Hydrophobic Larval Shells: Another Character for Higher Level Systematics of Gastropods

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Hydrophobic Larval Shells: Another Character for Higher Level Systematics of Gastropods J. Moll. Stud. (1997), 63,425-430 1 The Malacological Society of London 1997 HYDROPHOBIC LARVAL SHELLS: ANOTHER CHARACTER FOR HIGHER LEVEL SYSTEMATICS OF GASTROPODS RACHEL COLLIN* Zoology Department, University of Washington, Box 351800, Seattle, WA 98195, USA (Received 19 April 1996; accepted 8 January 1997) ABSTRACT branchs are still not well resolved (Bieler, 1992; Mikkelsen, 1996; Wise, 1996). This low Higher level relationships within the Gastropoda are resolution is due to both the small number of difficult to determine, in part due to the paucity of putative homologies that are phylogenetically identified synapomorphic characters. Larval shell hydrophobicity may be a useful additional character informative at this level, and inadequate avail- for gastropod family systematics. A survey of 57 able character information for many groups. species indicates that larval shell hydrophobicity is Because anatomical characters traditionally common or ubiquitous in pyramidellids, opistho- used for gastropod systematics are often absent branchs, and marine pulmonates but is unknown in or not informative for lower heterobranchs patellogastropods, vetigastropods, and caenogas- (Mikkelsen, 1996; Wise 1996), it is important to tropods. The taxonomic distribution of hydrophobia investigate unconventional characters. Descrip- larval shells is consistent with the hypothesis that it is tions of gastropod embryology and larvae are a heterobranch synapomorphy. Unfortunately the beginning to yield such potentially useful char- condition in key 'lower' heterobranchs such as archi- tectonicids and valvatoids is unknown. acters for systematics (van den Biggelaar & Haszprunar, 1996; Robertson, 1985). Useful characters should be consistent within taxa, INTRODUCTION vary among taxa and should not be obviously functionally dependent on other characters Malacologists have yet to come to a consensus used at the same level of analysis. Larval shell on higher level relationships within the class hydrophobicity may be one such unconven- Gastropoda (Bieler, 1992). Discerning relation- tional systematically useful character. ships is difficult because derived characters Larval shells of many heterograstropods and shared among these many disparate groups are opisthobranchs are hydrophobic (an unfortu- scarce. Considerable attention has recently nate but standard term); in other words they are been focused on the relationships among physically characterized by a surface that is groups within the 'lower' heterobranchs: the water repellent. Because calcium carbonate is architectonicids, pyramidellids, mathildids and hydrophilic, hydrophobic shells are probably others (Haszprunar, 1985, 1988; Ponder, 1991; due to lipids and non-polar proteins in either the Waren, 1993). These groups have traditionally shell's organic matrix or the periostracum. As a been viewed as morphological mosaics of consequence of this, larvae with hydrophobic prosobranch and opisthobranch characters, but shells frequently become trapped at the air- they also share several derived characters. The water interface in standing cultures and presence of a pigmented mantle organ (PMO), survival is significantly reduced unless measures ciliated strips in the mantle cavity, chalazae in are taken to break or reduce the surface tension. the egg masses, heterostrophic shells, and a In order to explore the systematic usefulness unique osphradial type unite several families of hydrophobic larval shells, I investigated its within this group and suggest relationships with distribution among marine gastropods using a opisthobranchs and pulmonates (Haszprunar, combination of my observations and published 1985, 1988; Ponder, 1991; Robertson, 1985; reports of larval hydrophobicity. Waren, 1993). Despite the clear monophyly of the hetero- MATERIALS AND METHODS branchs, the relationships among 'lower' hetero- Current Address: Committee on Evolutionary Biology, University of I observed development type and larval shell Chicago, Culver Hall, 1025 E. 57th St., Chicago, IL 60637, USA hydrophobicity. Adult Crepidula fornicata (Linnaeus, 426 R. COLLIN 1758) (Caenogastropoda) and Boonea bisuturalis larvae and empty larval shells of hydrophobic (Say, 1822) (Pyramidellidae) were collected in the species were also hydrophobic, while shells of summer of 1993 at Woods Hole, Massachusetts, other larvae were not. Larvae that are not U.S.A. All other specimens were collected at San normally hydrophobic do, however, become Juan Island, Washington, U.S.A. between 1994 and trapped in the surface tension after being fixed 1996. Eggs and egg masses or capsules were kept in small glass bowls at ambient sea temperature in 