Acta Geologica Polonica, Vol. 50 (2000), No. 1, pp. 169-174

The erroneous distinction between tetrabranchiate and dibranchiate

ZEEV LEWY

Geological Survey of Israel, 30 Malkhe Yisrael St., Jerusalem 95501, Israel. E-mail: [email protected]

ABSTRACT:

LEWY, Z. 2000. The erroneous distinction between tetrabranchiate and dibranchiate cephalopods. Acta Geologica Polonica, 50 (1), xxx-xxx. Warszawa.

The informal subclass name Dibranchiata is still attributed to extant coleoids, referring to the possible taxo- nomic significance of the gill number in cephalopods. Ammonoids and the dibranchiate octopods exhibit a remarkable similarity in breeding strategies and an ammonite shape of argonautid egg cases, suggesting close phylogenetic relationships in which octopods are nude ammonoids, and accordingly reflect the dibranchiate anatomy of ammonoids. All these cephalopods descended from the Paleozoic , which are represent- ed today by two genera with a tetrabranchiate gill structure and other anatomical features, which differ from those in extant coleoids. The physiology of extant nautiloids enables them to survive in waters with low oxy- gen content at a few hundred meters depth, toward where the nautiloids withdrew. The two pairs of gills, which occur in extant nautilids only, are suggested to reflect a minor anatomical modification to improve respiration in low oxygen settings by the duplication of the initial single pair of gills, and are thus of no tax- onomic significance.

Key words: Cephalopoda, Dibranchiata, Tetrabranchiata, Extant Nautiloids.

INTRODUCTION for which they and the fossil nautiloids were attrib- uted to subclass Ectocochlia or Tetrabranchiata All extant belong to the genera respectively (MILLER & FURNISCH 1957a). The and (WARD & SAUNDERS extant coleoids lack an external conch (a few have 1997) in a single family Nautilidae within the super- variably-shaped, internal, rudimentary skeletal fea- family , which appeared in the Upper tures), posessing a single pair of gills only, for which (KUMMEL & al. 1964; TEICHERT & they were distinguished as subclass Endocochlia or MATSUMOTO 1987). The phylogenetic scheme of Dibranchiata respectively (ibid.). OWEN (1832) these nautiloids suggests that they, like all other fos- applied this anatomical criterion for the systematic sil and extant cephalopods, descended from the same subdivision of fossil cephalopods as well, and Late ancestral organism (YOCHELSON included in the Tetrabranchiata the extinct nautiloids 1973). Anatomical and skeletal features in extant and ammonoids. Later (in SWEET 1964, p. K10) he cephalopods were assumed to be of phylogenetic assigned the extinct belemnoids to the Dibranchiata. significance for the subdivision of the class These subclass names were commonly used in the Cephalopoda into subclasses. Extant nautiloids have literature despite the awareness of scientific uncer- an external conch and two pairs of gills (ctenidia), tainties (MILLER & FURNISH 1957a, p. xxii, 1957b, p. 170 ZEEV LEWY

