See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/285808121 The shell in Vampyropoda (Cephalopoda): Morphology, functional role and evolution Article · January 2004 CITATIONS READS 65 2,638 1 author: Viacheslav Bizikov Russian Federal Research Institute of Fisheries and Oceanography 30 PUBLICATIONS 406 CITATIONS SEE PROFILE All content following this page was uploaded by Viacheslav Bizikov on 01 July 2016. The user has requested enhancement of the downloaded file. Всероссийский научно-исследовательский институт рыбного хозяйства и океанографии (ВНИРО) В. А. Бизиков РАКОВИНА VAMPYROPODA (CEPHALOPODA): морфология, функциональная роль и эволюция Ruthenica, Supplement 3 Moscow • December, 2004 CONTENTS Introduction 3 Material and methods 5 Results 8 Vampyroteuthis infernalis 8 Opisthoteuthis californiana 14 Grimpoteuthis umbellata 20 Cirroteuthis muelleri 24 Enteroctopus dofleini 29 Benthoctopus sibiricus 35 Bathypolypus salebrosus .....40 Eledone messyae 43 Alloposus mollis 46 Ocythoe tuberculata 54 Argonauta nodosa 58 Japetella diaphana 62 Amphitretus pelagicus 64 Discussssion 67 Variation of the shell structure and shell-soft body relationship in Vampyropoda 67 Homologies of the shell among Vampyropoda 74 The process of shell transformation 74 Paleontological evidences 77 Evolution of the shell in Vampyropoda 80 References 84 Editor of the volume: A. V. Sysoev Zoological museum of Moscow State University Camera-ready copy: Yu. I. Kantor, A.N.Severtzov Institute of Ecology & Evolution, Russian Ac. Sci. © V. A. Bizikov, 2004 © Ruthenica, 2004, design The shell in Vampyropoda (Cephalopoda): morphology, functional role and evolution Vyacheslav A. BIZIKOV All-Russian Research Institute of Fishery and Oceanography (VNIRO), V.-Krasnoselskaya str., 17, Moscow, 107140, RUSSIA; E-mail: [email protected] The shell ofmollusks is the part that determines the whole. Adolf Naef, 1921 ABSTRACT. Comparative functional morphology and mic- separation of stellate ganglia in all recent octopods presents rostructure of internal shell vestiges have been studied in 14 morphological evidence that this group evolved from some species of recent Vampyropoda including the single recent vampyromorph-like ancestor with wide middle plate of gla­ representative of vampire squids, Vampyroteuthis infernalis dius proostracum. Two crucial events took place in evolution Chun, 1903, 3 species of Cirrata and 10 species of Incirrata. of the shell in octopodian lineage: reduction of the middle Relationship between the shell and the soft body was studied plate of proostracum and conus resulting in transformation on total cross-sections of the mantle at different planes. The of vampyroteuthoid-like gladius into the gladius of the cirrate study shows that the shell plays different role in different type; and reduction of the transversal connection (saddle) in groups of eight-armed Coleoidea, and evolution of the shell the cirrate gladius resulting in its transformation into paired was stipulated by evolution of its function. In Vampyroteut­ stylets of the Incirrata. In Incirrata the shell underwent gra­ his, an early evolutionary offshoot of the Vampyropoda, the dual reduction until its complete loss in several evolved shell represents a typical gladius of the teuthoid type that forms. This last event, complete disappearance of the shell, provides attachment sites for the fins, mantle, funnel and head retractors, and the visceral sac. In cirrate octopods the has occurred independently in all three principal lineages of gladius represents a remnant of cone flags, wings and lateral Incirrata: Octopodoidea, Bolitaenoidea and Argonautoidea. plates of vampyromorph gladius, which is transformed mos­ In all cases the final loss of the shell was accompanied by tly into a 'fin support'. In the Incirrata the shell is reduced the reduction of jet-swimming in connection with develop­ to paired rods, stylets, functioning as anchors supporting the ment of a 'walking' habit involving the arms (benthic Octo­ funnel retractors. In several advanced lineages of Incirrata podoidea) or heavy reliance on passive floatation in pelagic the shell has been lost completely. Bolitaenoidea and Argonautoidea. The final loss of the shell Each lineage of recent octopodiforms — Vampyromorp- vestiges in advanced Incirrata did not change their soft-body hida, Cirrata and Incirrata — has its own characteristic type design, which remained generally the same as in primitive of shell structure and shell-soft body relationships. Wide benthic Octopodoidea. INTRODUCTION comprises less than 0,004% of the body mass [Zuev, 1965]. But even these vestiges disappear in some octopod lineages: Bolitenoidea, Argonautoi­ Octopods have the most unusual shell among dea, some