MALACOLOGIA, 1990, 32(1): 3-18 ANATOMICAL BASIS FOR THE ORIGIN AND EVOLUTION OF THE TOXOGLOSSAN MODE OF FEEDING Yuri I. Kantor A.N.Severtzov Institute of Animal Evolutionary Morphology and Ecology. Academy of Sciences of the USSR, LenlnskI Prospekt 33, Moscow 117071, USSR ABSTRACT Five types of feeding mechanism can be recognized in the Toxoglossa. The mechanism by which separate marginal teeth are used at the proboscis tip for stabbing and poisoning the prey with secretions from the venom gland originated in "lower" turrids possessing a radular mem- brane, solid marginal teeth, a central tooth and sometimes lateral teeth. The morphological prerequisite of the appearance of toxoglossan mode of feeding was firstly the appearance of the venom gland, which initiated the formation of the specialized intraembolic type of proboscis with the buccal mass situated at its base. Hollow marginal teeth originated repeatedly and indepen- dently in different phylogenetic lineages of Toxoglossa. It is supposed that the ancestors of Toxoglossa were primitive mesogastropods with a short acrembolic proboscis and taenioglos- san radula. The separation of Toxoglossa from the Rachiglossa occurred at an early evolution- ary stage, when the common ancestor had seven radular teeth in each transverse row. Key words: Toxoglossa, evolution, feeding, radula. INTRODUCTION origin of "toxoglossan" feeding mechanism. Does it have a single or repeated ongin in evolution, and what are the morphological The order Toxoglossa is large, diverse, and prerequisites for its appearance? The main well differentiated from the other prosobranch aim of this study was to clarify these prob- gastropods. It includes four Recent families: lems. Turhdae, Conidae, Pervicaciidae, and Tere- bridae. One of the most outstanding and well- known features of the order is the specialized MATERIALS AND METHODS feeding mechanism of its higher representa- tives. That is the use of separate hollow mar- Materials for the study were obtained ginal teeth at the proboscis tip for stabbing mainly from the collections of the Zoological and subsequent poisoning the prey, with the Museum of Moscow State University and In- venom produced by a usually well-developed, stitute of Oceanology of the USSR Academy tubular venom gland. Most representatives of of Sciences (Moscow). Other material was the order (the "higher" Turridae, Conidae and kindly provided by Dr. James H. McLean (Los part of the Terebridae) lack the radula mem- Angeles County Museum of Natural History, brane, and the radula itself consists of only USA); the late Dr. Virginia O. Maes (Academy hollow marginal teeth. The teeth being formed of Natural Sciences, Philadelphia, USA); Dr. in the radula sheath are finally stored in the Anders Waren (Naturhistohska Riksmuseet, short arm of the radula sac, which is probably Sweden); and Dr. R. N. Kilburn (Natal Mu- a homologue of the sublingual pouch. seum, South Africa). At the same time, many toxoglossans The morphology of the digestive tract was (mainly "lower" turrids) have a normally de- studied using sections 8-10 fxm thick, which veloped radular membrane with two to five were cut after dehydration and embedding in radular teeth per transverse row. Information paraffin wax. The sections were usually on feeding mechanisms and the morphology stained with Massons triple stain. Its second of these "lower" toxoglossans is very limited, solution, which contains orange-G and aniline although the functional analysis of their diges- blue, was used for staining the radula. Large tive system and feeding mechanism may elu- specimens were also dissected under the ste- cidate the pathways of ongin and evolution of reomicroscope. In total, the morphology of 18 "toxoglossan" mode of feeding. species of Turridae belonging to six subfam- One of the most interesting problems is the ilies was studied. — KANTOR RESULTS AND DISCUSSION oesophagus behind the buccal cavity. It has been shown that the venom gland produces a Within the Toxoglossa there is significant venom that immobilizes or kills prey animals variability both in the morphology of the rad- (Kline. 1956: Pearce, 1966: Miller, 1980: ular teeth and their number in a transverse Shimek & Kohn, 1981: Kohn, 1956, 1959, row (the radular formulae: 1-1-1-1-1, 1-0-1- 1968, many others). The buccal tube leads 0-1, 1-1-0-1-1, 1-0-0-0-1). The morphological from the buccal cavity to the mouth, which changes in the radular apparatus and associ- opens at the proboscis tip. The buccal tube ated structures of the anterior digestive sys- has thick muscular walls in "lower" toxoglos- tem form the main evolutionary trends of the sans, but is thin-walled and practically lacking order. Several authors have tried to classify muscular fibres in higher representatives. the radular types of Toxoglossa according to It should be noted that the functional anal- both the morphology and probable mecha- ysis was carried out mainly using the anatom- nism of function (Thiele, 1929: Powell. 