work, we focus on the definition ofthe putative Identification and Sequencing of Genomic Clones
clade that includes Conus praecellens. Using 12SrRNA Encoding O-Superfamily Peptides. Genomic DNA
sequences, we specifically evaluate which Conus species was prepared from 50 mg each oftissues ofConus acu-
are most closely related to Conus praecellens In addition tangulus Conus mitratus, Conus pracellens, and Conus
, PUREGENE DNA
tousingamolecularphylogenytoassess morphology-based stupa using the Centra Isolation Kit
taxonomy, we have gathered moleculardatain the form of Kit (Gentra Systems, Minneapolis, MN) according to the
the genes thatencode toxins expressed in thevenom ducts manufacturers standard protocol. These gendmie DNAs
of cone snails. As will be shown, these highly specialized were used as templates for polymerase chain reaction
“exogenes” (Olivera, 2006) are useful in defining discrete (PCR) with oligonucleotides corresponding to conserved
branches of a large biodiverse lineage such as the cone 5' intron and 3' UTR sequences of omega and delta
snails. This three-pronged approach defines a more com- prepropeptides. The resulting PCR products were puri-
pletepictureoftheevolutionaryhistoryof thesebiodiverse fied using the High Pure PCR Product Purification Kit
cone snails with the result that previous morphologically (Roche Diagnostics, Indianapolis, Indiana) following the
informedhypothesesmaybe moreobjectivelyassessed. manufacturers suggestedprotocol.
Page 4 TIIE NAUTILUS, Vol. 124, No. 1
The eluted DNA fragments were annealed to vania (ANSP 421619); the Museum national d’Histoire
pNEB206Avectorandtheresultingproductstransformed naturelle, Paris, France (MNHN 21131); the Field
into competent DH5a cells, using the USER Friendly MuseumofChicago, Chicago (FMHN 312461);the Har-
Cloning Kit (New England BioLabs, Beverly, Massachu- vard Museum ofComparative Zoology, Cambridge Mass
setts) following manufacturers suggested protocol. The (MCZ 361611); Zoological Museum of Moscow State
nucleic acid sequences of the resulting omega and delta University, Aloscow, Russia (Lc-37964) and The Bailey-
toxin-encoding clones were determined according to the Matthews Museum, Sanibel, Florida (BMSM 38672)
standardprotocol forautomatedsequencing. (see Appendix or a complete listingol paratypes).
Morphometric Analysis. Using dial calipers, we mea- Type Locality: The type locality for Conns anclremenezi
sured maximum diameter (mm) and total length (mm; is Aliguay Island, Philippines, where most specimens
including spire height) ofspecies within the praecellens in thetvpe series havebeen collectedbycommercial fish-
complex. Relative diameterwas calculated as the ratio of ermenusingsmalltrawlsatdepthsaround 150m.Another
maximum diameter to total length. All species were established locality is off Panglao, Bohol, from Balicasag
represented by multiple samples. In view of the low Island to Momo Beach where the species has been col-
between-sample variation, we calculated a single mean lectedbytangle nets indeeperwater (~200-300m).
relative diameter foreach species.
Geographical Distribution: From the Central to
RESULTS Northern Philippines, probablytoViet Namandpossibly
much furtherWest (see discussion below). In the recent
Systematic Descriptions ofThree New Species book of Thaeh (2005), the specimen figured as Conus
of Conus praecellens (Plate 61, Fig. 34) is likely to be a specimen
by Baldomero M. OliveraandJason Biggs ofConus anclremenezi.
SuperfamilyConoidea Fleming, 1822 Etymology: This species honors the memory ofAndre
FamilyConidae Fleming, 1822 Menez, one ofthe giants ofthe field oftoxinology.
