THE NAUTILUS
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Volume 124, Number 1 April 6, 2010 ISSN 0028-1344
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THE0NAUTILUS
CONTENTS
Volume 124, Number 1 April 6, 2010 ISSN 0028-1344
Jason S. Higgs Maren Watkins Patrice Showers Corneli Baldomero M. Olivera
Defining a clade by morphological, molecular, and toxinological criteria:
distinctive forms related to Conus praecellens A. Adams, 1854
(Gastropoda: Conidae) 1
Somsak Panha An anatomical note on Moellendorffia eastlakeuna (Mollendorff, 1882)
Chirasak Sutcharit a camaenid land snail from Vietnam (Gastropoda: Pulmonata:
Dang Ngoc Can Camaenidae) 20
Kristiina Ovaska Terrestrial gastropods from Haida Gwaii (Queen Charlotte Islands),
Lyle Chichester British Columbia, Canada, including description of a new northern
Lennart Sopuck endemic slug (Gastropoda: Stylommatophora: Arionidae) 25
Cleo Dihiei de Castro Oliveira How the number of hinge teeth may induce errors in the taxonomy of Tatiana Huguenin Morales Nuculidae and Nuculanidae (Bivalvia) 34
Richard E. Petit A new species of Z eadmete (Gastropoda: Cancellariidae) from
Lyle D. Campbell South Carolina, a genus previously unknown in the Atlantic Ocean 41
Sarah C. Campbell
Monica A. Fernandez Current distribution of the exotic freshwater snail Helisoma dtiri/i
Silvana C. Thiengo (Gastropoda: Planorbidae) in Brazil 44
Fernando S. M. Bezerra Lucia M. S. Alencar
Free Espinosa
Georgina A. Rivera-Ingraham Jose C. Garcia-Gomez
Early stages of development in the endangered limpet Patella fermginea Gmelin, 1791 (Gastropoda: Patellidae) 51
Notice
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Sponsored in part by the State of Florida, Department of State, Division of Cultural Affairs, the Florida Arts Council and the National Endowment for the Arts.
NATIONAL ENDOWMENT FOR THE ARTS
TIIE NAUTILUS 124(1):1-19, 2010
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Defining a clade by morphological, molecular, and toxinological criteria: distinctive forms related to Conus praecellens A. Adams, 1854 (Gastropoda: Conidae)^
Jason S. Higgs*
University of Guam Marine Laboratory, UOG Station
Mangilao, GU 96923 USA
and
Department of Biology, University of Utah Salt Lake City, UT 84112 USA
Maren Watkins*
Patrice Showers Corneli Baldoinero M. Olivera1
Department of Biology, University of Utah Salt Lake City, UT 84112 USA
ABSTRACT
We carried out a definition of the Conus praecellens A. Adams, 1854, species group using a combination of comparative morphological data, molecular phylogeny based on standard genetic markers, and toxinological markers. Prior to this work. Conus praecellens was generally postulated to belong to a clade of similarly high-spired, smaller species such as Conus pagoclus Kiener, 1845, Conus memiae (Habe and Kosuge, 1970) and Conus arcuatus Broderip and Sowerby, 1829. The molecular phylogeny and toxinological data demonstrate that these earlier hypotheses are incorrect, and that instead. Conus praecellens is in a branch of Conus that includes Conus stupa (Kuroda, 1956), Conus stupella (Kuroda, 1956), Conus acutangulus Lamarck, 1810, and surprisingly, some species that are mor- phologically strikingly different. Conus mitratus Sowerby, 1870, and Conus cylindraceus Broderip and Sowerby, 1830. A more careful analysis of the morphologically diverse forms assigned to Conus praecellens suggests that from the Philippine material alone, there are at least three additional species new to science. Conus andremenezi. Conus miniexcelstis, and Conus rizali. A reevaluation of protoconeh/early teleoconcii morphol- ogy also strongly suggests that Conus excelsus Sowerby III, 1908, is related to these species. Together, the different data suggest a clade including the 10 species above that we desig- nate the Turriconus (Shikama and Habe, 1968) clade; there are additional distinctive forms within the clade that may be sepa- rable at the species level. The phylogenetic definition using the multidisciplinary approach described herein provides a frame- work for comprehensively investigating biodiverse lineages of animals, such as the cone snails.