1966: ical evidence, because data on feeding be- Morrison, 1966: McLean. 1971). The most haviour and diet are scarce and chiefly complex classification was proposed by concern species of Conidae, Terebridae and Shimek & Kohn (1981), who isolated six func- some higher Turridae. As our knowledge of tional types of toxoglossan radula, four of the morphology of turrids becomes more pre- which are found in lower "non-toxoglossate" cise, the proposed classification may change. turrids (those with solid marginal teeth). How- ever, one can say that only two general feed- Feeding Mechanism Type 1 ing mechanisms include all the isolated types: "toxoglossate" for those gastropods which The first functional type of digestive system have only hollow marginal teeth and lack a and feeding mechanism, that in which the radular membrane, and "non-toxoglossate" radula is used as a whole organ only within for lower turrids. In the first feeding type, sep- the buccal cavity, was found among species arate, hollow marginal teeth are used at the of Pseudomelatominae (Turndae). This is an proboscis tip for stabbing and poisoning the endemic subfamily from central west Amer- prey: in the second type, the radula is used as ica, which includes three genera and several a whole organ only within the buccal cavity. In species (McLean, in Keen, 1971). The anat- their analysis, Shimek & Kohn (1981) used omy of two species Pseudomelatoma peni- mainly isolated radulae. without taking into cillata (Carpenter, 1864) and Hormospira account the morphology of the digestive tract, maculosa (Sowerby, 1834)—indicates the and this led to some misinterpretation (Sy- isolated position of the group among the Tox- soev & Kantor, 1987). oglossa (Kantor, 1988). This is obvious, in A functional morphological analysis of the particular, from the presence of long curve of digestive system of the species studied sug- the antehor part of the digestive tract, a rarely gests that there are at least four different found and undoubtedly secondary feature in types of feeding mechanism for toxoglossans turrids. The curve is formed either by elonga- possessing a radula and one type for radula- tion of the part of the oesophagus between less species. the nerve ring and the buccal mass (in Pseudomelatoma penicillata (Fig. 1 ), the buc- General Anatomy of Toxoglossa cal mass is situated at the proboscis base and far ahead of the nerve ring) or by the elonga- Before a more detailed analysis of the feed- tion of the posterior part of the buccal tube (in ing mechanism, a brief description of the an- Hormospira maculosa, the buccal mass is sit- terior part of the digestive system of the Tox- uated in front of the nerve ring, distant from oglossa is necessary. One of the outstanding the proboscis base). features of the order is the specialized in- Both species have a well-developed venom traembolic type of proboscis (Smith, 1967), gland, longer in H. maculosa (its length com- which is characterized by the position of the prises 0.5 of the shell height). Although the buccal mass at the base of the proboscis or diet of Pseudomelatominae is unknown, the even behind it. This precludes the use of the presence of the large venom gland testifies to radula as a whole organ for rasping and graz- predatory mode of feeding. The gastropods ing, as in other gastropods. The second fea- have a muscular proboscis with a wide oral ture is the presence of the well-developed tu- opening in the form of triangular or transverse bular venom gland entering the anterior slit and lack an oral sphincter. The radula of EVOLUTION OF TOXOGLOSSAN FEEDING FIG. 1. Anatomy of Pseudomelatoma penicillata (Carpenter). A—semidiagrammatic longitudinal section of the anterior part of the molluscan body. Salivary glands with the duct and convolutions of the venom gland together with the nerve ring are not shown. B, — organs of the body haemocoel (B: from the left, C: from above). Pseudomelatominae consists of a large and Shimek & Kohn (1981). The large inner vol- well-developed central tooth, flanked by ume of the buccal cavity and the curve of the large, sharply pointed, scythe-like marginal anterior part of the digestive tract suggests teeth. Thus, although the morphology of the that the prey is partially digested in the ante- marginal teeth is primitive, the absence of rior part of the digestive tract. lateral teeth indicates that the group has In summary, the main features of this feed- deviated greatly from the toxoglossan ances- ing mechanism are; prey capture with the aid tor. of the proboscis tip, without using marginal From the morphology of the digestive tract, teeth (since the oral opening lacks a sphincter one can suggest that prey capture probably and the shape of the marginal teeth prevents occurs with the aid of the proboscis tip and is their being held at the proboscis tip); use of facilitated by the presence of a wide and the large and powerful radula for slicing and highly extensible oral opening.