SubfamilyConinae Rafiuesque, 1815
Genus Conus Linnaeus, 1758 Remarks: The sculpture on die spirewhorls is diagnostic:
the spiral ribbons on the larger spire whorls are raised,
Conus anclremenezi Olivera and Biggs, newspecies. relativelynarrowto very narrow, and always far apart. The
(Figures 1, 2, 6) vide spacing on the spire whorls between narrow raised
spiralribsis adiagnostictraitofthisspecies; in mostsimilar
Description: Biconicalin shape, maturespecimens from forms,thespiralribbonsorridgesare muchclosertogether
25-53mm. Moderately solid, and with a relatively high andaremorelikeflattenedribbons,broadandshallow.The
spire, and generally broader than most related forms broad shape, purplish-brown spots, undulating spiral ribs,
(D/L 0.47). Last whorl is broadly conical, with raised and widely spaced ribs on the spire are characteristic
spiral ribs that are notsmooth but always undulating (and features tiiatseparatethe species fromsimilarforms.
in some specimens, the ribs seem to have arch-like pro- When the protoconch is decollated, this species is
tuberances, instead of a continuous smooth rib). Raised difficultto separate from some closelyrelated forms that
ribsonthebodywhorlarewellseparatedfromeachother, are potentiallyvariants of Conus praecellens. Most spec-
with interstices thathaveaxial scalesbetween them. imens can generally be differentiated by the distinctive
The body whorl has an off-white ground color with purple-brown color, the broader shell, the widelyspaced
characteristic purplish-brown spots that occur in zones; spiral ribbons on the spire whorls, and when preserved,
in the two darker zones, the spots generally cover more the conical protoconch. Most specimens in the type
spiral ribs and extend into the interspaces (although series come from Aliguay.
there is considerablevariation). Theprotoconchis decol- There is a group ofPhilippine specimens, not from the
lated in most specimens, but when preserved it is a type locality, which we tentatively assign to this species.
rounded conical shape, translucent, veiy light yellowish These were collected by the Musorstom expeditions
brown or off-white; the protoconch is followed by two prmoted by the Museum national d’Histoire naturelle,
white early teleoconch whorls that are lightly nodulose Paris, to Lubang Island/Mindoro. Several large mature
and angled at the periphery. The spots begin to appear specimensol Conusanclremenezi alldeadcollected,were
,
on theperipheryofthe third orfourth teleoconchwhorl, examined. All ofthese were collected at depths between
andtypicallythese are more closelyspacedto each other 160-198 meters; at more shallow collection stations, this
than are the largerspots in the later spire whorls. formwas absentandanarrowerConuspraecellensvariety
waspresent.Thisprovidesamoreaccurateestimateofthe
Type Material: The Holotype is deposited in the depth atwhich this species occurs.
Marine Science Institute (MSI) at the University ofthe Finally, there is a small specimen figured by Rockel
Philippines; Paratypes are deposited at the Academy of et al. (Plate 54, Fig. 14) that appears to be ajuvenile of
Natural Sciences ol Philadelphia, Philadelphia, Pennsyl- Conus anclremenezi: ifthe identity of this specimen can
S. Biggs et al., 2010 Page 5
J.
Figure 2. Two morphospecieswith non-“praecellens-\i\ce"protoconchs fromAliguay. Allol the specimens shownare from Aliguay
Island, Philippines, exceptthe lowerleftspecimenwhich was collectedfrom southern Japan. Top row: Conus andremenezi- Bottom
row: Conus miniexcelsus. For Conus andremenezi the Holotype (left), Paratype 7 (second from right), and Paratype 11 (right) are
,
shown. For Conus miniexcelsus the Holotype (second from right), Paratype 2 (third from right), and Paratype 18 (rightmost
,
specimen) are shown. All ofthe types figured are deposited at the Marine Science Institute (MSI), University of the Philippines.