L2). This superficial differentiation, whereby the ly in microconchs, the probable male form of a pair fossil nautiloids were emplaced within the of sexual dimorphs (e.g., COBBAN & KENNEDY Tetrabranchiata (=Tetrabranchia), led to the conclu- 1976). Many large ammonites slightly uncoil, inflate sion that the two pairs of ctenidia (Tetrabranchia) the terminal body chamber, and constrict the aper- represent the primitive anatomy of the cephalopods ture (Fig. 1.1). Others change mode of coiling and (NAEF 1913, 1926). YONGE (1964, p. I32) rejected develop a terminal hooked body chamber (Fig. 1.2- this interpretation and suggested that the early 5). The aperture in some of these latter heteromorphs cephalopods were probably slow moving dibranchi- faced the preceding whorl (Fig. 1.2-5), which pre- ates, which with the increase of activity and rate of vented the extension of the body for swimming and metabolism duplicated the ctenidia to improve respi- hunting. When these conchs were in floating orien- ration. The external conch prohibits the expansion of tation the aperture faced upward (Fig. 1), restricting the mantle cavity of cochleate cephalopods. lateral movement and predation (LEWY 1996). Probably the conchless coleoids regulate the intensi- Therefore, the heteromorph ammonites were sug- ty of the water circulation better than the cochleate gested to change from predating to feeding on plank- cephalopods, and therefore these coleoids retained tic organisms while moving vertically through the the initial cephalopod single pair of gills, which was water column (e.g., SEILACHER & LABRBERA 1995; sufficient for the respiration of these highly active WESTERMANN 1990). This awkward explanation creatures (ibid.). overlooks the functional morphology of the modi- The assumption that all fossil ectocochleate fied terminal body chamber and aperture, which in cephalopods were tetrabranchiate, and the endo- many cases must have resulted in the ultimate death cochleate or conchless coleoids were dibrachiate of the ammonoid. These pre-death, fatal modifica- like their extant relatives was recently questioned. tions had a crucial function in the life cycle of these LEWY (1996) compared the breeding strategies of ammonoids, which is successful breeding. The aper- octopods and ammonoids, and concluded that tural appendages in male microconch probably were octopods are nude ammonoids and reflect the involved in copulation (COPE 1967), whereas the ter- dibranchiate anatomy of the latter. This conclusion minal body chamber of female macroconchs needs further elaboration and substantiation by addi- changed into a boat-like, or hook-shaped egg case. tional evidence to examine the systematic signifi- Thousands of minute embryonic shells of cance of the number of gills in cephalopods. ammonoids occur in the body chambers of 15 mature macroconchs of the Upper Turonian Scaphites ferronensis (COBBAN), and in the adhering CLOSE RELATIONSHIP BETWEEN matrix (collected by W.A. COBBAN; LANDMAN AMMONOIDS AND OCTOPODS 1985). These macroconchs must have sunk to the bottom where part of their content fell out of the Some mature ammonoids modify their terminal conch. The two early growth stages represented by body chamber, constrict the aperture or add to it var- these ammonitellae evidence the presence in the ious appendages. Apertural appendages occur main- conch of pre-hatched ammonitellae together with

5 2 1 3 4

Fig. 1. Examples of ammonite modified terminal whorl and aperture, which restricted the activity of the ammonoid, resulting in the death of some by starvation; this modification turned the terminal body chamber into a floating egg case; 1. Neoptychites; 2. Nostoceras; 3. Nipponites; 4. Pravitoceras;5.Scaphites; scale bar 1 cm ERRONEOUS DISTINCTION BETWEEN TETRABRANCHIATE AND DIBRANCHIATE CEPHALOPODS 171

1a

2a 2b

1b

Fig. 2. Argonautid egg cases resembling Upper ammonites; the constricted aperture in some conchs was opened and enlarged;

1a. Argonauta hians LIGHTFOOT (from ABBOTT, 1968); 1b. Hoplitoplacenticeras (From PAULCKE, 1907); 2a. Argonauta nodosa

