Skip to main content
Log in

Ectopic ossicles associated with metacercariae of Apophallus brevis (Trematoda) in yellow perch, Perca ftavescens (Teleostei): development and identification of hone and chondroid bone

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

This paper describes the development and tissues in mineralized ossicles in the musculature of Perca flavescens infected with metacercariae of the trematode Apophallus brevis. Analysis involved light microscopy, transmission and scanning electron microscopy, X-ray scanning electron microprobe analysis, and tetracycline labelling. Two to 14 days post-infection, fibroblast-like host cells stream towards the parasite cyst forming a fusiform cellular capsule. By 14 days post-infection the capsule differentiates into an inner hypertrophied layer, an extensive middle layer of fibroblast-like cells, and a thin outer layer of flattened fibroblast-like cells forming a fibrous sheath at the capsule/muscle interface. From 21–35 days post-infection, a bony tissue is deposited periosteally in an equatorial ring around the cyst. With time, additional tissue is secreted over the ring increasing its thickness and advancing the matrix front towards the poles of the ossicle. Plump osteoblast-like cells cover the developing ossicle and may become trapped within the matrix in lacunae encapsulated by collagen. By 63 days post-infection, medium-sized ossicles are morphologically similar to large cysts from perch captured in the wild; ovoid with two polarized canals, but lacking acellular or lamellar bone-like tissue. Mineralized ossicles contain calcium, phosphorus and oxygen. Large ossicles retrieved from perch given multiple doses of tetracycline revealed discrete fluorescent bands, indicative of incremental growth. Fully developed ossicles are composed of two skeletal tissues, an inner region of chondroid bone and an outer region of acellular, lamellar bone.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Anderson HC (1976) Osteogenetic epithelial-mesenchymal cell interactions. Clin Orthop 119:211–224

    Google Scholar 

  • Ben-Ami Y, Mark K von der, Franzen A, Bernard B de, Lunazzi GC, Silbermann M (1993) Transformation of fetal secondary cartilage into embryonic bone in organ cultures of human mandibular condyles. Cell Tissue Res 271:317–322

    Google Scholar 

  • Benjamin M (1988) Mucochondroid (mucous connective) tissues in the heads of teleosts. Anat Embryol 178:461–474

    Google Scholar 

  • Benjamin M (1989a) The development of hyaline-cell cartilage in the head of the black molly, Poecilia sphenops. Evidence for secondary cartilage in a teleost. J Anat 164:145–154

    Google Scholar 

  • Benjamin M (1989b) Hyaline-cell cartilage (chondroid) in the heads of teleosts. Anat Embryol 179:285–303

    Google Scholar 

  • Benjamin M (1990) The cranial cartilages of teleosts and their classification. J Anat 169:153–172

    Google Scholar 

  • Benjamin M, Ralphs JR (1991) Extracellular matrix of connective tissues in the heads of teleosts. J Anat 179:137–148

    Google Scholar 

  • Benjamin M, Ralphs FR, Eberewariye OS (1992) Cartilage and related tissues in the trunk and fins of teleosts. J Anat 181:113–118

    Google Scholar 

  • Beresford WA (1981) Chondroid bone, secondary cartilage and metaplasia. Urban & Schwarzenberg, Baltimore

    Google Scholar 

  • Blazer VS, Gratzek JB (1984) Cartilage proliferation in response to metacercarial infections of fish gills. In: Snieszko SF (ed) Commemorative fish disease workshop. Arkansas, p 30

  • Boros DL, Lande MA (1983) Induction of collagen synthesis in cultured human fibroblasts by live Schistosome mansoni eggs and soluble egg antigens (SEA). J Trop Med Hyg 32:78–82

    Google Scholar 

  • Chandler AC (1951) Studies on metacercariae of Perca flavescens in Lake Itasca, Minnesota. Am Mid Nat 45:711–721

    Google Scholar 

  • Craig JF (1987) The biology of perch and related fish. Timber Press, Portland, Oregon

    Google Scholar 

  • Ekanayake S, Hall BK (1987) The development of acellularity of the vertebral bone of the Japanese medaka, Oryzias latipes (Teleostei; Cyprinidontidae). J Morphol 193:253–261

    Google Scholar 

  • Ekanayake S, Hall BK (1988) Ultrastructure of the osteogenesis of acellular vertebral bone in the Japanese medaka, Oryzias latipes (Teleostei, Cyprinidontidae). Am J Anat 182:241–249

    Google Scholar 

  • Ellender G, Feik SF, Carach BJ (1988) Periosteal structure and development in a rat caudal vertebra. J Anat 158:173–187

    Google Scholar 

  • Evans DL, Gratzek JB (1989) Immune defense mechanisms in fish to protozoan and helminth infections. Am Zool 29:409–418