MeasurementsprovidedinAppendix 1.
beverified, itextends the range ofthis species across the Conus miniexcelsus Olivera and Biggs, new species
entire Indian Ocean since the specimen is reportedtobe (Figures 1, 2, 4, 6 and S)
from Somalia. Thus, although almost all of specimens —
examined were from the Central Philippines, there is Conus praecellens f. subaequalis. Robin, 2008: 424,
strong evidence for the occurrence ofthe species in the fig. 14 (non Conus subaequalis, Sowerby III, 1870)
Northern Philippines, andthepossibilitythatit mayhave
a geographic distribution that is much wider is raised by Description: A moderately small shell; adult size range,
the Somali specimen in the Raybaudi-Massila collection. 25-37 mm. High-spired, with both spire and bodywhorl
Page 6 THE NAUTILUS, Vol. 124, No. 1
having a straight outline, making the shell narrowly and early teleoconch morphology between the two spe-
biconical. The larval shellhas3.0-3.5whorls, translucent cies areconsistentdistinguishingcharacters. This feature
brownishorpurplish. There are9-11 teleoconchwhorls, puts Conus miniexcelsus in the same group as Conus
the firstthreebeingivory-white,withoutspots, providing acutangulus, Conus andremenezi, and Conus excelsus
anotablecontrasttothetranslucent-coloredprotoconch. (except that the spire of Conus acutangulus has strong
At around the fourth teleoconch whorl, broad brown- tubercules at the sutures). Conus andremenezi is gener-
ish spots appear, centered around the periphery. The ally larger, with coarse spots that are purplish brown in
ground color is white, with chestnut-brown spots. On colorinsteadofchestnut. Conus miniexcelsus isprobably
the body whorl there are a series of flat spiral ribbons. most similar to Conus excelsus, although there is a strik-
The shell pattern on the bodywhorl can be divided into ingdifference in size atmaturity. Thetwo Japanese spec-
3-5 zones. The most posterior, next to the suture, are a imens examined are more solid and chunky than the
series ofabout 6 spiral ribbons with extremely fine chest- Aliguay material. Figure 8 shows the different shape and
nut brown spots. These are followed by a zone with 3 color ofthe protoconehs and the characteristic switch in
noticeablybroader spiralribbons that have deeperbrown Conus miniexcelsus from a conical translucent purplish
and larger spots. In most specimens, this is followed by brown protoconch, to the ivory white first teleoconch
three spiral ribbons that have a finer spottedpattern (but whorls, and finallyto the normal spottedpattern.
notas fine as in the spiral ribbons in the firstzone, closest
to the suture). The remainder ofthe shell towards the tip Conus rizali Olivera and Biggs, newspecies.
is covered by spiral ribbons that are darker in color and (Figures 1, 3, 6)
more heavily spotted; typically the first 3 to 4 are darker
than those towards the anteriorend ofthe shell, although Description: The species is medium-sized; specimens
mm
there is considerable variation in this regard. In some examined are 26-39 in length. The shell is biconic,
specimens, the light zone continues to the anterior of with an unusuallytall, straight, and sharply pointed spire
the shell. and a straight-sided body whorl, sharply angled at the
shoulder. Outline narrow (D/L = 0.397 ± 0.011); The
Type Material: The Holotype is deposited at the larval shell has two whorls, and is praecellens-like but
Marine Science Institute at the University ofthe Philip- somewhatproportionallybroaderthanformostspecimens
pines, Paratypes are deposited at the Field Museum, of Conus praecellens; this is followed by two teleoconch
Chicago, Illinois (FMNII 312462); the Museum National whorls that have a characteristic white-matte surface,
d’Histoire Naturelle, Paris, France (MNPIN 21132); the somewhat crinkly; starting with the fourth teleoconch
Harvard Museum of Comparative Zoology, Cambridge, whorl,there are 8-9 spottedspirewhorls.
Massachusetts (MCZ 361609); the Academy of Natural The body whorl is characterized by shallow spiral
Sciences of Philadelphia, Philadelphia Pennsylvania ribbons with only a narrow interstitial space between
(ANSP 421620); Zoological Museum of Moscow State them; these are broadly spotted in light yellow-brown.
