External Morphology and Ultrastructure of Tegumental Glands of Aegla platensis (Crustacea, Anomura, Aeglidae) Pleopods: Might They Play A Role in Egg Attachment?

Tainã Gonçalves Loureiro (Marine Lab, Department of Botany and Zoology, Stellenbosch University, Stellenbosch, South Africa)
Mauricio Pereira Almerão (UNILASALLE, Canoas, Brazil)
Maria Cristina Faccioni-Heuser (Department of Morphological Sciences, Federal University of Rio Grande do Sul, Porto Alegre, Brazi)
Georgina Bond-Buckup (Laboratory of Carcinology, Department of Zoology, Federal University of Rio Grande do Sul, Porto Alegre, Brazil)
Paula Beatriz de Araujo (Laboratory of Carcinology, Department of Zoology, Federal University of Rio Grande do Sul, Porto Alegre, Brazi)

Article ID: 806

DOI: https://doi.org/10.30564/re.v1i2.806


Egg incubation on the female abdomen is the parental care behavior observed in aeglids, in which eggs are kept adhered to maternal pleopods and maintained, cleaned and aerated. In A. platensis, egg attachment occurs with the aid of pleopodal setae, which are twisted around their axis in the distal region, forming the funiculus, and pleopodal glands, which are responsible for the production of the adhesive substance that seems to be involved in egg fixation to pleopodal setae. Those glands are acini formed by secretory cells arranged concentrically around a central duct, giving them a rosette appearance. Two types of secretory cells were observed, those that produce electron-lucid vesicles and those having electron-dense ones. Both kinds of vesicles are released in a duct whose opening pore is located on the pleopodal surface and constitute the adhesive substance that coats eggs and pleopodal setae, ensuring egg fixation to the female body and maternal care maintenance. This study investigates the internal and external morphology of Aegla platensis pleopods, to understand the egg attachment process and identify the structures involved in this phenomenon. Three microscopy techniques are used: scanning electron microscopy (SEM), transmission electron microscopy (TEM), and optical microscopy (OM).


Egg incubation; Pleopodal setae; Funiculus; Electron microscopy; Optical microscopy

Full Text:



[1] Hazlett, B. A.. Parental behavior in Decapod Crustacea.. In, S. Rebach and D. W. Dunham (eds), Studies in adaptation. The behavior of higher Crustacea [M]. John Wiley and Sons, New York, 1983: 171–193.

[2] Anger, K.. The biology of decapod crustacean larvae [M]. A.A. Balkema Publishers, Lisse, 2001.

[3] Baeza, J. A., and M. Fernández.. Active brood care in Cancer setosus (Crustacea:Decapoda): The relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Functional Ecology [J]. 2002, 16: 241–251.

[4] Burton, T., B. Knott, D. Judge, P. Vercoe and A. Brearley.. Embryonic and juvenile attachment structures in Cherax cainii (Decapoda: Parastacidae): Implications for maternal care. The American Midland Naturalist [J]. 2007, 157: 127–136.

[5] Clutton-Brock, T. H.. The evolution of parental care [M]. Princeton University Press, Princeton, 1991.

[6] Lereboullet, A.. Recherches sur le mode de fixation des oeufs aux fausses pattes abdominales dans les Ecrevisses. Annales des Sciences Naturelles [J]. IV, 1860, 14: 359–378.

[7] Andrew, E. A.. Egg-laying of crayfish. American Naturalist [J] , 1906, 40: 348–356.

[8] Malaczynska-Suchcitz, Z.. Observations on the manner in which newly hatched crayfish (P. astacus Leach and P. leptodactylus Esch.) are attached to the pleopods of the female. Bulletin de la Societe des Amis des Sciences et des Lettres de Poznań [J]. 1956, 13: 39.

[9] Cheung, T. S.. The development of egg-membranes and egg attachment in the shore crab, Carcinus maenas, and some related decapods. Journal of Marine Biology Association U.K. [J]. 1966, 46: 373–400.

[10] Mason, J. C.. Egg laying in the Western North American crayfish, Pacifastacus trowbridgii (Stimpson) (Decapoda, Astacidae). Crustaceana [J]. 1970, 19: 37–44.

[11] Aiken, D. E., and S. L. Waddy.. Cement gland development, ovary maturation, and reproductive cycles in the American lobster, Homarus americanus. Journal of Crustacean Biology [J]. 1982, 2: 315–327.

