Muricidae, Rafinesque, 1815

Webster, Nicole B & Vermeij, Geerat J, 2017, The varix: evolution, distribution, and phylogenetic clumping of a repeated gastropod innovation, Zoological Journal of the Linnean Society 180 (4), pp. 732-754 : 742-743

Muricidae

Species of Muricidae bear the most stereotypical and elaborate varices. They are currently divided into eleven subfamilies ( Barco et al., 2010, 2012), five of which we consider to be completely lacking varices: Rapaninae , Coralliophilinae , Trophoninae , Haustrinae , and Pagodulinae . All the other subfamilies have at least a few members with varices ( Fig. 2M–P ). Many species have axial lamellae rather than varices, such as those in the Trophoninae , with very thin lamellae that lack the robustness, intervarices, and the spacing of varices ( Fig. 3C ). The earliest varicate muricid is the Early Paleocene genus Timbellus ( Merle, Garrigues & Pointier, 2011) with three or four synchronized varices on each whorl. Although the subfamily to which Timbellus belongs is unclear, Barco et al. (2012) suggests it may fit with the typhines. We estimate seven origins of varices in the Muricidae , but the lack of subfamilial trees makes this a broad estimate at best, with clear evidence of phylogenetic clumping. These seven origins are one each for Muricinae , Ocenebrinae , Ergalataxinae , Typhinae + Tripterotyphinae , and Aspellinae , as well as two origins within the Muricopsinae .

Muricid varices are in most cases synchronized between whorls and, if not, are generally evenly spaced. One of the key features of Muricids is the intervarical ribs. Nearly all varicate species have a regular number of ribs interspersed between varices. This pattern often arises gradually during growth from a juvenile pattern where all axial elements appear as ribs or lamellae. As the snail grows, the elements differentiate into regularly spaced, more elaborate varices, with intervarical ribs ( Spight & Lyons, 1974). Although many Hexaplex lack intervarical ribs, these ribs are usually present on earlier whorls and intermittently present on the last whorl ( Merle et al., 2011). Generally, muricid varices grow episodically, with short intense spurts of shell growth completing an intervarical region and varix, followed by periods of quiescence where shell growth is limited to reinforcing the new shell segment ( MacKenzie, 1961; Inaba, 1967; MacGinitie & MacGinitie, 1968; Spight, Birkeland & Lyons, 1974; Spight & Lyons, 1974; Illert, 1981). Some authors report snails going into hiding and/or not eating during bursts of shell growth ( Inaba, 1967), but this is not true in the laboratory for Ceratostoma foliatum (Pers. Obs., NBW) .

Muricid varix morphology has four distinctive features. First is the base of the varix, which can be rounded (as in Haustellum ) or asymmetrical with a gradual adapertural side and abrupt abapertural side (as in Typhis and Hexaplex ). Second is height variation, from low structures ( Hexaplex ) to extended (most Timbellus ). Third is edge shape, which ranges from relatively smooth ( Ceratostoma and Haustellum ) through varying degrees of spinosity ( Murex ) including branching spines ( Chicoreus ). Last is the degree to which the spiral cords are emphasized in the varix, from very pronounced, forming a corrugated edge ( Ceratostoma ), to low spiral cords that are barely evident ( Siratus ). All of these parameters combine in various ways to describe the full diversity of varices in the Muricidae ( Powell, 1927; Marwick, 1934). The most common pattern is three varices per whorl, but two, four, and sometimes six per whorl also occur. In an extreme case, the genus Muricanthus ( Muricinae ) can have 12 varices per whorl.

