Reviews in Fish Biology and Fisheries

, Volume 18, Issue 1, pp 47–64 | Cite as

Comparison of the lateral line and ampullary systems of two species of shovelnose ray

Research Paper

Abstract

The anatomical characteristics of the mechanoreceptive lateral line system and electrosensory ampullae of Lorenzini of Rhinobatos typus and Aptychotrema rostrata are compared. The spatial distribution of somatic pores of both sensory systems is quite similar, as lateral line canals are bordered by electrosensory pore fields. Lateral line canals form a sub-epidermal, bilaterally symmetrical net on the dorsal and ventral surfaces; canals contain a nearly continuous row of sensory neuromasts along their length and are either non-pored or pored. Pored canals are connected to the surface through a single terminal pore or additionally possess numerous tubules along their length. On the dorsal surface of R. typus, all canals of the lateral line occur in the same locations as those of A. rostrata. Tubules branching off the lateral line canals of R. typus are ramified, which contrasts with the straight tubules of A. rostrata. The ventral prenasal lateral line canals of R. typus are pored and possess branched tubules in contrast to the non-pored straight canals in A. rostrata. Pores of the ampullae of Lorenzini are restricted to the cephalic region of the disk, extending only slightly onto the pectoral fins in both species. Ampullary canals penetrate subdermally and are detached from the dermis. Ampullae occur clustered together, and can be surrounded by capsules of connective tissue. We divided the somatic pores of the ampullae of Lorenzini of R. typus into 12 pore fields (10 in A. rostrata), corresponding to innervation and cluster formation. The total number of ampullary pores found on the ventral skin surface of R. typus is approximately six times higher (four times higher in A. rostrata) than dorsally. Pores are concentrated around the mouth, in the abdominal area between the gills and along the rostral cartilage. The ampullae of both species of shovelnose ray are multi-alveolate macroampullae, sensu Andres and von Düring (1988). Both the pore patterns and the distribution of the ampullary clusters in R. typus differ from A. rostrata, although a basic pore distribution pattern is conserved.

Keywords

Mechanosensory lateral line Ampullae of Lorenzini Shovelnose rays Electroreception Octavolateralis system 