LIGHTFOOT; 2b. Jeletzkytes nebrascensis (Owen) (from LANDMAN & WAAGE, 1993) just hatched ones. Such mode of breeding in a float- ammonites in the Cenozoic required the argonautids ing egg case is exclusively exhibited by octopod arg- to secrete a complete egg case in the shape that their onautids. The sexually mature female Argonauta ancestors learned to emend in the Upper Cretaceous. secretes from her pair of enlarged arms a fragile cal- However, the need of the ancestral argonautids to citic shell, in which it sits and lays numerous, tiny, lay the eggs in a floating case rather than in a sta- spherical eggs, similar to those found fossilized in a tionary protected site, remained unexplained. few ammonite body chambers (LEHMANN 1981). The remarkable physiological and morphological Fossil argonautid egg cases are known from the similarities between octopod and ammonoid Oligocene onward probably because of the rare cephalopods suggested that octopods are nude preservation of these fragile conchs (HOLLAND ammonoids which lost their conch, and hence the 1988), which did not protect the brood from preda- egg case, during the Mesozoic (LEWY 1996). They tors. Perhaps therefore, more efficient and “econom- were physiologically forced to perform either the ic” modes of pelagic breeding were developed by pelagic (in a floating egg case) or the stationary related octopods, which carry their tiny eggs in mod- mode of breeding. During the and ified arms (BOLETZKY 1986, p. 223). The develop- Cretaceous ammonoid empty conchs were available ment of eggs in floating egg cases has the advantage to serve as egg cases for the conchless octopods. To that it disperses the brood and increases its chances enter, for example, a scaphitid conch (Fig. 2.2b) they of survival compared to stationary egg concentra- had to break the constricted part of the terminal body tions. The motion of the drifting egg case probably chamber and enlarge the conch to contain them- aerated the tiny eggs and prevented their encrusta- selves and the eggs. The constructional modifica- tion by algae and fungi (indirect brood care; LEWY tions may have started with organic components and 1996). later these octopods developed means to secrete cal- The remarkable similarity between extant and fos- careous (calcitic) complementary parts of the empty sil argonautid egg cases to Upper Cretaceous ammonite which they favored to occupy. The lack of ammonites (Fig. 2), such as Hoplitoplacenticeras, an exoskeleton improves mobility, and hence com- the scaphitids Jeletzkytes and Discoscaphites and petition on food and life territory, and to escape from Phylloceras, strengthens the above discussed simi- predators. Because of these functional advantages larity between ammonoids and octopods. NAEF the octopod-ammonoids survive the K/T biological (1922) suggested that Cretaceous ancestral argonau- turnover, whereas the slow-moving cochleate tids used to lay eggs in empty ammonites, which ammonoids went extinct, probably through overpre- they partly modified for this purpose. The absence of dation (e.g., by crustaceans; RADWA¡SKI 1996). The 172 ZEEV LEWY scarcity of empty floating nautiloid conchs in of the nautiloids, and the resulting expulsion of the Cenozoic times forced the surviving octopod arg- latter into marginal, less hazardous habitats. Most of onautids to produce a complete egg case. Such egg the fossil endocochleate cephalopods such as the cases were constructed in the form of the empty teuthids and the belemnoids had probably ten arms ammonite conchs, which were preferably occupied, as their extant relatives have, two of which were modified and enlarged by the ancestral argonautids. longer and modified to skillfully catch prey, such as According to the advocated relationships between the slow moving nautiloids. These latter, together octopods and ammonoids, the former exhibit the with the ectocochleate ammonoids, were also inten- dibranchiate anatomy of ammonoids. Thus the living sively hunted by marine reptiles and fish, as well as and probably all fossil coleoids, together with the by other predators (SAUNDERS & al. 1987; ammonoids were dibranchiate, all of which evolved RADWA¡SKI 1996). Nevertheless the Mesozoic from Paleozoic nautiloids through the bactritoids. ammonoids and related cephalopods contributed to Therefore, it seems reasonable to assume that all nautiloid ultimate withdrawal to less dangerous liv- cephalopods descended from dibranchiate nautiloid ing niches, such as in dark, “deep” waters, as exem- ancestors. The extant tetrabranchiate nautiloid plified by the species of the extant Nautilus and species are assumed to represent an evolutionary Allonautilus. However, the gradual diversification duplication of the number of ctenidia under the and increase in size of the Cretaceous marine preda- strong ecological stresses to which extant nautilids tors likewise affected the slow-moving, nekto-benth- had to adapt. ic cochleate ammonoids.