Octopodoidea [Robson, 1932; Voight, cephalopod mollusks. It differs greatly from the 1997]. chambered, coiled shell of the pearly Nautilus, Origin of octopod shell is obscure. Its morpho­ from the calcareous buoyant sepion of cuttlefishes, logical elements reveal no apparent homology to and from the chitinous supporting pen (gladius) of any part of the shell of other coleoids, both recent teuthids. Reduction of the shell that occurs in all groups of Coleoidea reaches its apex in the Octo- and fossil. There is no trace of a phragmocone or poda. In finned octopods (suborder Cirrata) the proostracum. The octopod shell is soft and cartila­ shell is represented by a saddle-, butterfly- or U- ge-like, which differs from the hard, chitinous sub­ shaped structure while in finless octopods (subor­ stance of the teuthoid gladius. Naef [1921/1923, der Incirrata) it is reduced to a pair of widely se­ p.657] noted, 'it has to be assumed, that the shell parated spindle-like rods, or stylets, situated obli­ (of octopods) consists mainly of a remnant of the quely on the dorsal side of the mantle [Naef, proostracum with a flattered cone'. However, even 1921/23]. The stylets are very small: their mass if Neaf is correct, we do not know, what parts of 4 V. A. BizikpBiziko\v i Table 1. List of species examined in the study. Таблица 1. Список исследованных видов. ORDER Number of specimens examined Mantle length range, mm FAMILY males females males females Species VAMPYROMORPHIDA VAMPYROTEUTHIDAE Vampyroteuthis infernalis Chun, 1903 3 53 — 70 CIRRATA OPISTHOTEUTHIDAE Opisthoteuthis californiana Berry, 1949 25 7 40 — 64 19 — 44 Grimpoteuthis umbellata (Fisher, 1883) 2 45 — 49 CIRROTEUTHIDAE Cirroteuthis muelleri Eschricht, 1838 1 4 80 65 — 128 INCIRRATA OCTOPODIDAE Enteroctopus dofleini (Wulker, 1910) 16 8 135 — 265 145 — 260 Benthoctopus sibiricus Loyning, 1930 16 9 60 — 175 83 — 200 Bathypolypus salebrosus (Sasaki, 1920) 4 47 — 56 Eledone messyae Voss, 1964 1 1 63 35 ALLOPOSIDAE Alloposus mollis Verrill, 1880 2 1 63, 67 57 TREMOCTOPODIDAE Tremoctopus violaceus Chiaie, 1830 2 57, 60 OCYTHOIDAE Ocythoe tuberculata Rafinesque, 1814 2 96, 103 ARGONAUTIDAE Argonauta nodosa Solander, 1786 2 94, 108 BOLITAENIDAE Japetella diaphana Hoyle, 1885 1 57 AMPHITRETIDAE Amphitretus pelagicus Hoyle, 1885 1 26 the coleoid proostracum evolved into the octopod to the vampyromorphs, on the one hand, and to the shell and why. We also do not know what the ho­ cirroctopods and octopods, on the other hand. mology is between the U-shaped shell of Opistho- Knowledge of the highly variable morphology teuthidae, the saddle- or butterfly-shaped shell of of the shell in the Octopoda is fragmentary. The the Cirroteuthidae and the dorsal stylets of finless shell is better known in those finned octopods octopods. Possible clues for understanding the ori­ where it is used in systematic analysis [Aldred et gin and evolution of the shell in the Octopoda may al, 1983; Nesis, 1982/1987; Collins, Henriques, come from its sister group, Vampyromorphida Pic- 2000; Villanueva et al, 2002]. In finless octopods kford, 1939. The single living vampyromorph, details of the shell vestiges have been traditionally Vampyroteuthis infernalis Chun, 1903, has a set of absent from systematic descriptions, and their very characters combining such 'teuthid' features as a presence is rarely mentioned [Akimushkin, 1963; well-developed, chitinous gladius with a generally Voight, 1997]. The inner structure of octopod shell octopod-like brachial crown [Pickford, 1949]. and its growth pattern have not been studied. Vampyromorphida and Octopoda have long been Morphological variability of the octopod shell united into a single taxon with different names, first indicates variability of its function. In finned octo­ on the basis of general similarity: Octobrachia pods the shell is commonly considered a fin sup­ [Young, 1989], later on the basis of morphological port, its flattened lateral parts serving as the attac­ and genetic cladistic analyses: Vampyropoda [Bo- hment sites for the fin bases [Robson, 1932; Aldred letzky, 1992; 1999], Octopodiformes [Berthold, et al, 1983]. The function of stylets in finless oc­ Engeser, 1987; Young, Vecchione, 1996; Carlini, topods is not clear. Akimushkin [1963] considered Graves, 1999; Haas, 2002]. The name Vampyropo­ them as mere vestiges without any specific functi­ da (Boletzky, 1992) seems to be the most approp­ on. Naef [1921/1923, p. 676] believed the stylets riate and will be used in the present paper. It alludes 'serve mainly as points of attachment for the ret- Shell in Vampyropoda 5 ractors of funnel and cephalopodium'. The shell is ce caecum clearly not a useless vestige, at least in species cenp central thickened part (in the