University, Moscow, Russia (Le-37965) and The Bailey- Characteristically, immediately below the periphery, the
Matthews Museum, Sanibel, Florida (BMSM 38673) first spiral ribbon lacks spots, leaving a white zone. Al-
(see Appendixoracomplete listingofparatypes). though there is some variation, the spots are much ligh-
ter in color than in related forms (Paratype 2 almost
Type Locality: Aliguay Island, Philippines. Most spec- completely lacks spots in the bodywhorl).
imens in the type series were collected by the commer-
cial small-trawl operations offAliguay Island, at depths Type Material: The Holotype is deposited at the
of30-150m. Marine Science Institute at the University ofthe Philip-
pines; Paratypes are deposited at the Academy ofNatu-
Geographical Distribution: Presently known from the
ral Sciences ofPhiladelphia, Philadelphia, Pennsylvania
Central Philippines toWakayama, Japan (Paratype#23). (ANSP 421621); the Harvard Museum of Comparative
Etymology: The specific epithetemphasizes some strik- Zoology, Cambridge, Massachusetts (MCZ 361610) and
ingandunexpectedsimilarities to Conusexcelsus despite in the Museum National d’Histoire Naturelle, Paris
France (MNIIN 21133) (see Appendix for a complete
the considerable disparityin size.
listingofparatypes).
Remarks: A distinguishing characteristic ofthis species
are the spots on the whorls closest to the suture, which Type Locality: All type specimens were obtained from
are generally extremely line in pattern and greater in commercial dealers in the Philippines, and the exact
number than for any other similar species, followed collection locality of the types could not be verified.
by the thicker, darker brown spiral ribbons at the Springsteen and Leobrara show a figure ofConus rizali
center of the body whorl. These features are clearly (labeled Conus subaequalis) indicating Punta Lugano,
illustrated in the specimens shown in Figure 3. Conus Cebu, suggesting that these were probably collected by
miniexcelsus is a distinct species, most easily confused fishermen usingtangle nets at depths of100-200m.
with Conus praecellens. However, as discussed above
and shown in Figure 3, the differences in protoconch Geographical Distribution: Philippines.
S. Biggs et al., 2010 Page 7
J.
Figure 3. Three distinctive forms with “praecellens-like” protoconchs. Top row is a series of Conus praecellens, "sowerbii form .
Bottom rowis Conus praecellens, “Aliguay form”. In the middle row are two specimens of Conus rizali new species, the Holotype
(left) and Paratype2 (right),both MSI. Measurementsprovided in Appendix 1.
Etymology: This species is named in honor of |ose assigned to Conus praecellens. The narrower outline,
Rizal, the National Hero of the Philippines. Dr. Rizal, the shallow ribbons on the body whorl, and differences
who was executed by the Spanish Colonial Administra- in protoconch/early teleoconch moiphology separate
tion in 1898, collected shells as ahobby. Conus rizali from other related forms. Conus rizali was
previously figured as Conus suhaequalis Sowerby III,
Discussion: Ofall ofthe similar forms. Conus rizali has 1870, by authors. This name was used by Springsteen
the most narrow outline (D/L = 0.397 ± 0.011); spec- and Leobrera, and by Lim and Wee (1992); however,
imens of Conus praecellens from Aliguay, which the specimen recently figured by Robin (2008) as Conus
are generally narrower than the “Sowerbii form” have a subaequalis is not Conus rizali but Conus minexcelsus.