Additional keywords: Neogastropoda, Turriconus , 12SrRNA sequences, phylogenetic analysis, exogenes
Support for this work was provided by grants from the NII4GMS POl GM048677 (to BMO) and the NIHGMS Diver- sity Supplement Fellowship 3 POl GM048677-13S1 (to JSB)
; To whom correspondence should be addressed: olivera@ biology, utah.edu
INTRODUCTION
The evolutionary histories of biodiverse Conus lineages are a challenge to elucidate. In part this is because the genus is so speciose (about 700 species) but also because most prior data in the literature is morphological. The usual approach is to characterize each species in the lineage based on its shell morphology and to evaluate phylogenetic relationships using additional anatomical data, when available.
Prior attempts to divide Conus into subgeneric groups have been based largely on shell morphology. In this work, we focus on one particular branch of Conus that includes the species known as Conus praecellens. Sev- eral previous attempts to determine which species are most closely related to Conus praecellens have grouped C. praecellens with other high-spired forms (Figure 1) that are collected in deep offshore locations. Some of the specific prior hypotheses that have been proposed are summarized in Table 1.
In the most comprehensive modem treatise on Indo- Paeifie Conus species (Rockel et ah, 1995), Conus praecellens is regarded as most closely related to Conus acutangulus. In most of the schemes shown in Table 1 (Marsh and Rippingale, 1964; Okutani, 2000), Conus praecellens is grouped together with Conus acutangulus in the subgenus Conasprella Thiele, 1929. The designated type of Conasprella is “C. cancellatus " ( = C. pagodus). Another species generally thought to belong to this subgenus is the Eastern Pacific Conus arcuatus. In one of the 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 acutangulus in Kerniasprella are forms such as Conus memiae and Conus nereis (Petuch, 1979), the latter regarded by Rockel et ah, 1995 as a form of Conus wakayamaensis (Kuroda, 1956). Thus, the high-spired
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Figure 1. High-spired Conus species previously postulated to be related to Conus praecellens-. Top from left: Conus acutangulus, “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 of the specimens shown are from the Philippines, except lor Conus arcuatus. Measurements provided in Appendix 1.
J. S. Biggs et al., 2010
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Table 1. Previous taxonomic assignments of Conus praecel- lens and Conus acutangulus.
|
Marsh and Rippingale (1964): |
DaMotta (1991): |
Okutani (2000): |
|
Conasprella |
Conasprella |
Conasprella |
|
praecellens |
praecellens |
praecellens |
|
pagodas |
pagodus |
pagoda |
|
arcuatus |
arcuatus |
gracatapi |
|
acutangulus wakayamaensis |
acutangulus |
|
|
Kennasprella |
Endemnoconus |
|
|
acutangulus |
memiae |
|
|
memiae |
wakayamaensis |
|
|
wakayamaensis nereis jaspideus |
tone |
Conus species including Conus praecellens were either all grouped together in Conasprella, or were divided into a praecellens/pagodus group (Conasprella) and an acutangulus/memiae group (Kennasprella) .
These shell morphology-based suggestions can he independently evaluated using molecular data. If only morphological analyses are used, the resulting systemat- ics may not reflect evolutionary trends as the traits may be subject to selection forces that do not reflect common descent. Distinguishing similarity by descent (reflecting the phylogeny) from similarity directed by selection (convergence or parallelism) is problematic without independent data corroborating the morphological evi- dence. Hence a widespread attempt to define biodiver- sity using molecular markers, notably a segment of the COI gene, has led to the “barcode initiative”. Although this initiative has been widely implemented, workers who need to identify field specimens require a more seamless integration of the molecular with the morphological data.
Our first goal is to define a phylogenetic tree with clades that reflect the branching pattern and in turn the evolutionary history of the species. Molecular data pro- vide independent evidence for such a phylogeny and a useful organizational framework for in-depth studies of species-rich groups. The morphological traits mapped onto such a tree distinguish the respective roles of com- mon descent and selection in the evolutionary process.
In this work, we focus on the definition of the putative clade that includes Conus praecellens. Using 12SrRNA sequences, we specifically evaluate which Conus species are most closely related to Conus praecellens . In addition to using a molecular phylogeny to assess morphology-based taxonomy, we have gathered molecular data in the form of the genes that encode toxins expressed in the venom ducts of cone snails. As will be shown, these highly specialized “exogenes” (Olivera, 2006) are useful in defining discrete branches of a large biodiverse lineage such as the cone snails. This three-pronged approach defines a more com- plete picture of the evolutionary history of these biodiverse cone snails with the result that previous morphologically informed hypotheses may be more objectively assessed.
