Abstract
The present investigation is the first in Egypt to give histomorphological data about Heterosaccus dollfusi, a rhizocephalan parasitic barnacle of the brachyuran crab Charybdis longicollis, collected from the eastern Mediterranean coast of Egypt at shallow depths (10–20 m). The structure of the mature externa and its male organs are essential for perception of both the taxonomy and reproductive biology of these specialized parasites. We use scanning electron microscopy and histological methods coupled with morphological description to investigate the anatomy of mature externa. The mature externa is distinguished by a visceral mass which comprises the ovary, paired colleteric glands, paired male receptacles and paired receptacle ducts. Attention is focused on the developmental stages of male organs and/or tracing of spermatozoa after settlement of male cypris implantation of the trichogon during fertilization process. For the first time, the lateral tube that connects the left male receptacle with the right, smaller receptacle was observed in sagittal section and illustrated in the diagrammatic figure of male organs. This tube is probably the generator of sperm ribbons. As well, the existence of the spermatozoa inside the lumen of this connecting tube may indicate their free movement between the two receptacles. Moreover, strips of sperm that drag from the sperm ribbon ball, and surround the developing ovules can also be seen in the mantle cavity.
Similar content being viewed by others
References
Alvarez F, Hines AH, Reaka-Kudla ML (1995) Effects of parasitism by the barnacle Loxothylacus panopaei (Gissler) (Cirripedia: Rhizocephala) on growth and survival of the host crab Rhithropanopeus harrisii (Gould) (Brachyura: Xanthidae). J Exp Mar Bio Ecol 192:221–232
Alvarez F, Bortolini J, Høeg JT (2010) Anatomy of virgin and mature externae of Loxothylacus texanus, parasitic on the dark blue crab Callinectes rathbunae (Crustacea: Cirripedia: Rhizocephala: Sacculinidae). J Morphol. https://doi.org/10.1002/jmor.10790
Boschma H (1928) Rhizocephala. Dan Ingolf Exped 3(10):1–52
Boschma H (1931) Die Rhizocephalen der Siboga. Expedition supplement. Siboga Expeditie 31bis:1–67
Boschma H (1933) New species of Sacculinidae in the collection of the United States National Museum. Tijdschr Ned Dierkd Ver 3:219–241
Boschma H (1957) Heterosaccus indicus, sp. nov., a rhizocephalan parasite of the crab Portunus pelagicus (L.). Ann Biol 2:1–20
Boschma H (1960) A rhizocephalan parasite of the crab Charybdis hoplites (Wood-Mason). Crustaceana 1(58):67
Boyko CB, Boxshall G (2018) World list of Rhizocephala. Heterosaccus Smith, 1906. Accessed through: world register of marine species at: http://www.marinespecies.org/aphia.php?p=taxdetails&id=234070. Accessed 10 Aug 2018
Bresciani J, Høeg JT (2001) Comparative ultrastructure of the root system in Rhizocephalan barnacles (Crustacea: Cirripedia: Rhizocephala). J Morphol. https://doi.org/10.1002/jmor.1039
Chan BKK (2004) First record of the parasitic barnacle Sacculina scabra Boschma 1931 (Crustacea: Cirripedia: Rhizocephala) infecting the shallow water swimming crab Charybdis truncata. Raffles B Zool 52(2):449–453
Delage Y (1884) Evolution de la Sacculine (Sacculina carcini Thomps.), Crustace endoparasite de l’ordren ouveaud es Kentrogonides. Arch Zool Exp Gen 2(2):417–736
Diechmann M, Høeg JT (1990) Boschmaella japonica, new species, a parasite on the barnacles Chthamalus challengeri and Balanus amphitrite amphitrite from Japan (Crustacea: Cirripedia: Rhizocephala: Chthamalophilidae). Acta Zool 71:173–175
Galil BS, Lützen J (1995) Biological observations on Heterosaccus dollfusi Boschma (Cirripedia: Rhizocephala), a parasite of Charybdis longicollis Leene (Decapoda: Brachyura), a lessepsian migrant to the Mediterranean. J Crustacean Biol 15:659–670
Galil BS, Lützen J (1998) Jeopardy: host and parasite lessepsian migrants from the Mediterranean coast of Israel. J Nat Hist 32:1549–1551
Glenner H, Hebsgaard MB (2006) Phylogeny and evolution of life history strategies of the parasitic barnacles (Crustacea, Cirripedia, Rhizocephala). Mol Phylogenet Evol. https://doi.org/10.1016/j.ympev.2006.06.004
Glenner H, Høeg JT, O´Brien JJ, Sherman TD (2000) The invasive vermigon stage in the parasitic barnacles Loxothylacus texanus and L. panopaei (Sacculinidae): closing of the rhizocephalan life cycle. Mar Biol 136:249–257. https://doi.org/10.1007/s002270050683
Glenner H, Thomsen PF, Rybakov AV, Galil BS, Høeg JT (2008) The phylogeny of rhizocephalan parasites of the genus Heterosaccus using molecular and larval data (Cirripedia: Rhizocephala: Sacculinidae). Isr J Ecol Evol 54:223–238
Høeg JT (1982) The anatomy and development of the rhizocephalan barnacle Clistosaccus paguri to its host Pagurus bernhardus (L.). J Exp Mar Biol Ecol 58:87–125
Høeg JT (1985) Male cypris settlement in Clistosaccus paguri Lilljeborg (Crustacea: Cirripedia: Rhizocephala). J Exp Mar Biol Ecol 89:221–235