D/L = 0.44, and for Conus miniexcelsus (D/L = 0.416) A specimen was also figured by Roekel et al. (Plate 54,
;
these are both narrower than Conus andremenezi. Figure 6) but theyreferthis to Conuspraecellens. Conus
Although Roekel et ah, put this species in synonymy rizali is sufficiently distinct so that it can immediatelybe
with Conus praecellens we believe that it is a distinctive picked out from otherrelated forms discussed elsewhere
,
form that can readily be separated from specimens in this article: the narrow outline of the shell sets it
0
PagOe 8 THE NAUTILUS, Vol. 124, No. 1
immediately apart, and in fact the form that is most spiral ridges that undulate, with a wade space between
similar in outline is Conus gratacapi from Japan, which ribbons with axial scales between the spiral ridges. More
is an unrelated species. This species has onlybeen inter- consistently, the sculpture on the spiral whorls has nar-
mittently collected over the last four decades, and never row, raised ridges, widely spaced from each other. This
in large numbers. As has been discussed in detail by suite of characteristics consistently distinguishes this
Rockel et al., and is shown in the original figure of species from C. praecellens ofsimilar size (see Figure 1)
Sowerby (which Rockel et al., reproduced), the spec- and from Conus miniexcelsus (see next species); Conus
imens that we assign to Conus rizali are clearly not con- rizali is even more distinctive from C. andremenezi.
specific with the figure of Conus subaequalis which There are a group of small Conus praecellens that are
,
likely refers to a different form in the Conus praecellens most easily confusedwith Conus andremenezi; these are
complex. discussed under Conus praecellens below.
Conus miniexcelsus Olivera and Biggs, newspecies
(Figure 2)
Morphological Definition of Species inthe Conus
PRAECELLENS COMPLEX: TWO“a/FVIEXCELSCS-LIKE” FORMS This very distinctive species is characterized by its rela-
tively narrow shell outline (D/L ~ 0.42 vs. 0.47 for C.
In this section, we describe and define two distinc- andremenezi), the multispiral protoconch of 2.5-3.
tive forms in the Conus praecellens complex from the whorls, which is translucent and distinctly brownish or
Philippines. As wall be defined in the Discussion, the purplish and contrasts in its color with the first 2.0-2.5
“Conus praecellens complex” can be divided into two teleoeoneh whorls that are ivory white. In most spec-
broad groups on the basis of protoconch morphology, imens, these white whorls are smooth or have, at most,
the “praecellens-like” forms and the “miniexcelsus-like” nearly obsolete tubercles. This is followed by 6-10 spot-
forms. ted teleoeoneh whorls that are grooved and have strong
The two miniexcelsus-like forms from Aliguay Island axial structure so that the upper part of each spire
(i.e., thosewith non-praecellens-likeprotoconchs),which whorl has a distinctly tiled appearance. The bodywhorl
we proposed to designate as new species, are discussed lias shallow spiral ribbons with regular, brown spots
first. The Aliguay specimens of these two forms are that have a characteristic pattern described in the
easily distinguishable from each other (see Figure 4). Appendix in detail. The colored, translucent protoconch
Since both ofthese miniexcelsus-like forms were appar- contrasting in color with the first two shiny-white
ently unnamed, these are formally described in the sec- teleoeoneh whorls, combined with the slender shape
tion above. The appendixsummarizestheindividual type and the very fine spotted pattern are diagnostic of this
specimens onwhich the newtaxaare based. distinctive species. There is considerable variation in
how dark the spots are; a range ofvariations is shown in
Conus andremenezi Olivera and Biggs, new species Figure 4. A full description ofthis new species was pro-
(Figure 2) vided in the previous section; detailed measurements
ofall the types are provided in the appendix. Almost all
This form may be similar or identical to Conus bicolor specimens havebeencollectedbysmalltrawls in Aliguay
Sowerby I, 1833,which is apreoccupied name. Sowerby from 60-130 m, but occasional specimens have also
then provided a new name in 1841, Conus sinensis. been collected using gill nets off Balicasag Island. One
Rockel et al., (1995) stated that “taxonomic status of specimen assigned to this species from southern Japan
Conus bicolor/ Conus sinensis (Sowerby II, 1841) is included in the type series (Figure 4). Figure 2
remains disputable because the type specimen is lost makes evident the generally finer pattern and narrower
and the type figure (Plate 54, fig. 3) does not match C. shell shape of Conus miniexcelsus compared to Conus
praecellens in a satisfying way: the pictured shell has a andremenezi. In addition the spiral ribbons of the body
comparatively low spire. . .is somewhat bulbous below whorl of Conus miniexcelsus are smooth, but are dis-
the shoulder and its colorpattern consists ofbrown axial tinctlycrenulated in Conus andremenezi.