PREDATION ON NAUTILOIDS ADAPTATION TO LOW-OXYGEN SETTINGS

The nautiloids nearly disappeared at the end of the Live nautiloids occur confined to a small bio- Cretaceous, when the cochleate ammonoids became province extending from the offshore of Burma and extinct. Survivors temporarily revived the nautiloid Australia in the Indian Ocean to the east and south, stock in the early Tertiary, but with limited success, off the Fiji Island in the western Pacific Ocean and as evidenced by the two extant genera. While the off Japan in the north (SAUNERS 1981). During day- ammonoids thrived in the Mesozoic oceans they did time they stay in rather cool waters at depths of 400- not avoid preying on their own young (LEHMANN 600 m (e.g., ROUX & al. 1991). They rise to shal- 1973, 1981), and may have fed on small nautiloids lower waters of about 100 m to search for food dur- as well, which occupied the same living niches as the ing the night (STENZEL, 1964 p. K92). This few hun- ammonoids. SAUNDERS & al. (1987) described dred meters thick water column comprises oxygen extant Nautilus conchs with octopod borings as evi- depleted zones in which the live nautiloid survives dence for octopod predation on nautilids. This obser- in its daily trips by “depressing its metabolic rate to vation can be extended to fossil octopods and their match the amount of ambient oxygen available” cochleate form the ammonoids, even though the (BOUTILLER & al. 1996, p. 534; see BALDWIN 1987, feeding strategy has changed. Ammonoids broke and HOCHACHKA 1987). “Nautilus is unique conchs and swallowed skeletal particles such as amongst the cephalopod molluscs in having the ammonoid aptychi, bivalves, echinoderm fragments capacity to survive prolonged periods of low oxy- and periopods of small decapod crustaceans gen levels”, which may be the result of a physiolog- (LEHMANN 1973, 1981; RIEGERAF & al. 1984; JÄGER ical modification of the blood circulation, and the & FRAAYE 1997). However, the extant octopods bore possible utilization of oxygen contained in the into the exoskeleton by radular rasping, and inject a buoyancy chambers to help sustain aerobic metabo- venum to kill the prey (SAUNDERS & al. 1978). No lism (BOUTILLER & al. 1996, p. 536). Thus the pre- such octopod borings were hitherto recorded from sent nautiloid is a hypometabolic, hypoxic , fossil conchs (BISHOP 1975, p. 274). It may be spec- which moves slowly in deep waters, mainly verti- ulated that this latter mode of feeding was probably cally (O’DOR & al. 1993). Physiologically it must acquired not long ago, and that the Mesozoic considerably differ from its Paleozoic and Mesozoic octopods broke exoskeletons and swallowed hard relatives, which were active marine predators main- parts as the cochleate ammonoids did. ly in shallow waters (common in reefal and carbon- Ammonoids probably increased in diversity and ate platform sediments). The few Upper Cretaceous quantity during the Mesozoic through the oppression and Tertiary nautiloid genera are frequently found ERRONEOUS DISTINCTION BETWEEN TETRABRANCHIATE AND DIBRANCHIATE CEPHALOPODS 173 in outer shelf and pelagic sediments. This profound REFERENCES reduction in diversity and the preference of deeper marine settings than in earlier times resulted from ABBOT, R.T. 1968. Seashells of North America. 