[12] Goudeau, M., P. Talbot and R. Harper.. Mechanism of egg attachment stalk formation in the lobster Homarus. Gamete Research [J]. 1987, 18: 279–289.

[13] Johnson, B., and P. Talbot.. Ultrastructural analysis of the pleopod tegumental glands in male and female lobsters, Homarus americanus. Journal of Crustacean Biology [J]. 1987, 7: 288–301.

[14] Talbot, P.. Ovulation, attachment and retention of lobster eggs.. In, A. Wenner and A. Kuris (eds.), Crustacean Issues [C]. Crustacean Egg Production. A. A. Belkema, Rotterdam, 1991, 7: 9–18

[15] Talbot, P., P. Zao.. Secretion at molting by the pleopod tegumental glands of the lobster Homarus americanus (Milne-Edwards). Journal of Crustacean Biology [J]. 1991, 11: 1–9.

[16] Thomas, W. J.. Aspects of egg attachment in Austropotamobius pallipes (Lereboullet, 1858) (Decapoda, Astacidae). Crustaceana [J]. 1991, 61: 287–293.

[17] Bond-Buckup, G., and Santos S. Crustáceos Anomuros de Águas Continenentais- Diversidade e aspectos biológicos. Ciência and Ambiente [J]. 2007, 35: 47–54.

[18] Tudge, C. C.. Endemic and enigmatic: the reproductive biology of Aegla (Crustacea: Anomura: Aeglidae) with observations on sperm structure. Memoirs of Museum Victoria [C]. 2003, 60: 63–70.

[19] Bond-Buckup, G., C. G. Jara, M. Pérez-Losada, L. Buckup and K. A. Crandall.. Global diversity of crabs (Aeglidae: Anomura: Decapoda) in freshwater. Hydrobiologia [J]. 2008, 595: 267–273.

[20] McLaughlin, P. A., R. Lemaitre and K. A. Crandall.. Annotated checklist of anomuran decapod crustaceans of the world (exclusive of the Kiwaoidea and families Chirostylidae and Galatheidae of the Galatheoidea). Part III. Aegloidea. Raffles Bulletin of Zoology [C]. 2010, (Suppl. 23) 131–137.

[21] McLaughlin, P. A., and T. Murray.. Clibanarius fonticola, new species (Anomura: Paguridea: Diogenidae) from a fresh-water pool on Espiritu Santo, Vanuatu. Journal of Crustacean Biology [J]. 1990, 10: 695–702.

[22] Wilkens, H., J. Parzefall and A. Ribowski.. Population biology and larvae of the anchialine crab Munidopsis polymorpha (Galatheidae) from Lanzarote (Canary Islands). Journal of Crustacean Biology [J]. 1990, 10: 667–675.

[23] Burns, J.. The distribution and life history of South American freshwater crabs (Aegla) and their role in trout streams and lakes. Transactions of the American Fisheries Society [J]. 1972, 101: 595–607.

[24] Bond-Buckup, G., and L. Buckup.. A família Aeglidae (Crustacea, Decapoda, Anomura). Arquivos de Zoologia [J]. 1994, 2: 159–346.

[25] Lizardo-Daudt, H. M., Bond-Buckup, G.. Morphological aspects of the embryonic development of Aegla platensis (Decapoda, Aeglidae). Crustaceana [J]. 2003, 76: 13–25.

[26] Swiech-Ayoub, B. P., and S. Masunari.. Biologia reprodutiva de Aegla castro Schmitt (Crustacea, Anomura, Aeglidae) no Buraco do Padre, Ponta Grossa, Paraná, Brasil. Revista Brasileira de Zoologia, 2001, 18: 1019–1030.

[27] Fransozo, A., R. C. Costa, A. L. D. Reigada and J. M. Nakagaki.. Population structure of Aegla castro Schmitt, 1942 (Crustacea: Anomura: Aeglidae) from Itatinga (SP), Brazil. Acta Limnologica Brasiliensia, 2003, 15: 13–20.

[28] López-Greco, L. S., V. Viau, M. Lavolpe, G. Bond-Buckup and E. M. Rodriguez.. Juvenile hatching and maternal care in Aegla uruguayana (Anomura, Aeglidae). Journal of Crustacean Biology [J]. 2004, 24: 309–313.

[29] Martin, J. W., and L. G. Abele.. External morphology of the genus Aegla (Crustacea: Anomura: Aeglidae). Smithsonian Contributions to Zoology [J]. 1988, 453: 1–46.