MATERIALS AND METHODS
Specimen Collection. Most forms in the Conus praecellens complex are collected offshore from 30-250 meters in depth. The bulk of Philippine specimens in collections assigned to this species were collected (together with such species as Tibia fusus (Linnaeus, 1758) and Xenopliora Solaris (Kosuge and Nomoto, 1072) around 1960, primarily from a few classical fish trawler localities (Maqueda Bay in Samar Is, Tayabas Bay in Luzon); at the time, these were mostly identified as Conus sowerbii (see Reeve, 1849; Springsteen and Loebrera, 1986). Because other forms in the praecellens complex are mostly from even deeper water, these were less well represented in collections; most specimens available in museums are poorly preserved and/or dead-collected. However, the combination of gill net and hookah collec- tions in the Cebu/Bohol area of the Central Philippines and intensive small trawl collections around the Island of Aliguay has increased accessibility to several forms in the Conus praecellens complex. Some of these are smaller specimens that were sparsely represented in earlier col- lections. A range of live-collected specimens with pre- served protoconchs has become available, which has facilitated the reevaluation of the Conus praecellens spe- cies complex.
Phylogenetic Analysis. We aligned sequences using Clustal X (Larkin et ah, 2007) and refined by eye using MaeClade (Maddison and Maddison, 2005). The tree was inferred using MrBayes (Huelsenbeck et ah, 2001; Ronquist and Huelsenbeck, 2003). The run comprised 1,000,000 generations with the first 25% of the sampled generations discarded as burn-in trees. Two MCMCMC runs (metropolis-coupled Monte-Carlo nrarkov-chain), using four chains each, were used to thoroughly explore tree space. Convergence of the likelihoods was deter- mined by comparing the average standard error of the difference (ASED) in split frequencies between the two runs and by comparing plots of the log-likelihood after the burnin to the end of the runs. Optimality was also judged adequate when tire PSRL (Potential scale reduc- tion factor) for the total tree length and for each model parameter reached 1.00.
Identification and Sequencing of Genomic Clones Encoding O-Superfamily Peptides. Genomic DNA was prepared from 50 mg each of tissues of Conus acu- tangulus, Conus mitratus, Conus pracellens, and Conus stupa using the Centra PUREGENE DNA Isolation Kit Kit (Gentra Systems, Minneapolis, MN) according to the manufacturers standard protocol. These gendmie DNAs were used as templates for polymerase chain reaction (PCR) with oligonucleotides corresponding to conserved 5' intron and 3' UTR sequences of omega and delta prepropeptides. The resulting PCR products were puri- fied using the High Pure PCR Product Purification Kit (Roche Diagnostics, Indianapolis, Indiana) following the manufacturers suggested protocol.
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The eluted DNA fragments were annealed to pNEB206A vector and the resulting products transformed into competent DH5a cells, using the USER Friendly Cloning Kit (New England BioLabs, Beverly, Massachu- setts) following manufacturers suggested protocol. The nucleic acid sequences of the resulting omega and delta toxin-encoding clones were determined according to the standard protocol for automated sequencing.
Morphometric Analysis. Using dial calipers, we mea- sured maximum diameter (mm) and total length (mm; including spire height) of species within the praecellens complex. Relative diameter was calculated as the ratio of maximum diameter to total length. All species were represented by multiple samples. In view of the low between-sample variation, we calculated a single mean relative diameter for each species.
RESULTS
Systematic Descriptions of Three New Species of Conus
by Baldomero M. Olivera and Jason Biggs
Superfamily Conoidea Fleming, 1822 Family Conidae Fleming, 1822 Subfamily Coninae Rafiuesque, 1815 Genus Conus Linnaeus, 1758
Conus anclremenezi Olivera and Biggs, new species. (Figures 1, 2, 6)
Description: Biconical in shape, mature specimens from 25-53mm. Moderately solid, and with a relatively high spire, and generally broader than most related forms (D/L 0.47). Last whorl is broadly conical, with raised spiral ribs that are not smooth but always undulating (and in some specimens, the ribs seem to have arch-like pro- tuberances, instead of a continuous smooth rib). Raised ribs on the body whorl are well separated from each other, with interstices that have axial scales between them.
The body whorl has an off-white ground color with characteristic purplish-brown spots that occur in zones; in the two darker zones, the spots generally cover more spiral ribs and extend into the interspaces (although there is considerable variation). The protoconch is decol- lated in most specimens, but when preserved it is a rounded conical shape, translucent, veiy light yellowish brown or off-white; the protoconch is followed by two white early teleoconch whorls that are lightly nodulose and angled at the periphery. The spots begin to appear on the periphery of the third or fourth teleoconch whorl, and typically these are more closely spaced to each other than are the larger spots in the later spire whorls.