Høeg JT (1987) Male cypris metamorphosis and a new male larval form, the trichogon, in the parasitic barnacle Sacculina carcini (Crustacea: Cirripedia: Rhizocephala). Philos Trans R Soc Lond B Biol Sci 317:47–63
Høeg JT (1991) Functional and evolutionary aspects of the sexual system in the Rhizocephala (Crustacea: Thecostraca: Cirripedia). In: Bauer RT, Martin JW (eds) Crustacean sexual biology. Columbia University Press, New York, pp 208–227
Høeg JT (1992) Rhizocephala. In: Harrison FW, Humes AG (eds) Microscopic anatomy of invertebrates. Crustacea, vol 9. Wiley, New York, pp 313–345
Høeg JT (1995) The biology and life cycle of the Rhizocephala (Cirripedia). J Mar Biol Assoc UK 75:517–550
Høeg JT, Lützen J (1995) Life cycle and reproduction in the Cirripedia Rhizocephala. Oceanogr Mar Biol An 33:427–485
Høeg JT, Lützen J (1996) Rhizocephala. In: Forest J (ed) Traité de Zoologie, Crustacés, Généralités (suite) et Systématique, vol 7, vol 2. Masson et Cie, Paris, pp 541–568
Høeg JT, Kapel CM, Thor P, Webster P (1990) The anatomy and sexual biology of Boschmaella japonica, an akentrogonid rhizocephalan parasite on barnacles from Japan (Crustacea: Cirripedia: Rhizocephala). Acta Zool 71:177–188
Høeg JT, Glenner H, Shields J (2005) Cirripedia Thoracica and Rhizocephala (barnacles). In: Rohde K (ed) Marine parasites. CABI Publishing, Wallingford, pp 154–165
Holthuis LB (1961) Report on a collection of Crustacea Decapoda and Stomatopoda from Turkey and the Balkans. Zool Verh 47:1–67
Ichikawa A, Yanagimachi R (1960) Studies on the sexual organization of the Rhizocephala. II. The reproductive function of the larval (cypris) males of Peltogaster and Sacculina. Annot Zool Jpn 33:42–56
Innocenti G, Galil BS (2011) Live and let live: Invasive host, Charybdis longicollis (Decapoda: Brachyura: Portunidae), and invasive parasite, Heterosaccus dollfusi (Cirripedia: Rhizocephala: Sacculinidae). In: Galil BS et al (eds) In the wrong place—alien marine Crustaceans: distribution, biology and impacts, invading nature. Springer, Dordrecht, p 6
Innocenti G, Galil BS, Yokeş MB, Diamant A, Goren M (2009) Here and there: a preliminary note on the prevalence of an alien Rhizocephalan parasite at the southern and northern limits of its introduced range. J Parasitol Res 95(6):1387–1390
Kruse I, Hare MP (2007) Genetic diversity and expanding nonindigenous range of the rhizocephalan Loxothylacus panopaei parasitizing mud crabs in the western North Atlantic. J Parasitol Res 93(3):575–582
Lange S (2002) The colleteric glands in Sacculinidae (Crustacea, Cirripedia, Rhizocephala): an ultrastructural study of ovisac secretion. Contrib Zool 70:229–242
Leene JE (1938) The Decapoda Brachyura of the Siboga Expedition. VII. Brachygnatha Portunidae Siboga-Expeditie 31:1–156
Lützen J, Itani G, Jespersen Å, Hong J-S, Rees D, Glenner H (2016) On a new species of parasitic barnacle (Crustacea: Rhizocephala), Sacculina shiinoi sp. nov., parasitizing Japanese mud shrimps Upogebia spp. (Decapoda: Thalassinidea: Upogebiidae), including a description of a novel morphological structure in the Rhizocephala. Zool Sci 5:44. https://doi.org/10.2108/zs150112
Øksnebjerg B (2000) The Rhizocephala (Crustacea: Cirripedia) of the Mediterranean and Black Seas: taxonomy, biogeography, and ecology. Zool, Isr J. https://doi.org/10.1560/RCLC-NM2U-HV5L-6Q52
Øksnebjerg B, Enzenross R, Enzenross L (1997) First record of Rhizocephala (Crustcea: Cirripedia) from Turkish waters with notes on lessepsian migration. Stutt Beitr Naturkd Serie A (Biologie) 557:1–7
Özcan T, Katağan T (2016) Prevalence of Heterosaccus dollfusi Boschma, 1960 (Rhizocephala: Sacculinidae) on Charybdis longicollis Leene, 1938 (Brachyura: Portunidae) from Iskenderun Bay, Turkey. J Black Sea Medit Environ 22:128–136
Reinhard E (1942) The reproductive function of the complemental males of Peltogaster. J Morphol 70:389–402
Smith G (1906) Rhizocephala. Fauna und Flora des Golfes von Neapel 29:1–123
Thompson JV (1836) Natural history and metamorphosis of an anomalous crustaceous parasite of Carcinus maenas, the Sacculina carcini. Entomol Mag 3:452–456
WoRMS (2018). Rizocephala. http://www.marinespecies.org/aphia.php?p=taxadaetails&id=1109. Accessed 10 Aug 2018
Yanagimachi R, Fujimaki N (1967) Studies on the sexual organization of the Rhizocephala. IV. On the nature of the ‘‘testis” of Thompsonia. Annot Zool Jpn 40:98–104
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Ethical statement
This article does not contain any studies with human participants performed by any of the authors. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This study did not involve endangered or protected species.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Nour Eldeen, M.F., El Gamal, M.M., Abdelsalam, K.M. et al. Histomorphological investigation of the mature externa of Heterosaccus dollfusi (Crustacea, Rhizocephala). Zoomorphology 138, 463–473 (2019). https://doi.org/10.1007/s00435-019-00453-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00435-019-00453-5