References

  1. Aadland CR (1992) Anatomical observation and description of the ampullae of Lorenzini in the shortfin mako shark Isurus oxyrinchus. PhD Thesis, Bucknell UniversityGoogle Scholar
  2. Andres KH, von Düring M (1988) Comparative anatomy of vertebrate electroreceptors. Prog Brain Res 74:113–131PubMedCrossRefGoogle Scholar
  3. Bodznick D, Boord RL (1986) Electroreception in chondrichthyes. Central anatomy and physiology. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley and Sons Interscience Publications, pp 225–257Google Scholar
  4. Boord RL, Campbell CBG (1977) Structural and functional organization of the lateral line system of sharks. American Zool 17:431–441Google Scholar
  5. Bullock TH, Szabo T (1986) Introduction. In: Bullock TH, Heiligenberg W (eds) Electroreception. John Wiley and Sons, New York, pp 1–12Google Scholar
  6. Cavanagh RD, Kyne PM, Fowler SL, Musick JA, Bennett MB (eds) (2003) The Conservation status of Australasian chondrichthyans. Report of the IUCN Shark Specialist Group. Australia and Oceania Regional Red List Workshop. The University of Queensland, School of Biomedical Sciences, Brisbane, AustraliaGoogle Scholar
  7. Chu YT, Wen MC (1979) A study of the lateral- line canal system and that of the Lorenzini ampullae and tubules of elasmobranchiate fishes of China. Monograph of Fishes of China, Academic Press, ShanghaiGoogle Scholar
  8. Compagno LJV (1999) Endoskeleton. In: Hamlett WC (ed) Sharks, skates and rays. The biology of elasmobranch fishes. John Hopkins Univ. Press, pp 69–92Google Scholar
  9. Compagno LJV, Last PR (1999) Order Rhinobatiformes. In: Carpenter EK, Niem VH (ed) FAO Species identification guide for fisheries purposes. The living marine resources of the western central Pacific, Vol 3. Batoid fishes, chimaeras and bony fishes part 1 (Elopidae to Linophrynidae). Rome FAO, pp 1397–2068Google Scholar
  10. Coombs S, Montgomery JC (2005) Comparing octavolateralis sensory systems: What can we learn? In: Bullock TH, Hopkins CD, Popper AN, Fay RR (ed) Electroreception. Springer handbook of auditory research, Vol 21. Springer Science + Business Media, Inc., pp 318–359Google Scholar
  11. Culling CFA (1974) Handbook of histopathological techniques. Butterworth and Co, LondonGoogle Scholar
  12. Dijkgraaf S (1963) The functioning and significance of the lateral line organs. Biol Rev 38:51–106PubMedGoogle Scholar
  13. Fishelson L, Baranes A (1998) Morphological and cytological ontogenesis of the ampullae of Lorenzini and the lateral line canals in the Oman shark, Iago omanensis Norman 1939 (Triakidae) from the Gulf of Aqaba, Red Sea. Anatom Rec 252:532–545CrossRefGoogle Scholar
  14. Hueter RE, Mann DA, Maruska KP, Sisneros JA, Demski LS (2004) Sensory biology of elasmobranchs. In: Carrier CC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, pp 325–368Google Scholar
  15. Jorgensen JM (2005) Morphology of electroreceptive sensory organs. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer handbook of auditory research, Vol 21. Springer Science + Business Media, Inc. pp 47–67Google Scholar
  16. Kajiura SM (2000) Head morphology and electrosensory pore distribution of carcharhinid and sphyrnid sharks. Env Biol Fishes 61:125–133CrossRefGoogle Scholar
  17. Kalmijn AJ (1974) The detection of electric fields from inanimate and animate sources other than electric organs. In: Fessard A (ed) (1974) Electroreceptors and other specialized receptors in lower vertebrates. Springer Berlin Heidelberg, pp 147–200Google Scholar
  18. Kasumyan AO (2003) The lateral line in fish: Structure, function and role in behaviour. J Ichthyol 43(Suppl2):S175–S203Google Scholar
  19. Karnovsky MJ (1965) A formaldehyde - glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:137A–138AGoogle Scholar
  20. Kemp NE (1999) Integumentary system and teeth. In: Hamlett WC (ed) (1999) Sharks, skates and rays. The biology of elasmobranch fishes. John Hopkins University Press, pp 43–68Google Scholar
  21. Köhler W, Schachtel G, Proske P (2002) Biostatistik. Eine Einführung für Biologen und Agrarwissenschaftler, Vol 3. Auflage Springer VerlagGoogle Scholar
  22. Kroese AB, Schellart NAM (1992) Velocity- and acceleration sensitive units in the trunk lateral line of the trout. J Neurophysiol 68:2212–2221PubMedGoogle Scholar
  23. Kyne PM, Bennett MB (2002) Reproductive biology of the eastern shovelnose ray, Aptychotrema rostrata (Shaw and Nodder, 1794), from Moreton Bay, Queensland, Australia. Mar Freshwater Res 53:583–589CrossRefGoogle Scholar
  24. Last PR, Compagno LJV, Nakaya K (2004) Rhinobatos nudidorsalis, a new species of shovelnose ray (Batoidea: Rhinobatidae) from the Mascarene Ridge, central Indian Ocean. Ichthyol Res 51:153–158CrossRefGoogle Scholar