Type Material: The Holotype is deposited in the Marine Science Institute (MSI) at the University of the Philippines; Paratypes are deposited at the Academy of Natural Sciences ol Philadelphia, Philadelphia, Pennsyl-
vania (ANSP 421619); the Museum national d’Histoire naturelle, Paris, France (MNHN 21131); the Field Museum of Chicago, Chicago (FMHN 312461); the Har- vard Museum of Comparative Zoology, Cambridge Mass (MCZ 361611); Zoological Museum of Moscow State University, Aloscow, Russia (Lc-37964) and The Bailey- Matthews Museum, Sanibel, Florida (BMSM 38672) (see Appendix or a complete listing ol paratypes).
Type Locality: The type locality for Conns anclremenezi is Aliguay Island, Philippines, where most specimens in the tvpe series have been collected by commercial fish- ermen using small trawls at depths around 150 m. Another established locality is off Panglao, Bohol, from Balicasag Island to Momo Beach where the species has been col- lected by tangle nets in deeper water (~200-300m).
Geographical Distribution: From the Central to Northern Philippines, probably to Viet Nam and possibly much further West (see discussion below). In the recent book of Thaeh (2005), the specimen figured as Conus praecellens (Plate 61, Fig. 34) is likely to be a specimen of Conus anclremenezi.
Etymology: This species honors the memory of Andre Menez, one of the giants of the field of toxinology.
Remarks: The sculpture on die spire whorls is diagnostic: the spiral ribbons on the larger spire whorls are raised, relatively narrow to very narrow, and always far apart. The vide spacing on the spire whorls between narrow raised spiral ribs is a diagnostic trait of this species; in most similar forms, the spiral ribbons or ridges are much closer together and are more like flattened ribbons, broad and shallow. The broad shape, purplish-brown spots, undulating spiral ribs, and widely spaced ribs on the spire are characteristic features tiiat separate the species from similar forms.
When the protoconch is decollated, this species is difficult to separate from some closely related forms that are potentially variants of Conus praecellens. Most spec- imens can generally be differentiated by the distinctive purple-brown color, the broader shell, the widely spaced spiral ribbons on the spire whorls, and when preserved, the conical protoconch. Most specimens in the type series come from Aliguay.
There is a group of Philippine specimens, not from the type locality, which we tentatively assign to this species. These were collected by the Musorstom expeditions prmoted by the Museum national d’Histoire naturelle, Paris, to Lubang Island/Mindoro. Several large mature specimens ol Conus anclremenezi , all dead collected, were examined. All of these were collected at depths between 160-198 meters; at more shallow collection stations, this form was absent and a narrower Conus praecellens variety was present. This provides a more accurate estimate of the depth at which this species occurs.
Finally, there is a small specimen figured by Rockel et al. (Plate 54, Fig. 14) that appears to be a juvenile of Conus anclremenezi: if the identity of this specimen can
J. S. Biggs et al., 2010
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Figure 2. Two morphospecies with non-“praecellens-\i\ce" protoconchs from Aliguay. All ol the specimens shown are from Aliguay Island, Philippines, except the lower left specimen which was collected from 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 of the types figured are deposited at the Marine Science Institute (MSI), University of the Philippines. Measurements provided in Appendix 1.
be verified, it extends the range of this species across the entire Indian Ocean since the specimen is reported to be from Somalia. Thus, although almost all of specimens examined were from the Central Philippines, there is strong evidence for the occurrence of the species in the Northern Philippines, and the possibility that it may have a geographic distribution that is much wider is raised by the Somali specimen in the Raybaudi-Massila collection.