[30] Almerão, M., M. C. Faccioni-Heuser and G. Bond-Buckup.. An ultrastructural study of tegumental glands of the fifth pereiopods of Aegla platensis (anomura: aeglidae). Journal of Crustacean Biology [J]. 2007, 27: 529–533.

[31] Reynolds, E. S.. The use of lead citrate at high pH as an electron opaque stain in electron microscopy. Journal of Cell Biology [J]. 1963, 17: 208–212.

[32] Martin, J. W., and B. E. Felgenhauer.. Grooming behaviour and the morphology of grooming appendages in the endemic South American crab genus Aegla (Decapoda, Anomura, Aeglidae). Journal of Zoology [J]. 1986, 209: 213–224.

[33] Jacques, F.. The setal system of crustaceans: Types of setae, groupings, and functional morphology, pp.1–13. In, B. E. Felgenhauer, L. Watling and A. B. Thistle (eds.), Functional morphology of feeding and grooming in Crustacea. Crustacean Issues [C]. A.A. Balkema, Rotterdam, 1989, 6.

[34] Watling, L.. A classification system for crustacean setae based on the homology concept. In, F. R. Schram (ed.), Functional morphology of feeding and grooming in Crustacea. Crustacean Issues [C]. 1989, 6: 15–26.

[35] Teodósio, E. A. F. M. O., and S. Masunari.. Description of first two juvenile stages of Aegla schmitti Hobbs III, 1979 (Anomura: Aeglidae). Nauplius [J]. 2007, 15: 73–80.

[36] Fisher, W. S., and W. H. Jr. Clark.. Eggs of Palaemon macrodactylus: I. Attachment to the pleopods and formation of the outer investment coat. The Biological Bulletin [J]. 1983, 164: 189–200.

[37] Pawlos, D., A. Korzelecka-orkisz, E. Rosciszewska and K. Formicki.. Egg case ultrastructure in the narrow-clawed crayfish Astacus leptodactylus Eschscholtz, 1823 (Decapoda, Astacidae). Crustaceana [J]. 2011, 84: 623–633.

[38] Rabalais, N. N.. Egg production in crabs with abbreviated development. Ln, A. Wenner and A. Kurls (eds.), Crustacean egg production [M]. Rotterdam, A.A.Balkema, 1991: 217–234.

[39] Scholtz, G.. Phylogeny and evolution. In, D. m. Holdich (ed.), Biology of freshwater crayfish [M]. Blackwell Science, Oxford, 2002: 30–52.

[40] Vogt, G.. Abbreviation of larval development and extension of brood care as key features of the evolution of freshwater Decapoda. Biological Reviews of the Cambridge Philosophical Society [J]. 2013, 88: 81–116.

[41] Jalihal, D. R., K. N. Sankolli, S. Shenoy.. Evolution of larval developmental patterns and the process of freshwaterization in the prawn genus Macrobrachium Bate, 1868 (Decapoda, Palaemonidae). Crustaceana [J]. 1993, 65: 365–376.

[42] Hancock, M. A.. The relationship between egg size and embryonic and larval development in the freshwater shrimp Paratya australiensis (Decapoda: Atyidae). Freshwater Biology [J]. 1998, 39: 715–723.

[43] Bauer, R. T.. Grooming behavior and morphology in the decapod Crustacea. Journal of Crustacea Biology [J]. 1981, 1: 153–173.

[44] Saigusa, M.. A substance inducing the loss of premature embryos from ovigerous crabs. The Biological Bulletin [J]. 1994, 186:81-89.

[45] Saigusa, M.. Bioassay and preliminary characterization of ovigerous-hair stripping substance (OHSS) in hatch water of crab larvae. The Biological Bulletin [J]. 1995, 189: 175–184.

[46] Saigusa, M., M. Terajima and M. Yamamoto.. Structure, formation, mechanical properties, and disposal of the embryo attachment system of an estuarine crab, Sesarma haematocheir. The Biological Bulletin [J]. 2002, 203: 289–306.

[47] Andrew, E. A.. Breeding habits of crayfish. American naturalist [J]. 1904, 38: 165–206.

[48] Yonge, C. M.. The nature and significance of the membranes surrounding the developing eggs of Homarus vulgaris and other Decapoda. In: Proceedings of the Zoological Society of London [J]. 1937, 107: 499–517.