    Google Scholar 

  • Ferguson HW (1989) Systemic pathology of fish. Iowa State University Press, Iowa

    Google Scholar 

  • Glowacki J, Cox KA, O'Sullivan J, Wilkie D, Deftos LJ (1986) Osteoblasts can be induced in fish having an acellular bony skeleton. Proc Natl Acad Sci USA 83:4104–4107

    Google Scholar 

  • Gray DH, Speak KS (1979) The control of bone induction in soft tissues. Clin Orthop 143:245–230

    Google Scholar 

  • Goret-Nicaise M (1984) Identification of collagen type I and type II in chondroid tissue. Calcif Tissue Int 36:682–689

    Google Scholar 

  • Goret-Nicaise M, Dhem A (1987) Electron microscopic study of chondroid tissue in the cat mandible. Calcif Tissue Int 40:219–223

    Google Scholar 

  • Hall BK (1978) Developmental and cellular skeletal biology. Academic Press, New York

    Google Scholar 

  • Hall BK (1983) Embryogenesis: cell-tissue interactions. Skeletal Res 2:53–87

    CAS  Google Scholar 

  • Hall BK (1984) Development processes underlying the evolution of cartilage and bone. Symp Zool Soc London 52:155–176

    Google Scholar 

  • Hall BK (1987) Earliest evidence of cartilage and bone development in embryonic life. Clin Orthop 225:225–272

    Google Scholar 

  • Hall BK (1988) The embryonic development of bone. Am Sci 174–177

  • Hall BK (1990) Bone, vol 1. The osteoblast and osteocyte. Telford, Caldwell

    Google Scholar 

  • Hanken J, Wassersug R (1981) A new double-stain technique reveals the nature of “hard” tissues. Funct Photo 16:22–26

    CAS  PubMed  Google Scholar 

  • Harjes K, Collier B, Tavassoli M (1986) The developmental features of marrow stroma in ectopic bone marrow implants. Scanning Microsc 111:1057–1061

    Google Scholar 

  • Huysseune A (1986a) Late skeletal development at the articulation between upper pharyngeal jaws and neurocranial base in the fish, Astatotilapia elegans, with the participation of a chondroid form of bone. Am J Anat 177:119–137

    Google Scholar 

  • Huysseune A (1986b) Chondroid bone on the upper pharyngeal jaws and neurocranial base in the adult fish Astatotilapia elegans. Am J Anat 177:527–535

    Google Scholar 

  • Huysseune A (1989) Morphogenetic aspects of the pharyngeal jaws and neurocranial apophysis in postembryonic Astatotilapia elegans (Trewavas 1933) (Teleostei: Cichlidae). Med K Acad Wet, Lett Schone Kunsten Bel, K Wet 51:11–35

    Google Scholar 

  • Huysseune A, Sire J-Y (1990) Ultrastructural observations on chondroid bone in the teleost fish Hemichromis bimaculatus. Tissue Cell 22:371–383

    Google Scholar 

  • Huysseune A, Verraes W (1986) Chondroid bone on the upper pharyngeal jaws and neurocranial base in the adult fish Astatotilapia elegans. Am J Anat 177:527–535

    Google Scholar 

  • Huysseune A, Verraes W (1990) Carbohydrate histochemistry of mature chondroid bone in Astatotilapia elegans (Teleostei, Cichlidae) with a comparison to acellular bone and cartilage. Ann Sci Nat Zool Biol Anim 11:29–43

    Google Scholar 

  • Koskinen KP, Kanwar YS, Sires B, Veis A (1985) An electron microscopic demonstration of induction of chondrogenesis in neonatal rat muscle outgrowth cells in monolayer cultures. Connect Tissue Res 14:141–158

    Google Scholar 

  • McLean FC, Urist MR (1968) Bone. Fundamentals of the physiology of skeletal tissue, 3rd edn. University of Chicago Press, Chicago

    Google Scholar 

  • McVicar AH, McLay HA (1985). Tissue response of plaice, haddock and rainbow trout to the systemic fungus Ichthyophorus. In: Ellis AE (ed) Fish and shellfish pathology. Academic Press, London, pp 329–346

    Google Scholar 

  • Mizoguchi I, Nakamura M, Takahashi I, Sasano Y, Kagayama M, Mitani H (1993) Presence of chondroid bone on rat mandibular condylar cartilage. An immunohistochemical study. Anat Embryol 187:9–15

    Google Scholar 

  • Moss ML (1961) Studies of the acellular bone of teleost fish. Acta Anat 46:343–462

    Google Scholar 

  • Nathanson MA, Hay ED (1980) Analysis of cartilage differentiation from skeletal muscle grown on bone matrix. Dev Biol 78:301–331