  25. Liem KF, Summers AP (1999) Muscular system: Gross anatomy and functional morphology of muscles. In: Hamlett WC (ed) Sharks, skates and rays. The biology of elasmobranch fishes. John Hopkins Univ Press, pp 93–114Google Scholar
  26. Maruska KP (2001) Morphology of the mechanosensory lateral line system in elasmobranch fishes: ecological and behavioural considerations. Env Biol Fishes 60:47–75CrossRefGoogle Scholar
  27. Maruska KP, Tricas TC (2004) Test of the mechanotactile hypothesis: neuromast morphology and response dynamics of mechanosensory lateral line primary afferents in the stingray. J Exp Biol 207:3463–3476PubMedCrossRefGoogle Scholar
  28. McEachran JD, Dunn KA, Miyake T (1996) Interrelationships of the Batoid fishes (Chondrichtyes: Batoidea). In: Stiassney M, Parenti L, Johnson D (eds) Interrelationships of fishes. New York Academic Press, pp 63–83Google Scholar
  29. Murray RW (1962) The response of the ampullae of Lorenzini to electrical stimulation. J Exp Biol 39:119–128 PubMedGoogle Scholar
  30. Murray RW (1974) The ampullae of Lorenzini. In Fessard A (ed) (1974) Electroreceptors and other specialized receptors in lower vertebrates. Springer Berlin Heidelberg, pp 125–146Google Scholar
  31. Norris BW (1929) The distribution and innervation of the ampullae of Lorenzini of the dogfish, Squalus acanthias. Some comparisons with conditions in other plagiostomes and corrections of prevalent errors. J Comp Neurol 47:449–465CrossRefGoogle Scholar
  32. Peach MB (2001) The dorso-lateral pit organs of the Port Jackson shark contribute sensory information for rheotaxis. J Fish Biol 59:696–704CrossRefGoogle Scholar
  33. Peach MB (2003) Inter- and intraspecific variation in the distribution and number of pit organs (Free neuromasts) of sharks and rays. J Morph 256:89–102PubMedCrossRefGoogle Scholar
  34. Raschi WG (1978) Notes on the gross functional morphology of the ampullary system in two similar species of skates, Raja erinacea and R. ocellata. Copeia 1:48–53CrossRefGoogle Scholar
  35. Raschi WG (1984) Anatomical observations on the ampullae of Lorenzini from selected skates and galeoid sharks of the western north Atlantic. PhD Thesis, College of William and Mary in Virginia Google Scholar
  36. Raschi WG (1986) A morphological analysis of the ampullae of Lorenzini in selected skates (Pisces, Rajoidei). J Morphol 189:225–247CrossRefGoogle Scholar
  37. Raschi WG, Mackanos LA (1989) The structure of the ampullae of Lorenzini in Dasyatis garouaensis and its implications on the evolution of freshwater electroreceptive systems. J Exp Zool (Suppl. 2):101–111Google Scholar
  38. Statsoft Inc. (2004) Electronic statistics textbook. Tulsa, Ok. Available via Statsoft web site http://www.statsoft.com/textbook/stathome.html Cited 10 February 2006
  39. Szabo T (1974) Anatomy of the specialized lateral line organs of electroreception. In: Fessard A (ed) Electroreceptors and other specialized receptors in lower vertebrates. Springer Berlin Heidelberg, pp 13–58Google Scholar
  40. Szamier RB, Bennett MVL (1980) Ampullary electroreceptors in the fresh water ray, Potamotrygon. J Comp Physiol 138:225–230CrossRefGoogle Scholar
  41. Tricas TC, Michael SW, Sisneros JA (1995) Electrosensory optimization to conspecific phasing signals for mating. Neurosci Letters 202:129–132CrossRefGoogle Scholar
  42. Tricas TC, New JG (1998) Sensitivity and response dynamics of elasmobranch electrosensory primary afferent neurons to near threshold fields. J Comp Physiol A 182:89–101PubMedCrossRefGoogle Scholar
  43. Waltmann B (1966) Electrical ties and fine structure of the ampullary canals of Lorenzini. Acta physiol Scand 66(Suppl 264):1–60Google Scholar
  44. White WT, Platell ME, Potter IC (2004) Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for source partitioning. Mar Biol 144:439–448CrossRefGoogle Scholar
  45. Whitehead DL (2002) Ampullary organs and electroreception in freshwater C. leucas. J Physiol Paris 96:391–395PubMedCrossRefGoogle Scholar
  46. Wilga CD, Motta PJ (1998) Feeding mechanism of the Atlantic guitarfish Rhinobatos lengtinosus: modulation of kinematic and motor activity. J Exp Biol 201:3167–3184PubMedGoogle Scholar
  47. Wilkens LA, Hofmann MH (2005) Behavior of animals with passive, low-frequency electrosensory systems. In: Bullock TH, Hopkins CD, Popper AN, Fay RR (eds) Electroreception. Springer Handbook of Auditory Research, Vol 21. Springer Science + Business Media, Inc. pp 229–263Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of ZoologyUniversity of ViennaViennaAustria
  2. 2.Centre for Marine StudiesUniversity of QueenslandBrisbane, St LuciaAustralia
  3. 3.Sensory Neurobiology Group, School of Biomedical SciencesUniversity of QueenslandBrisbane, St LuciaAustralia

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