Conus miniexcelsus Olivera and Biggs, new species (Figures 1, 2, 4, 6 and S)
Conus praecellens f. subaequalis. — Robin, 2008: 424, fig. 14 (non Conus subaequalis , Sowerby III, 1870)
Description: A moderately small shell; adult size range, 25-37 mm. High-spired, with both spire and body whorl
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THE NAUTILUS, Vol. 124, No. 1
having a straight outline, making the shell narrowly biconical. The larval shell has 3. 0-3.5 whorls, translucent brownish or purplish. There are 9-11 teleoconch whorls, the first three being ivory-white, without spots, providing a notable contrast to the translucent-colored protoconch. At around the fourth teleoconch whorl, broad brown- ish spots appear, centered around the periphery. The ground color is white, with chestnut-brown spots. On the body whorl there are a series of flat spiral ribbons. The shell pattern on the body whorl can be divided into 3-5 zones. The most posterior, next to the suture, are a series of about 6 spiral ribbons with extremely fine chest- nut brown spots. These are followed by a zone with 3 noticeably broader spiral ribbons that have deeper brown and larger spots. In most specimens, this is followed by three spiral ribbons that have a finer spotted pattern (but not as fine as in the spiral ribbons in the first zone, closest to the suture). The remainder of the shell towards the tip is covered by spiral ribbons that are darker in color and more heavily spotted; typically the first 3 to 4 are darker than those towards the anterior end of the shell, although there is considerable variation in this regard. In some specimens, the light zone continues to the anterior of the shell.
Type Material: The Holotype is deposited at the Marine Science Institute at the University of the Philip- pines, Paratypes are deposited at the Field Museum, Chicago, Illinois (FMNII 312462); the Museum National d’Histoire Naturelle, Paris, France (MNPIN 21132); the Harvard Museum of Comparative Zoology, Cambridge, Massachusetts (MCZ 361609); the Academy of Natural Sciences of Philadelphia, Philadelphia Pennsylvania (ANSP 421620); Zoological Museum of Moscow State University, Moscow, Russia (Le-37965) and The Bailey- Matthews Museum, Sanibel, Florida (BMSM 38673) (see Appendix or a complete listing of paratypes).
Type Locality: Aliguay Island, Philippines. Most spec- imens in the type series were collected by the commer- cial small-trawl operations off Aliguay Island, at depths of 30- 150m.
Geographical Distribution: Presently known from the Central Philippines to Wakayama, Japan (Paratype #23).
Etymology: The specific epithet emphasizes some strik- ing and unexpected similarities to Conus excelsus despite the considerable disparity in size.
Remarks: A distinguishing characteristic of this species are the spots on the whorls closest to the suture, which are generally extremely line in pattern and greater in number than for any other similar species, followed by the thicker, darker brown spiral ribbons at the center of the body whorl. These features are clearly illustrated in the specimens shown in Figure 3. Conus miniexcelsus is a distinct species, most easily confused with Conus praecellens. However, as discussed above and shown in Figure 3, the differences in protoconch
and early teleoconch morphology between the two spe- cies are consistent distinguishing characters. This feature puts Conus miniexcelsus in the same group as Conus acutangulus, Conus andremenezi, and Conus excelsus (except that the spire of Conus acutangulus has strong tubercules at the sutures). Conus andremenezi is gener- ally larger, with coarse spots that are purplish brown in color instead of chestnut. Conus miniexcelsus is probably most similar to Conus excelsus, although there is a strik- ing difference in size at maturity. The two Japanese spec- imens examined are more solid and chunky than the Aliguay material. Figure 8 shows the different shape and color of the protoconehs and the characteristic switch in Conus miniexcelsus from a conical translucent purplish brown protoconch, to the ivory white first teleoconch whorls, and finally to the normal spotted pattern.
Conus rizali Olivera and Biggs, new species.
(Figures 1, 3, 6)
Description: The species is medium-sized; specimens examined are 26-39 mm in length. The shell is biconic, with an unusually tall, straight, and sharply pointed spire and a straight-sided body whorl, sharply angled at the shoulder. Outline narrow (D/L = 0.397 ± 0.011); The larval shell has two whorls, and is praecellens- like but somewhat proportionally broader than for most specimens of Conus praecellens; this is followed by two teleoconch whorls that have a characteristic white-matte surface, somewhat crinkly; starting with the fourth teleoconch whorl, there are 8-9 spotted spire whorls.
The body whorl is characterized by shallow spiral ribbons with only a narrow interstitial space between them; these are broadly spotted in light yellow-brown. Characteristically, immediately below the periphery, the first spiral ribbon lacks spots, leaving a white zone. Al- though there is some variation, the spots are much ligh- ter in color than in related forms (Paratype 2 almost completely lacks spots in the body whorl).
Type Material: The Holotype is deposited at the Marine Science Institute at the University of the Philip- pines; Paratypes are deposited at the Academy of Natu- ral Sciences of Philadelphia, Philadelphia, Pennsylvania (ANSP 421621); the Harvard Museum of Comparative Zoology, Cambridge, Massachusetts (MCZ 361610) and in the Museum National d’Histoire Naturelle, Paris France (MNIIN 21133) (see Appendix for a complete listing of paratypes).
