Morphological Perspectives of the Seahorse Hippocampus kuda (Bleeler) Vertebral System
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1 Abstract: Morphological Perspectives of the Seahorse Hippocampus kuda (Bleeler) Vertebral System K.Kumaravel, E.Rethina Priya, S.Ravichandran, and T.Balasubramanian Centre of Advanced Study in Marine Biology, Annamalai University, Parangipettai The vertebral system in Hippocampus kuda is highly specialized because of the vertical locomotion and tail prehensility. The vertebral elements represent a special case of morphological changes. We investigated the vertebral spine in H. kuda through skeletal morphometric characters, in order to describe functional and structural patterns. Actually, the dorso-ventral tail bending ability in the genus Hippocampus is one of the most impressive morphological modifications in the evolutionary history of fishes respectively. The vertebral size decreases from the anteriormost element backward, with some local variation at the dorsal area. The allometric trajectory leads to a natural ventral bending of the tail, promoting its prehensile function. A fan-shaped array of cartilaginous bones, the pterigiophores, forms the internal supporting structure of the dorsal fin. Each pterigiophore is composed of a proximal radial that extends from a vertebra to the dorsal side of the animal, where it fuses to a middle radial. The middle radials fuse with each other to form a dorsal ridge upon the spheroidal distal radials. The dorsal and pectoral fins are the primary locomotor organs in seahorses (Hippocampus) and pipefish (Syngnathus). The small dorsal fins beat at high oscillatory frequencies against the viscous medium of water. Key words: Seahorse, Vertebral system, Locomotion, Dorsal fins INTRODUCTION: Seahorses are found primarily in warm and coastal waters; they are worldwide distributed in tropical and temperate regions, roughly from 50 degrees north to 50 degrees south latitude. Seahorses and few other syngnathids are the only fishes that can bend the tail in a strict spiral used as a prehensile appendage. Considering the 52 genera of syngnathids (Nelson, 1994), the dorso-ventral tail bending ability have been evolved only in Hippocampus and in few other taxa like Acentronura and Amphelikturus (Dawson, 1985). Though Solenostomidae -the sister-group of Syngnathidae - share many characters and a common evolutionary history with them, the new movement of seahorse tail can be considered a real apomorphy into this family (Hale, 1993). Seahorses spend most of time attached to algae and corals by their prehensile tail, cryptic with the surrounding substratum. Swimming is highly specialized through rapid oscillations of the dorsal fin (Breder & Edgerton, 1942, Ashley-Ross, 2002), the caudal fin being absent and the whole caudal region having lost its role in locomotion. Locomotion by fin undulation is widespread among fishes that need of a slow 63
2 speed and high maneuverability within complex, obstacle-strewn environments such as coral reefs (Lindsey, 1978). A unique way of swimming called hovering (Videler, 1993) evolved with the seahorse new anatomy and the camouflage ability. Seahorse tail has also an important function in the social behavior of these animals: males strongly hang each other with the tail when competing for females and it is softly used by the couple during mating (Vincent, 1994). The new tail bending skills and posture of seahorses have probably opened ecological alternatives that revealed advantageous considering the high number of species into this genus. At least theoretically almost all pipefishes have preserved a lateral movement of the tail and in most cases the tail fin as well. Compared with the general organization of the biomechanical system of other fishes, Hippocampus undergoes substantial modifications in relation to the proportions of the myotome parts (Rauther, 1925, Hale, 1996). Previous experimental approaches have demonstrated a direct involvement of a couple of cordon like median ventral muscles, and their connection with hemal spines (Hale, 1996). Nevertheless, significant innovations in the axial skeleton of seahorses have not been explored. In this paper we explore the variation of the vertebral metameric series in Hippocampus kuda through geometric morphometrics. (e.g., Bookstein, 1996, Rohlf & Marcus, 1993, Adams et al., 2004). Metameric elements represent a specific case of morphological