[49] Silberbauer, B. I.. The biology of the South African rock lobster Joasus lalandii (H. Milne Edwards). Developmental, Investment and Reproductive Diversity in Fish South African [J]. 1971, 92: l–70.

[50] Goudeau, M., and F. Lachaise.. Fine structure and secretion of the capsule enclosing the embryo in a crab (Carcinus maenas (L.)). Tissue and Cell [J]. 1980, 12: 287–308.

[51] Goudeau, M., and J. Becker.. Fertilization in a crab. II. Cytological aspects of the cortical reaction and fertilization envelope elaboration. Tissue and Cell [J]. 1982, 14: 273–282.

[52] Goudeau, M.. Structure of the egg funiculus and deposition of embryonic envelopes in a crab. Tissue and Cell [J]. 1983, 15: 47–62.

[53] Felgenhauer, B. E.. External Anatomy and Integumentary Structures, In, F. W. Harrison, and G. A. Humes (eds.), Microscopic Anatomy of Invertebrates[M]. Wiley-Liss, New York, 1991: 7–43.

[54] Talbot, P., and D. Demers.. Tegumental glands of Crustacea. In, M. N. Horst and J. A. Freeman (eds.), The crustacean integument: morphology and biochemistry [M]. CRC Press, Boca Raton, 1993: 151–191.

[55] Yonge, C. M.. On the nature and permeability of chitin. I.–The chitin lining the foregut of Decapod Crustacea and the function of the tegumental glands. Proceedings of the Royal Society of London. Series B, Containing Papers of a Biological Character [C]. 1932, 111: 298–329.

[56] Lang, D., and C. M. Yonge.. The function of the tegumental glands in the statocyst of Homarus vulgaris. Journal of the Marine Biological Association of the U. K.[J]. 1935, 20: 333.

[57] Babu, D., K. Rao, K. Shyamasundari and D. Umadevi.. Histochemistry of the cuticle of the crab Menippe rumphii (Fabricius) (Crustacea: Brachyura) in relation to moulting. Journal of Experimental Marine Biology and Ecology [J]. 1985, 88: 129–144.

[58] Beninger, P. G., and R. Larocque.. Gonopod tegumental glands: a new accessory sex gland in the Brachyura. Marine Biology [J]. 1998, 132: 435–444.

[59] Tudge, C. C., and R. Lemaitre. . Studies of male sexual tubes in hermit crabs (Crustacea, Decapoda, Anomura, Paguroidea) II. Morphology of the sexual tube in the land hermit crabs, Coenobita perlatus and C. clypeatus (Coenobitidae). Crustacean Research [J]. 2006, 6: 121–131.

[60] Doughtie, D. G., and K. R. Rao.. Rosette glands in the gills of the grass shrimp, Palaemonetes pugio. I. Comparative morphology, cyclical activity, and innervation. Journal of Morphology [J]. 1982, 171: 41–67.

[61] Ikeda, H., Y. Hirano and M. Saigusa.. A pair of rosette glands in the embryo and zoeal larva of an estuarine crab, Sesarma haematocheir, and classification of the tegumental glands in the embryos of other crabs. Journal of Morphology [J]. 2004, 259: 55–68.

[62] Alberts, B., D. Bray, J. Lewis, M. Raff, K. Roberts and J. D. Watson.. Molecular Biology of the Cell [M]. Garland Publishing, New York, 1994.

[63] Stevenson JR, Schneider RP. Tyrosinase activity of organs containing tegumental glands in the crayfish. Journal of Experimental Zoology [J], 1962, 150: 17–25.

[64] Bushmann, P. J., and J. Atema.. Nephropore rosette glands of the lobster Homarus americanus: Possible sources of urine pheromones. Journal of Crustacean Biology [J]. 1996, 16: 221–231.

[65] Alexander, C. G.. Tegumental glands in the paragnaths of Palaemon serratus (Crustacea: Natantia). Journal of the Marine Biology Association UK[J]. 1989, 69: 53–64.

[66] McKenzie, L., and C. Alexander.. Mucus-secreting glands in the paragnaths and second maxillipeds of the Banana Prawn, Penaeus merguiensis de Man. Marine and Freshwater Research [J]. 1989, 40: 669–677.

Copyright © 2019 Tainã Gonçalves Loureiro, Mauricio Pereira Almerão, Maria Cristina Faccioni-Heuser, Georgina Bond-Buckup, Paula Beatriz de Araujo

Creative Commons License
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.