flames. .we favor synonomy with Conus praecellens.'
.
The figure shown by Rockel et al. (originallydrawn from
“Conus bicolor”) is similar to the species we describe Overviewand Description ofthe
above as C. andremenezi;we have notadoptedthe name “PRAECELLENS-LIKE FORMS”
Conus sowerbii for this species because the syntype in
the British Museum does not appear to be nonspecific Conus praecellens remains a confusing taxon, and the
with C. andremenezi. scheme proposed below is not entirely satisfactory; mul-
We believe that Conus andremenezi is clearly dis- tiple forms have been assigned to this species byvarious
tinguishable from typical Philippine specimens of workers. Even after the two “miniexcelsus-like forms”
C. praecellens; first, the protoconch is not “praecellens- are separated as new species, what remains still com-
like”; second, this form is generally broader and has a prises a confusing set of specimens, most of which we
We
characteristic purplish-brown coloration. Furthermore, are provisionally retaining in C. praecellens. believe
on the body whorl, there are raised but not flattened that the retention ofdiverse forms within C. praecellens
S. Biggs et al., 2010 Page 9
J.
Figure 4. An illustrationofthe "miniexcelsus-hke complex”. Shown are five specimens (left five) andclose-ups oftheirrespective
protoconchs (right five). Left, top and bottom: Conus miniexcelsus (Paratypes 2 and 18, respectively), middle: Conus excelsus, and
righttopandbottom: Conusacutangulus. MeasurementsprovidedinAppendix 1.
will prove to be only an interim solution, and new mor- is describedabove as Conussubaequalis. The three forms
phologically similar species will be identified once a are shown in Figure 5.
more extensive molecular and morphological analysis
Conus praecellens “Aliguay form”
has been carried out over a wider suite of specimens
from a greatergeographic range. (Figure 3)
There is a widely illustrated specimen designated as The series ofspecimens thatwe assign to C. praecellens,
“apossible syntype”ofConuspraecellens from the British “Aliguay form”, appears to be the closest to the type in
Museum. This is atypical ol specimens assigned to the BMNH in shell pattern; these have mostly been
C. praecellens from the Philippines. This possible syntype collected in 30-80 fathoms off Aliguay Island, between
from the China Sea is lighter in color and finer in sculp- Mindanao and Bohol in the Philippines. The Philippine
BMNH
ture on the body whorl than either of the two major specimens are smaller than the “syntype” (aver-
Philippine varieties thatweinclude in C. praecellens. The age size ~ 24mm);keyfeatures thatdistinguishthis form
first group, “the Aliguay form,” which is small and light are a blunt, paucispiral protoconch of two whorls, the
colored, has been extensively collected both by the small relatively smaller size, and the chestnut color of the
dredge operations in AliguayIsland, andis the form illus- spots. Details ofthe spire sculpture and bodywhorl that
trated in Figure 3. A second morevariable group thatwe are also diagnostic are delineated below.
refer to as the “sowerbii forms,” include larger specimens The shells of this form (see Figure 5) typically have
that vary considerably in shell pattern, shape, and size. 2.0-2.5protoconchwhorls, thefirstbeingquite spherical
Thesecomprise mostspecimens collectedbyfish trawlers and inflated, and the second narrower and more elon-
intheperiodfrom 1955-1965,particularlyfrom twolocal- gate. The first two teleoconeh whorls are typically
ities, Tayabas Bayand Maqueda Bay. Athirdgroup is that white andflattened compared to the protoconch whorls,
referred to by previous authors as Conus subaequalis and and they are knobbed on the periphery, while the two
Page 10 THE NAUTILUS, Vol. 124, No. 1
acutangulus-< TurriconusW?