The Ergalataxinae have a few varicate members: Ergalatax , Cronia , and Phrygiomurex , as well as the fossil taxa Odontopolys and Lyropupura, which are related to the nonvaricate Vitularia , and Daphnellopsis and Lindapterys whose relationships are poorly understood ( Palmer, 1937; Lozouet, Ledon & Lesport,1994; Claremont et al., 2013). The origin of the Ergalataxinae is difficult to determine, but appears to have been in the Eocene ( Vermeij & Carlson, 2000; Claremont et al., 2013), with multiple varicate taxa from that time ( Daphnellopsis , Odontopolys , Morula purulansis Martin, 1914 , and Lyropupura). Ergalataxine varices are generally low and rounded, while they are flared in Lyndapterys and are mostly synchronized with two per whorl, even in the earliest L. vokesae Petuch, 1987 (E. Miocene) ( Lozouet et al., 1994). In some taxa, such as Tenguella and Morula spinosa (H. Adams & A. Adams, 1853), individuals have evidence of a growth stoppage prior to the aperture that resembles a varix. This may be a polymorphic trait in these species or could be due to failed predation events altering shell growth. Some shells show remnants of apertural teeth inside the shell at these locations, which we believe supports the latter hypothesis ( Fig. 3A ).

Few Muricopsinae have true varices, despite having some of the most elaborate axial sculpture among muricids. Most species actually have impressively elaborate lamellae like the seemingly impossible branching club lamellae in Homalocantha anatomica (Perry, 1811) and its relatives ( Fig. 3F ). Three groups show true varices: Subpterynotus textilis (Gabb, 1873) , with three alate synchronized varices per whorl and identifiable intervarical nodes (E. Miocene – Pliocene) ( Vermeij, 2005b). The other varicate genera belong to the Favartia complex: Pygmaepterus menoui (Houart, 1990) , some similar species and several Caribiella . We believe these represent two separate origins, based on the distinct morphology of Subpterynotus . This subfamily was deemed polyphyletic by Barco et al. (2010), and a great deal of uncertainty about generic placement remains.

Only in the Typhinae , which arose in the Early Eocene, and the very similar Tripterotyphinae , do all members appear to have varices ( D’Attilio & Hertz, 1988). These subfamilies have similar large alate varices with a distinct intervarical anal tube. Only the most recent excurrent tube is open; previous ones are filled in during growth of the next varix. Shells in these subfamilies can have two to five varices; Distichotyphis for example has two varices per whorl, but most have three to four varices aligned per whorl.

Most Muricinae have varices, and the few exceptions are generally fossil groups that may be more properly considered Muricidae sensu lato, or stem muricids ( Attiliosa , Bouchetia , Calotrophon , Crassimurex , Eopaziella , Flexopteron , Nucellopsis , Paziella , Poirieria ). Truly spiny varices, epitomized by Murex pecten , only occur within the muricines. Bolinus , with generally five to seven varices on the last whorl, has an interesting trend where the two earliest species, B. beyrichi (?L. Eocene – E. Oligocene) and B. submuticus (Early-Mid Miocene) ( Grateloup, 1846) , are the most variable in the number of both varices and intervarical ribs, a pattern that we would expect if varices arise before the canalization of their positioning.

Although the validity of the Aspellinae , all of whom have varices, is contested, we have kept it separate here ( Barco et al., 2010; Houart & Héros, 2013). Aspella bear two varices per whorl, on the edges of the dorsoventrally flattened shell. This genus arose in the Late Oligocene with A. subanceps ( Merle et al., 2011) . Varix number is more variable in Dermomurex s.l, with two to eight varices on the last whorl, depending on the species. On earlier whorls, these are interspersed with intervarical ribs, which fade away gradually, and in some species, the number of varices also gradually decreases ( Vokes, 1985). Viator has the largest number of varices (eight), while Gracilimurex only has two per whorl. The varices are aligned either with previous varices or previous intervarical ribs ( Vokes, 1985). Dermomurex is the oldest genus, with Dermomurex s.s, Takia , and Viator extending back to the Early Oligocene ( Merle et al., 2011). Ingensia has four varices on the last whorl and is most similar to Dermomurex , and no fossils are known ( Houart, 2001). These genera are united by a thick intritacalx (an outer calcareous shell layer, above or replacing the periostracum), and low, rounded, smooth varices.