    Google Scholar 

  • Nilsson OS, Bauer HCF, Brosjo O, Tornkvist H (1986) Influence of indomethacin on induced heterotopic bone formation in rats. Clin Orthop 207:239–245

    Google Scholar 

  • Pantin CFA (1960) Notes on microscopical technique for zoologists. Cambridge University Press, Cambridge

    Google Scholar 

  • Peignoux-Deville J, Bordat C, Vidal B (1989) Demonstration of bone-resorbing cells in elasmobranchs: comparison with osteoclasts. Tissue Cell 21:925–933

    Google Scholar 

  • Pike AW, Burt MDB (1983) The tissue response of yellow perch, Perca flavescens Mitchell to infections with the metacercarial cyst of Apophallus brevis Ransom, 1920. Parasitology 87:393–404

    Google Scholar 

  • Roberts RJ (1975) Melanin-containing cells of teleost fish and their relation to disease. III. Lesions of organ systems, the pathology of fishes. University of Wisconsin Press, Madison, pp 399–428

    Google Scholar 

  • Saunders WB (1974) Medical dictionary, 26th edn. Saunders, Philadelphia

    Google Scholar 

  • Sinclair NR (1972 a) Studies on the heterophyid trematode Apophallus brevis, the “sand-grain grub” of yellow perch (Perca flavescens) I. Redescription and resolution of synonymic conflict with Apophallus imperator Lyster, 1940 and other designations. Can J Zool 50:357–364

    Google Scholar 

  • Sinclair NR (1972b) Studies on the heterophyid trematode Apophallus brevis, the “sand-grain grub” of yellow perch (Perca flavescens) II. The metacercaria: position, structure and composition of the cyst; hosts; geographical distribution and variation. Can J Zool 50:577–584

    Google Scholar 

  • Smith MM, Hall BK (1990) Development and evolutionary origins of vertebrate skeletogenic and odontogenic tissues. Biol Rev 65:277–373

    Google Scholar 

  • Smith MM, Hall BK (1993) A developmental model for evolution of the vertebrate exoskeleton and teeth: the role of cranial and trunk neural crest. Evol Biol 27:387–448

    Google Scholar 

  • Smyth JD, Halton DW (1983) The physiology of trematodes, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Taylor LH (1991) Developmental pathology of ectopic chondroid bone and acellular bone within ossicles of Apophallus brevis, Ransom (Digenia, Heterophyidae) in yellow perch (Perca flavescens, Mitchell). M.Sc. thesis, Dalhousie University, Halifax, NS

    Google Scholar 

  • Taylor LH, Hall BK, Cone DK (1993) Experimental infection of yellow perch (Perca flavescens) with Apophallus brevis (Digenea, Heterophyidae): parasite invasion, encystment and ossicle development. Can J Zool 71:1886–1894

    CAS  PubMed  Google Scholar 

  • Tenenbaum HC (1990) Cellular origins and theories of differentiation of bone-forming cells. In: Hall BK (ed) Bone, vol. 1. The osteoblast and osteocyte. Telford, Caldwell, pp 41–70

    Google Scholar 

  • Triffitt JT (1988) Initiation and enhancement of bone formation. Acta Orthop Scand 58:673–684

    Google Scholar 

  • Urist MR (1973) A bone morphogenetic system in residues of bone matrix in the mouse. Clin Orthop 91:210–220

    Google Scholar 

  • Urist MR, DeLange RJ, Finerman GAM (1983) Bone cell differentiation and growth factors. Science 220:680–686

    Google Scholar 

  • Vaughan JM (1975) The pathology of bone, 2nd edn. 2. Cellular elements of the skeleton. Clarendon Press, Oxford

    Google Scholar 

  • Warren BH (1953) A new type of metacercarial cyst of the genus Apophallus, from the perch, Perca flavescens, in Minnesota. Am Mid Nat 50:397–401

    Google Scholar 

  • Weiss RE, Watabe N (1979) Studies on the biology of fish bone. III Ultrastructure of osteogenesis and resorption in osteocytic (cellular) and anosteocytic (acellular) bones. Calcif Tiss Int 28:43–58

    Google Scholar 

  • Whitfield PJ (1979) The biology of parasitism; an introduction to the study of associating organisms. Arnold, London

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Taylor, L.H., Hall, B.K., Miyake, T. et al. Ectopic ossicles associated with metacercariae of Apophallus brevis (Trematoda) in yellow perch, Perca ftavescens (Teleostei): development and identification of hone and chondroid bone. Anat Embryol 190, 29–46 (1994). https://doi.org/10.1007/BF00185844

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00185844

Key words

Navigation