variation. Thus, shape variables can be regressed and compared by virtue of their serial position.hence this research paper focuses on the skeletal morphology of H.kuda based on their vertebral structures. LOCOMOTION DORSAL FINS: Locomotion via movements of the median fins has arisen independently multiple times in the evolution of fishes. The methods of median fin propulsion are as varied as the taxa that employ them (Lindsey, 1978). Locomotion by dorsal fin undulation is classified as amiiform exemplified by Amia calva, but also seen in many mormyrids, Gymnarchus, and syngnathids, including Syngnathus and Hippocampus). Gymnotiform locomotion is characterized by undulations of the anal fin only (seen in gymnotids and notopterids). Undulation of both dorsal and anal fins is referred to as balistiform (seen in triggerfish and their relatives, some cichlids, centriscids, and flatfish). Finally, tetraodontiform locomotion is defined as oscillations of short-based dorsal and anal fins (seen in pufferfish and ostraciids). Median fin propulsion is associated with relatively slow, but precise, locomotion in complex habitats such as coral reefs and obstacle-strewn stream or sea beds (Lindsey, 1978, Videler, 1993). Most fishes that use median fin propulsion generate low-frequency waves (E2 Hz) of high amplitude in the fins, allowing them to swim with high hydrodynamic efficiency (defined as useful power output divided by power input to move the fin; Blake, 1980). The family Syngnathidae, comprising the seahorses and pipefish, is an exception members of this group which undulate their dorsal fins at very high frequencies (440 Hz in seahorses(breder and Edgerton,1942,Blake, 1976) with low amplitude, leading to reduced efficiency and very slow swimming speeds (Blake,1980). Because the swimming speeds of seahorses and pipefish are slow, one may expect that the musculature powering dorsal fin movements would be relatively weak. However, the dorsal fin muscle is required to contract against substantial resistance as it beats the fin back and forth through the viscous medium of water. Furthermore, the muscle must contract at a high frequency while performing positive work against the environment. Indeed, the oscillation is so rapid 64
3 MATERIAL AND METHODS Sampling and configurations. Specimens of Hippocampus kuda were obtained from by catch in Tuticorin coastal environment during summer One adult male was selected according to its good maturity status and lack of pathological or sub pathological alterations. One individual has been used because of the explorative purpose of this study. The specimen has been cleaned by immersion in 2-3 % KOH solution for few hours. Digestion of skin and soft flesh parts has exposed the skeleton and the characteristic bony plates that cover syngnathids body. (Fig.1) Head Pectoral fin Eye Dorsal fin Snout Brood pouch Tail fin Fig.1: Morphology of Hippocampus kuda (male) RESULTS: The exposed skeletal parts of seahorses were arranged in order with respect to the vertebral status (Fig.2 &3). The dorsal and cervical vertebrae are clearly distinguished. 65
4 Fig.2. Skeletal morphology of H.kuda Fig.3.Cephalic part of H.kuda Cervical vertebrae: This group is heterogeneous, with the three elements showing different shapes. The first is mainly characterized by a compression of the posterior area, backward bending of the entire structure and protruding of the neuro-caudal edge. The second vertebra shows the enlargement of the neuro-cephalic quarter, and reduction of the neuro-caudal one. The third cervical vertebra is the less diversified, showing just a minor anterior enlargement of the upper neural edge. 66
5 Abdominal vertebrae. Compared to the consensus average shapes, the abdominal structures are characterized by a slightly shorter and higher neural area that is, a vertical stretching of the upper part.