280 pp. the threat of numerous, more skillful marine preda- Golden Press; New York. tors. The gradual adaptation of the nautiloids to the BALDWIN, J. 1987. Energy metabolism of Nautilus swim- harsh ecological settings in these deep marine ming muscles. In: W.B. SAUNDERS & N.H. LANDMAN, waters was probably achieved through physiologi- (Eds), Nautilus: the biology and paleobiology of a liv- cal modifications such as the suppression of meta- ing fossil. Topics in Geobiology, 6, 325-329. Plenum bolic rates. The retraction into less menacing niches Press; New York. started already in Late Mesozoic times, and thus BISHOP, G.A. 1975. Traces of predation. In: R.W. FREY proceeded for more than 65 million years. This time (Ed.), The study of trace fossils, pp. 261-281. span is more than necessary in evolutionary Springer-Verlag; New York. processes to result in the anatomical modifications, BOLETZKY, S. v. 1986. Encapsulation of cephalopod whereby extant nautilids differ from other living embryos: a search for functionalcorrelations. American cephalopods (e.g., STENZEL 1964). It is suggested Malacological Bulletin, 4, 217-227. that among these evolutionary modifications is the BOUTILIER, R.G., T.G. WEST, G.H. POGSON, K.A. MESA, duplication of the single pair of cephalopod ctenidia J.W. WELLS, & WELLS, M.J., 1996. Nautilus and the art into the tetrabranchiate anatomy of extant Nautilus of metabolic maintenance. Nature, 282, 534-536. and Allonautilus species to improve respiration in London. oxygen-depleted waters in which they live. COPE, J.C.W. 1967. The palaeontology and stratigraphy of Accordingly, the two pairs of gills in extant nau- the lower part of the Upper Kimmeridge Clay of tiloids are merely an anatomical modification of the Dorset. Bulletin of the British Museum (Natural basic dibranchiate anatomy of all extant and fossil History), Geology, 15, 1-79. London. cephalopods. Hence, the term Dibranchiata should HOCHACHKA, P.W. 1987. Oxygen conformity and metabol- not be used, even as an informal characterization of ic arrest in Nautilus. Analysis of mechanisms and func- the endocochleate and conchless cephalopods, as tions. In: W.B. SAUNDERS & N.H. LANDMAN (Eds), the exocochleate were dibranchiate as well, apart Nautilus: the biology and paleobiology of a living fos- from the Recent and perhaps some earlier sil. Topics in Geobiology, 6, 331-338. Plenum Press; (Pleistocene, Neogene?) nautiloids. In this aspect of New York. it is suggested (LEWY 1996) to transfer HOLLAND, C.H. 1988. The Paper Nautilus. New Mexico the octopods (at least the Incirrata) from the Bureau of Mines & Mineral. Research Memoire 44, to the . 109-114. Socorro. JÄGER, M. & Fraaye. R. 1997. The diet of the Early Toarcian ammonite Harpoceras falciferum. CONCLUSIONS Palaeontology, 40, 557-574. Oxford. KUMMEL, B., with FURNISH, W.M. & GLESNISTER, B. 1964. The close similarity in modes of breeding and Nautiloidea-, K383-K457. In: R.C. MOORE shape of the egg case between ammonoids and (Ed.), Treatise on Invertebrate Paleontology, Pt. K, extant octopods suggests that octopods are nude 3: Geological Society of America and ammonoids, and hence reflect the dibranchiate University of Kansas Press; New York. anatomy of the latter. These dibranchiate LANDMAN, N.H. & WAAGE, K.M. 1993. Scaphitid ammonoids and extant coleoids descended from ammonites of the Upper Cretaceous (Maastrichtian) Paleozoic nautiloids, which were supposed to be Fox Hills Formation in South Dakota and Wyoming. tetrabranchiate as their extant relatives were. This Bulletin of the American Museum of Natural History, assumption overlooks the remarkable ecological 215, 1-257. New York. change that the nautilids underwent in Cenozoic LEHMANN, U. 1973. Zur Anatomie und Ökologie von times by adapting through profound physiological Ammoniten: Funde von Kropf und Kiemen. and anatomical changes to waters of a low oxygen Paläontologische Zeitschrift, 47, 69-76. Stuttgart. content. The duplication of the cephalopods initial — 1981. The ammonites. Their life and their world. 246 pair of gills in extant nautilids is regarded as anoth- pp. Cambridge University Press; Cambridge. er minor anatomical modification to withstand LEWY, Z. 1996. Octopods: Nude ammonoids that survived these harsh settings, and has no taxonomic signifi- the Cretaceous-Tertiary boundary mass extinction. cance. Geology, 24, 627-630. Boulder. 174 ZEEV LEWY