Type Locality: All type specimens were obtained from commercial dealers in the Philippines, and the exact collection locality of the types could not be verified. Springsteen and Leobrara show a figure of Conus rizali (labeled Conus subaequalis) indicating Punta Lugano, Cebu, suggesting that these were probably collected by fishermen using tangle nets at depths of 100-200m.
Geographical Distribution: Philippines.
J. S. Biggs et al., 2010
Page 7
Figure 3. Three distinctive forms with “praecellens- like” protoconchs. Top row is a series of Conus praecellens, "sowerbii form . Bottom row is Conus praecellens, “Aliguay form”. In the middle row are two specimens of Conus rizali new species, the Holotype (left) and Paratype 2 (right), both MSI. Measurements provided in Appendix 1.
Etymology: This species is named in honor of |ose Rizal, the National Hero of the Philippines. Dr. Rizal, who was executed by the Spanish Colonial Administra- tion in 1898, collected shells as a hobby.
Discussion: Of all of the similar forms. Conus rizali has the most narrow outline (D/L = 0.397 ± 0.011); spec- imens of Conus praecellens from Aliguay, which are generally narrower than the “Sowerbii form” have a D/L = 0.44, and for Conus miniexcelsus ; (D/L = 0.416) these are both narrower than Conus andremenezi.
Although Roekel et ah, put this species in synonymy with Conus praecellens , we believe that it is a distinctive form that can readily be separated from specimens
assigned to Conus praecellens. The narrower outline, the shallow ribbons on the body whorl, and differences in protoconch/early teleoconch moiphology separate Conus rizali from other related forms. Conus rizali was previously figured as Conus suhaequalis Sowerby III, 1870, by authors. This name was used by Springsteen and Leobrera, and by Lim and Wee (1992); however, the specimen recently figured by Robin (2008) as Conus subaequalis is not Conus rizali but Conus minexcelsus. A specimen was also figured by Roekel et al. (Plate 54, Figure 6) but they refer this to Conus praecellens. Conus rizali is sufficiently distinct so that it can immediately be picked out from other related forms discussed elsewhere in this article: the narrow outline of the shell sets it
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immediately apart, and in fact the form that is most similar in outline is Conus gratacapi from Japan, which is an unrelated species. This species has only been inter- mittently collected over the last four decades, and never in large numbers. As has been discussed in detail by Rockel et al., and is shown in the original figure of Sowerby (which Rockel et al., reproduced), the spec- imens that we assign to Conus rizali are clearly not con- specific with the figure of Conus subaequalis , which likely refers to a different form in the Conus praecellens complex.
Morphological Definition of Species in the Conus
PRAECELLENS COMPLEX: TWO “a/FVIEXCELSCS-LIKE” FORMS
In this section, we describe and define two distinc- tive forms in the Conus praecellens complex from the Philippines. As wall be defined in the Discussion, the “ Conus praecellens complex” can be divided into two broad groups on the basis of protoconch morphology, the “ praecellens -like” forms and the “miniexcelsus- like” forms.
The two miniexcelsus- like forms from Aliguay Island (i.e., those with non-praecellens-like protoconchs), which we proposed to designate as new species, are discussed first. The Aliguay specimens of these two forms are easily distinguishable from each other (see Figure 4). Since both of these miniexcelsus -like forms were appar- ently unnamed, these are formally described in the sec- tion above. The appendix summarizes the individual type specimens on which the new taxa are based.
Conus andremenezi Olivera and Biggs, new species (Figure 2)
This form may be similar or identical to Conus bicolor Sowerby I, 1833, which is a preoccupied name. Sowerby then provided a new name in 1841, Conus sinensis. Rockel et al., (1995) stated that “taxonomic status of Conus bicolor/ Conus sinensis (Sowerby II, 1841) remains disputable because the type specimen is lost and the type figure (Plate 54, fig. 3) does not match C. praecellens in a satisfying way: the pictured shell has a comparatively low spire. . .is somewhat bulbous below the shoulder and its color pattern consists of brown axial flames. . .we favor synonomy with Conus praecellens.' The figure shown by Rockel et al. (originally drawn from “ Conus bicolor”) is similar to the species we describe above as C. andremenezi ; we have not adopted the name Conus sowerbii for this species because the syntype in the British Museum does not appear to be nonspecific with C. andremenezi.