(fig.4&5).this pattern is more evidenced in the pre-dorsal segments than in the postdorsal ones. Dorsal vertebrae: The two dorsal elements show the vertical stretching of the posterior body, with consequent bending of the whole structure becoming relatively shorter. The supradorsal vertebra is conversely characterized by a marked development of the neuro-cephalic quarter, and reduction of the neuro-caudal area. The pattern is similar to that expressed in the 3rd vertebra, just more stressed and exaggerated. Furthermore, in the 10th element the enlargement of the neuro-cephalic area is more vertically directed. The dorsal fin ray is wedged (Fig.6) 3 4 Fig th Abdominal vertebrae Fig th Abdominal vertebrae 5 Fig.6. Dorsal Fin ray DISCUSSION: Outstanding position of the seahorses within the framework of the teleostean variability provides a very good opportunity to analyze a discrete and well delineated evolutionary casestudy. H.kuda displays a unique structural arrangement of the axial skeleton compared to the basic organization of teleosts, with changes in the relationships of the metameric elements (Rauther,1925, Hale, 1996). The tail apomorphy in seahorses differ from species to species and this diversity brings about their slight differences in their locomotion.the vertebral series in H. kuda shows variations both in size and shape. Concerning size, there is a general decrease from the cephalic to the caudal extremes. Nevertheless, changes are not always gradual a reduction 67
6 is evident mostly after the dorsal elements, and a homogeneous decrease in size is only displayed in the caudal set. The structural configuration of the vertebral series accounts for the vertical locomotion and posture, while the caudal morphology supports the prehensile properties of the tail. This study is aimed at characterizing the vertebral series in H. kuda testing the patterns of shape variation through a morphometric approach. Using morphometrics it is possible to recognize this taxon. These groups can be conventionally defined according to their position and role along the vertebral sequence. Seahorse body posture and dorso-ventral tail bending ability probably opened to a series of new ecological opportunities that have been revealed successful and possibly involved in the high speciation rate of the genus. ACKNOWLEDGEMENT: The authors are thankful to the Ministry of Earth Science; Government of India for providing financial supports for our research work and as well the director, CAS in Marine Biology, Annamalai University for rendering a great support. REFERENCES: 1. Adams, D. C.; Rohlf, F. J. & Slice, D. E Geometric morphometrics: ten years of progress following the"revolution". Ital. J. Zool., 71(1):5-16, 2. Ashley-Ross, M. A Mechanical properties of the dorsal fin muscle of seahorse (Hippocampus) and pipefish (Syngnathus). J. Exp. Zool., 293(6):561-77, 3. Blake, R. W On seahorse locomotion. J. Marine Biol. Assoc., 56: Blake RW Undulatory median fin propulsion of two teleosts with different modes of life. Can J Zool 58: Bookstein, F. L. Marcus, L.; Corti, M.; Loy, A.; Naylor, G. J. P. & Slice,D 1996.Combining the tools of geometric morphometrics. In: Advances in morphometrics. Eds.. Plenum Press, New York,. 6. Breder, C. M. & Edgerton, H. E An analysis of the locomotion. of the seahorse, Hippocampus, by means of high speed. Cinematography. Ann. N. Y. Acad. Sci., 43:145-72, 7. Dawson, C. E Indo-Pacific pipe fishes (Red Sea to the Americas). Gulf Coast Research Laboratory. Ocean Springs, Mississippi, 8. Hale, M. E Mechanisms of bending and holding in seahorses and pipefishes (Teleostei: Syngnathidae). Am. Zool., 33:120A. 9. Hale, M. E Functional morphology of ventral tail bending and prehensile abilities of the seahorse, Hippocampus kuda. J. Morphol., 227: Lewis, E. B A gene complex controlling segmentation in Drosophila. Nature, 276(5688):565-70, 68
7 11. Lourie, S. A.; Vincent, A. C. J. & Hall, H. J Seahorses: an identification guide to the world's species and their conservation. Project Seahorse, London, 12. Lindsey CC Form, function, and locomotory habits in fish. In: Hoar WS, Randall DJ, editors. Fish physiology. New York: Academic Press. Pp: Marcus, L. F.; Corti, M.; Loy, A.; Naylor, G. J. P. & Slice, D. E Advances in Morphometrics. Plenum Press, New York. 14. Nelson, J. S Fishes of the world. 3rd. Ed. John Wiley & Sons, New York, 15. Rauther, M Die Syngnathiden des Golfes von Neapel. Friedlander & Sohn, Berlin, 16. Rohlf, F. J. & Marcus, L. F A Revolution in Morphometrics. Trends Ecol. Evol., 8:129-32, 17. Videler, J. J Fish swimming. Chapman & Hall, London,. 18. Vincent, A. C. J Seahorses exhibit conventional sex roles in mating competition, despite male pregnancy. Behavior, 128(1-2):135-51, FIGURE LEGENDS: Figure 1 Figure.2 Figure.3 Figure.4 Figure.5 Figure.6 - Morphology of Hippocampus kuda (male) - Skeletal morphology of H.kuda - Cephalic part of H.kuda - 12th Abdominal vertebrae - 19th Abdominal vertebrae - Dorsal Fin ray 69
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