Rhizoconus W
brunneus
eg,us StephanoconusVZ
Dauciconus W
vittatus
IldVebCeilb
gr.?r)um —egt|itacenunssuiL.sterpioartuisconusW
W
Viitulinus
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Conasprella W
B.tippetti
Figure 5. Phylogenetic tree ofsome Conus species based on 12SrRNA sequences. Species shown in Figure 1 are indicatedwith
arrows. Branches are labeledwith Bayesianconfidencevalues (posteriorprobabilities expressed as percentages). These data clearly
separateConusacutangulus and Conuspraecellens from the Conasprella specieswith 100% confidenceandjointhemwith C. stupa
and C. mitratuswith97% confidence.
protoconch whorls are smooth. There are 8 to 9 whorls pearly white protoconch whorls. A range of specimens
spottedwith achestnut brown color, with the firstone or collectedfromvarious Philippinelocalities, allwithtypical
two spotted whorl(s) also knobbed. The earlyteleoconch “praecellens-like” protoconchs that are well preserved are
whorls are characterized by a deep spiral groove on the shown in Figure 5 (the contrast between these and the
upper section ol the whorl; these spiral grooves gradually “Aliguayform” is alsoillustratedinthat figure).
increase in number as the whorls get larger; these are Given the distinctive (and mutually similar)
narrowfurrowsthatcanirebisectedbyaxialsculpturethat protoconchsofboththe Aliguayandthe “sowerbiiforms,”
varies considerably in strength; in specimens where the we have provisionally assigned these in C. praecellens.
axial sculpture is strong, the area immediatelyadjacent to However, furthercharacterization ofboth the radularand
thesuturelooksasilitweretiled, sincethecombinationof gut morphology, as well as a molecular characterization,
the spiral grooves and the axial sculpture divide the area mayprovethatthesearedistinctfromeachother, andthat
between grooves intosquaresections. Thebroaderpartof there are additional separable species embedded in the
the spiral whorl is smooth to the periphery; the lower “sowerbii forms”, a possibility that clearly needs to be
sutureisbelowthe sharplyangledperiphery. furtherevaluated.
Conus praecellens “sowerbii forms” Conuspraecellens other distinctive varieties.
,
(Figure 3) A smaller form of Contis praecellens was recently col-
There are forms in the C. praecellens complex most com- lectedbyMNHN,offAurora, EasternLuzon, Philippines.
monly found in collections; most specimens were col- These specimens were notable because they were veiy
lected by trawlers around I960 in great numbers in the similar to Conus andremenezi, but much smaller. They
Maqueda and Carigara bays of Samar Island, and in are easily separable from Conus andremenezi because
Tayabas Bay of Southwestern Luzon, from Jolo Island in they have the typical “praecellens-type” protoconch.
the Sulu Sea. The “sowerbii forms” are larger and more These lookveiydifferent from the two Conuspraecellens
denselyspotted than the specimens ofthe “Aliguay form" “forms” described above. We note that in general. Conus
described above. There is considerable variation in shell andremenezi is a larger species; however, there have
morphology: somespecimensareslenderandnarrowwith been juvenile Conus andremenezi specimens collected
line sculpture; others appear to be much broader at the using lumum-lumum nets in the Camotes Sea, along
shoulders with an overall coarser sculpture. However, with specimens of the Conus praecellens “Aliguay form,"
,
when preserved, the protoconchs of all of these have described above. It seems likely that only juvenile spec-
the typical highly inflated first whorl, with only two. imens of Conus andremenezi are collected at this