We believe that Conus andremenezi is clearly dis- tinguishable from typical Philippine specimens of C. praecellens; first, the protoconch is not “praecellens- like”; second, this form is generally broader and has a characteristic purplish-brown coloration. Furthermore, on the body whorl, there are raised but not flattened
spiral ridges that undulate, with a wade space between ribbons with axial scales between the spiral ridges. More consistently, the sculpture on the spiral whorls has nar- row, raised ridges, widely spaced from each other. This suite of characteristics consistently distinguishes this species from C. praecellens of similar size (see Figure 1) and from Conus miniexcelsus (see next species); Conus rizali is even more distinctive from C. andremenezi. There are a group of small Conus praecellens that are most easily confused with Conus andremenezi; these are discussed under Conus praecellens below.
Conus miniexcelsus Olivera and Biggs, new species (Figure 2)
This very distinctive species is characterized by its rela- tively narrow shell outline (D/L ~ 0.42 vs. 0.47 for C. andremenezi), the multispiral protoconch of 2.5-3. 0 whorls, which is translucent and distinctly brownish or purplish and contrasts in its color with the first 2. 0-2.5 teleoeoneh whorls that are ivory white. In most spec- imens, these white whorls are smooth or have, at most, nearly obsolete tubercles. This is followed by 6-10 spot- ted teleoeoneh whorls that are grooved and have strong axial structure so that the upper part of each spire whorl has a distinctly tiled appearance. The body whorl lias shallow spiral ribbons with regular, brown spots that have a characteristic pattern described in the Appendix in detail. The colored, translucent protoconch contrasting in color with the first two shiny- white teleoeoneh whorls, combined with the slender shape and the very fine spotted pattern are diagnostic of this distinctive species. There is considerable variation in how dark the spots are; a range of variations is shown in Figure 4. A full description of this new species was pro- vided in the previous section; detailed measurements of all the types are provided in the appendix. Almost all specimens have been collected by small trawls in Aliguay from 60-130 m, but occasional specimens have also been collected using gill nets off Balicasag Island. One specimen assigned to this species from southern Japan is included in the type series (Figure 4). Figure 2 makes evident the generally finer pattern and narrower shell shape of Conus miniexcelsus compared to Conus andremenezi. In addition the spiral ribbons of the body whorl of Conus miniexcelsus are smooth, but are dis- tinctly crenulated in Conus andremenezi.
Overview and Description of the
“PRAECELLENS-LIKE FORMS”
Conus praecellens remains a confusing taxon, and the scheme proposed below is not entirely satisfactory; mul- tiple forms have been assigned to this species by various workers. Even after the two “miniexcelsus- like forms” are separated as new species, what remains still com- prises a confusing set of specimens, most of which we are provisionally retaining in C. praecellens. We believe that the retention of diverse forms within C. praecellens
J. S. Biggs et al., 2010
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Figure 4. An illustration of the "miniexcelsus-hke complex”. Shown are five specimens (left five) and close-ups of their respective protoconchs (right five). Left, top and bottom: Conus miniexcelsus (Paratypes 2 and 18, respectively), middle: Conus excelsus, and right top and bottom: Conus acutangulus. Measurements provided in Appendix 1.
will prove to be only an interim solution, and new mor- phologically similar species will be identified once a more extensive molecular and morphological analysis has been carried out over a wider suite of specimens from a greater geographic range.
There is a widely illustrated specimen designated as “a possible syntype” of Conus praecellens from the British Museum. This is atypical ol specimens assigned to C. praecellens from the Philippines. This possible syntype from the China Sea is lighter in color and finer in sculp- ture on the body whorl than either of the two major Philippine varieties that we include in C. praecellens. The first group, “the Aliguay form,” which is small and light colored, has been extensively collected both by the small dredge operations in Aliguay Island, and is the form illus- trated in Figure 3. A second more variable group that we refer to as the “sowerbii forms,” include larger specimens that vary considerably in shell pattern, shape, and size. These comprise most specimens collected by fish trawlers in the period from 1955-1965, particularly from two local- ities, Tayabas Bay and Maqueda Bay. A third group is that referred to by previous authors as Conus subaequalis and
is described above as Conus subaequalis. The three forms are shown in Figure 5.