It is difficult to separate the varicate and nonvaricate Ocenebrinae into clear clades without a broad phylogeny of this morphologically diverse subfamily. The earliest appear in the Early Oligocene, while Ocenebrinae probably arose near the Middle Eocene ( Vermeij & Vokes, 1997; Merle et al., 2011). Although two varicate taxa included in the phylogeny of Barco et al. (2010), Eupleura nitida (Broderip, 1833) and Ocinebrellus inornata (Récluz, 1851) (called Ceratostoma in Barco et al., 2010), were not sister taxa, we feel greater taxon sampling will be required to answer this question. About half of ocenebrine genera have varices, and only Ocinebrina and Ocenebra appear to have both varicate and nonvaricate species, with a high degree of variability, even intraspecifically. Interestingly, the only muricid with a subterminal varix that we encountered was Ocinebrina paddeui Bonomolo & Buzzurro, 2006 , which occasionally produces a single dorsal varix, about half whorl back from the aperture ( Bonmolo & Buzzurro, 2006). Ocenebrine varices can vary from low and rounded in Ocinebrina edwardsii (Payraudeau, 1826) (these are only occasional) to the huge alate varices of Pteropurpura and Ceratostoma . Most have three varices aligned per whorl, except Eupleura , with two varices along the plane of the dorsoventrally flattened shell, and Ceratostoma rorifluum (Adams & Reeve, 1849) , with four.

Figures

Figure 2. Examples of varices. (A) Ellobiidae: Pythia scarabaeus (L., 1758), lateral view. (B) Ellobiidae: Ellobium aurisjudae (L., 1758), dorsal view. (C) Epitoniidae: Cirsotrema varicosum (L., 1822) JVM3131, lateral view. (D) Eulimidae: Melanella martinii (A. Adams in Sowerby, 1854) JVM1093, apical view; (D’) Lateral view. (E) Batillariidae: Pyrazus ebeninus (Bruguière, 1792), oblique apical view. (F) Cerithiidae: Cerithium eburneum Bruguière, 1792, JVM1132, apical view. (G) Potamididae: Cerithideopsis californica (Haldeman, 1840), apical view. (H) Strombidae: Laevistrombus canarium (L., 1758), O365(D-58), apertural view. (I) Cassidae: Phalium areola (L., 1758), JVM851, apical view. (J) Bursidae: Crossata ventricosa (Broderip, 1833), apertural view, arrowhead; hollow varix. (K) Pseudomelatomidae: Imaclava sp., apertural view. (L) Drilliidae: Imaclava pilsbryi Bartsch, 1950, JVM3053, lateral view. (M) Muricinae: Chicoreus nobilis Shikama, 1977, apertural view. (N) Aspellinae: Aspella pyramidalis (Broderip, 1833), JVM1488, apical view. (N’) Dorsal view. (O) Typhinae: Haustellotyphis cumingii (Broderip, 1833), JVM1362, apertural view. (P) Ocenebrinae: Eupleura nitida (Broderip, 1833), JVM1504, apertural view. (Q) Colubrariidae: Colubraria tortuosis (Reeve, 1844), apertural view. (R) Columbellidae: Strombina fusinoidea Dall, 1916, JVM1634, apical view. (S) Photinae: Phos senticosus (L., 1758), JVM1676, dorsal view. (T) Cancellariidae: Bivetiella cancellata (Linnaeus, 1767), JVM2879, apertural view. Scale bars: 5 mm; arrows indicate one (not all visible) varix. JVM and O represent the University of Alberta collection specimen numbers, specimens without collection numbers come from the Vermeij collection.

Figure 3. Varix-like sculpture not considered to be a true varix. (A) Ergalataxinae: Tenguella granulata (Duclos, 1832) dorsal view, with scar-like rib (arrow). (A’) Apertural view, showing previous apertural teeth associated with scar-like rib (arrow). (B) Vasum turbinellus (L., 1758), dorsal view. (C) Trophoninae: Nipponotrophon stuarti (E. A. Smith, 1880), lateral view. (D) Harpidae: Harpa amouretta Röding, 1798, apical view. (D’) Dorsal view. (E) Epitoniidae: Epitonium scalare (L., 1758), JVM3118, apertural view. (F) Muricopsinae: Homalocantha anatomica (Perry, 1811), apertural view. Scale bars: 5 mm. JVM and O represent the University of Alberta collection specimen numbers, specimens without collection numbers come from the Vermeij collection.