MILLER, A.K. & FURNISH, W.M. 1957a. Introduction to Posidonienschifer. Biostratigraphie, Fauna und Fazies Cephalopoda, xx-xxii. In: R.C. MOORE (Ed.), Treatise des südwestdeutschen Untertoarciums (Lias epsilon). on Invertebrate Paleontology, Pt. L, Mollusca 4. 195 pp. Enke; Stuttgart Geological Society of America and University of SAUNDERS, W.B. 1981. The species of living Nautilus and Kansas Press. New York. their distribution. The Veliger 24, 8-17. Berkeley. — & — 1957b. Introduction to Ammonoidea. L1-L2. In: SAUNDERS, W.B., C. SPINOSA & DAVIS, L.E. 1987. R.C. MOORE (Ed.), Treatise on Invertebrate Predation on Nautilus. In: SAUNDERS, W.B. & Paleontology, Pt. L, Mollusca 4. Geological Society of LANDMAN N.H. (Eds), Nautilus: the biology and paleo- America and University of Kansas Press; New York. biology of a living fossil. Topics Geobiology, 6. MOORE, R.C., LALICKER, C.G. & FISCHER, A.G. 1952. Plenum Press, 201-212. New York . Invertebrate fossils. 766 pp. McGraw-Hill Book SEILACHER, A. & LABARBERA, M. 1995. Ammonites as Comp; New York. cartesian divers. Palaios 10, 493-506. Tulsa. NAEF, A., 1913, Studien zur generellen Morphologie der STENZEL, H.B. 1964. Living Nautilus, K59-K93. In: Mollusken, 1. Ergebnisse und Fortschritte in MOORE, R.C. (Ed.), Treatise on Invertebrate Paleonto- Zoologie, 3, 73-164. Jena. logy, Pt. K, Mollusca 3. Geological Society of America — 1922. Die fissilen Tintenfische. Verlag von Gustav and University of Kansas Press. New York. Fischer, 1-322. Jena. SWEET, W.C. 1964. Cephalopoda - General features. K4- — 1926. Studien zur generellen Morphologie der K13. In: MOORE, R.C. (Ed.), Treatise on Invertebrate Mollusken, 3. Ergebnisse und Fortschritte in Paleontology, Pt. K, Mollusca 3. Geological Society of Zoologie, 6, 27-127. Jena. America and University of Kansas Press; New York. O’DOR, R.K., J. FORSYTHE, D.M. WEBBER, J. WELLS & TEICHERT, C. & MATSUMOTO, T. 1987. The ancestry of the WELLS, M.J. 1993. Activity levels of Nautilus in the Nautilus. In SAUNDERS, W.B. & LANDMAN, N.H. wild. Nature, 362, 626-628. London. (Eds), Nautilus: the biology and paleobiology of a liv- OWEN, R. 1832. Memoir on the pearly nautilus (Nautilus ing fossil. Topics in Geobiology, 6, 25-32. Plenum pompilius, LINN.) with illustrations of its external form Press; New York. and internal structure. Royal College of Surgeons, 1- WARD, P.D. & SAUNDERS, W.B. 1997. Allonautilus: a new 68. London. genus of living nautiloids cephalopod and its bearing PAULCKE, W. 1907. Die Cephalopoden der oberen Kreide on phylogeny of the Nautilida. Journal of Südpatagoniens. Berichte der Naturforschenden Paleontology, 7, 1054-1064. Tulsa. Geselschaft zu Freiburg i. Br., 15, 1-82. Freiburg. YOCHELSON, E.L. 1973. The bearing of the new Late RADWA¡SKI, A. 1996. The predation upon, and the extinc- Cambrian monoplacophoran genus Knightoconus tion of, the latest Maastrichtian populations of the upon the origin of the Cepalopoda. Lethaia, 6, 275- ammonite species Hoploscaphites constrictus (J. 310. Oslo. SOWERBY, 1817) from the Middle Vistula Valley, YONGE, C.M. 1964. General characteristics of Mollusca, Central Poland. Acta Geologica Polonica, 46 (1-2), I3-I36. In: MOORE, R.C.(Ed.), Treatise on Invertebrate 117-135. Warszawa. Paleontology, Pt. I, Mollusca 1. Geologica Society of RIEGRAF, W., G. WERNER & LÖRCHER, F. 1984. Der America and University of Kansas Press; New York.

Manuscript submitted: 27th October 1999 Revised version accepted: 20th February 2000