Conus praecellens “Aliguay form”
(Figure 3)
The series of specimens that we assign to C. praecellens , “Aliguay form”, appears to be the closest to the type in the BMNH in shell pattern; these have mostly been collected in 30-80 fathoms off Aliguay Island, between Mindanao and Bohol in the Philippines. The Philippine specimens are smaller than the BMNH “syntype” (aver- age size ~ 24mm); key features that distinguish this form are a blunt, paucispiral protoconch of two whorls, the relatively smaller size, and the chestnut color of the spots. Details of the spire sculpture and body whorl that are also diagnostic are delineated below.
The shells of this form (see Figure 5) typically have 2. 0-2. 5 protoconch whorls, the first being quite spherical and inflated, and the second narrower and more elon- gate. The first two teleoconeh whorls are typically white and flattened compared to the protoconch whorls, and they are knobbed on the periphery, while the two
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THE NAUTILUS, Vol. 124, No. 1
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Figure 5. Phylogenetic tree of some Conus species based on 12SrRNA sequences. Species shown in Figure 1 are indicated with arrows. Branches are labeled with Bayesian confidence values (posterior probabilities expressed as percentages). These data clearly separate Conus acutangulus and Conus praecellens from the Conasprella species with 100% confidence and join them with C. stupa and C. mitratus with 97% confidence.
protoconch whorls are smooth. There are 8 to 9 whorls spotted with a chestnut brown color, with the first one or two spotted whorl(s) also knobbed. The early teleoconch whorls are characterized by a deep spiral groove on the upper section ol the whorl; these spiral grooves gradually increase in number as the whorls get larger; these are narrow furrows that can ire bisected by axial sculpture that varies considerably in strength; in specimens where the axial sculpture is strong, the area immediately adjacent to the suture looks as il it were tiled, since the combination of the spiral grooves and the axial sculpture divide the area between grooves into square sections. The broader part of the spiral whorl is smooth to the periphery; the lower suture is below the sharply angled periphery.
Conus praecellens “sowerbii forms”
(Figure 3)
There are forms in the C. praecellens complex most com- monly found in collections; most specimens were col- lected by trawlers around I960 in great numbers in the Maqueda and Carigara bays of Samar Island, and in Tayabas Bay of Southwestern Luzon, from Jolo Island in the Sulu Sea. The “sowerbii forms” are larger and more densely spotted than the specimens of the “Aliguay form" described above. There is considerable variation in shell morphology: some specimens are slender and narrow with line sculpture; others appear to be much broader at the shoulders with an overall coarser sculpture. However, when preserved, the protoconchs of all of these have the typical highly inflated first whorl, with only two.
pearly white protoconch whorls. A range of specimens collected from various Philippine localities, all with typical “praecellens- like” protoconchs that are well preserved are shown in Figure 5 (the contrast between these and the “Aliguay form” is also illustrated in that figure).
Given the distinctive (and mutually similar) protoconchs of both the Aliguay and the “sowerbii forms,” we have provisionally assigned these in C. praecellens. However, further characterization of both the radular and gut morphology, as well as a molecular characterization, may prove that these are distinct from each other, and that there are additional separable species embedded in the “sowerbii forms”, a possibility that clearly needs to be further evaluated.
Conus praecellens , other distinctive varieties.
A smaller form of Contis praecellens was recently col- lected by MNHN, off Aurora, Eastern Luzon, Philippines. These specimens were notable because they were veiy similar to Conus andremenezi, but much smaller. They are easily separable from Conus andremenezi because they have the typical “praecellens- type” protoconch. These look veiy different from the two Conus praecellens “forms” described above. We note that in general. Conus andremenezi is a larger species; however, there have been juvenile Conus andremenezi specimens collected using lumum-lumum nets in the Camotes Sea, along with specimens of the Conus praecellens , “Aliguay form," described above. It seems likely that only juvenile spec- imens of Conus andremenezi are collected at this
J. S. Biggs et al., 2010
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locality because lumun-lumiin nets were used, and it pre- sumably takes longer than the three months lumun-lumun nets are laid out for Conus andremenezi to reach full maturity. These small specimens of Conus andremenezi do have the characteristic protoconchs of that spe- cies, though they are somewhat lighter in color than the Alignay series. In contrast, the variety of Conus praecellens collected off Aurora (trawled at 83 m depth) have the praecellens -type protoconch. At the same site, the MNHN expedition collected two dead, somewhat eroded specimens, that were larger in size, in a trawl 189-307 meters in depth that are likely to lie true Conus andremenezi.
In addition, a species was recently described as Conus beatrix, Poppe and Tagaro, 2006. We have not had an opportunity to examine the Holotype of this species; it maybe that these represent a series of unusually pale spec- imens, possibly continuous