10% formalin. These observations provide (8-12°C) until hatching. Larvae were reared in further evidence that larvae become trapped at unstirred 0.45 ^m-filtered sea water and fed a mixture the surface as a result of shell surface properties of Isochrysis galbana and Rhodomonas sp. All obser- and not larval behaviour. vations were of live larvae of known parents. Larvae that became trapped at the air-water interface were counted as hydrophobic while those that were never DISCUSSION stuck at the surface were not considered to be hydrophobic. When placed on a slide with a cover slip, larvae with hydrophobic shells also became The distribution of hydrophobic larval shells trapped at the air-water interface along the edge of among gastropods suggests that it is a derived the water drop. character shared by pyramidellids, opistho- I also surveyed published accounts of larval shell branchs and marine pulmonates. Its distribu- hydrophobicity. Species were scored as hydrophobic tion is congruent with, but not identical to the if the author stated that veligers became trapped in distribution of pigmented mantle organs the surface tension or if special methods of reducing (PMOs), heterostrophic larval shells, ciliated the surface tension were necessary to successfully strips in the mantle cavity, chalazae in the egg rear larvae. Unfortunately, many studies of larval masses, and unique osphradial and sperm development do not mention hydrophobicity or the specific conditions of larval culture and could not be morphology (Haszprunar, 1985, 1988; Ponder, used for this survey. Because hydrophobic shells 1991; Robertson, 1985; Waren, 1993). Because cause higher mortality in cultures of long-lived feed- a phylogenetic hypothesis that resolves the ing larvae than in ephemeral non-feeding larvae, relationships among the 'lower' heterobranchs studies of feeding larvae were more likely to mention is not currently available, none of these puta- hydrophobicity. tive homologies can be tested for congruence on a cladogram (Patterson, 1982). However our inability to demonstrate homology a priori does RESULTS not preclude a character's use in phylogenetic analyses (Hennig, 1966). Larval shell hydrophobicity is clearly associ- Before larval shell hydrophobicity can be ated with taxonomic category (Tables 1 and 2; used as a character in a thorough phylogenetic three-way G-test, 53.1<G<64.1, df = 2, analysis additional taxonomic sampling is p«0.005). None of the patellogastropod, veti- necessary. The state of this character needs to gastropod, or caenogastropod larvae had be determined for other lower heterobranchs hydrophobic shells; neither those that I reared such as architectonicids and mathildids, and the nor those described in published records. In representation of tropical species needs to be contrast, it is clear from both my observations increased. Shell hydrophobicity and other such and published accounts of larvae (Table 1) that larval characters might also be useful in deter- larval shell hydrophobicity is widespread mining the problematic relationships of groups among pyramidellids, opisthobranchs, and such as pteropods for which adult characters marine pulmonates. Although few non-feeding have not been particularly informative. (4) or direct developing (2) opisthobranch One of the consequences of hydrophobic larvae were included in the survey, hydro- larval shells is that larvae in laboratory cultures phobic larval shells were not convincingly tend to clump together and become trapped in associated with larval type, independent of tax- the surface film. Trapped larvae die unless they onomy (Table 2; three-way G-test; 0<0<11.7, are quickly submerged. Amio (1955) thought df = 1). that tiny air bubbles inside pulmonate and Microscopic observations of larvae in culture opisthobranch larval shells cause them to dishes and on microscope slides with cover slips aggregate at the surface. However microscopic showed that when hydrophobic larvae swim observations show that this is not true (pers. near the surface they become trapped with the obs. and R. Robertson, pers. com.). Addition- shell extending above the water surface. Larvae ally, agents like cetyl alcohol that chemically of other species often swim at the surface but reduce surface tension can be used to prevent never become trapped. Additionally, dead larvae from becoming trapped. LARVAL SHELL HYDROPHOBICITY 427 Table 1. Systematic list of gastropod larval type and hydrophobicity. Species Larval type* Hydrophobic Referencet Patellogastropoda Lottia digitalis (Rathke) nf, p n Loft/a pe/fa (Rathke) nf, p n Tectura scutum (Rathke) nf, p n Vetigastropoda Calliostoma annulatum (Lightfoot) nf, p n Calliostoma ligatum (Gould) nf, p n Diodora aspera (Rathke) nf, p n Haliotis kamschatkana Jonas nf, p n Margarites pupillus (Gould) nf, p n Tegula funebralis (Adams) nf, p n A. Moran,
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