Hostname: page-component-848d4c4894-mwx4w Total loading time: 0 Render date: 2024-06-24T09:39:57.345Z Has data issue: false hasContentIssue false
  • English
  • Français

Patterns of trunk spine growth in two congeneric species of acanthocephalan: investment in attachment may differ between sexes and species

Published online by Cambridge University Press:  06 February 2012

JESÚS S. HERNÁNDEZ-ORTS ,
JUAN T. TIMI ,
JUAN A. RAGA ,
M. GARCÍA-VARELA ,
ENRIQUE A. CRESPO  and
FRANCISCO J. AZNAR
JESÚS S. HERNÁNDEZ-ORTS
Affiliation:
Cavanilles Institute of Biology and Evolutionary Biology, University of Valencia, Calle Catedrático José Beltrán 2, E-46980, Paterna, Valencia, Spain
JUAN T. TIMI
Affiliation:
Laboratorio de Parasitología, Instituto de Investigaciones Marinas y Costeras (IIMyC), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata – Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
JUAN A. RAGA
Affiliation:
Cavanilles Institute of Biology and Evolutionary Biology, University of Valencia, Calle Catedrático José Beltrán 2, E-46980, Paterna, Valencia, Spain
M. GARCÍA-VARELA
Affiliation:
Departamento de Zoología, Instituto de Biología, Universidad Nacional Autónoma de México, D.F., México
ENRIQUE A. CRESPO
Affiliation:
Centro Nacional Patagónico, CONICET, Boulevard Brown 3600 (9120), Puerto Madryn, Chubut, Argentina
FRANCISCO J. AZNAR*
Affiliation:
Cavanilles Institute of Biology and Evolutionary Biology, University of Valencia, Calle Catedrático José Beltrán 2, E-46980, Paterna, Valencia, Spain
*
*Corresponding author: Cavanilles Institute of Biodiversity and Evolutionary Biology, University of Valencia, CalleCatedrático José Beltrán N. 2, 46980, Paterna Valencia, Spain. Tel: +34 963543657. Fax +34 963543733. E-mail: Francisco.Aznar@uv.es
Get access Rights & Permissions [Opens in a new window]

Summary

Acanthocephalans have evolved a hooked proboscis and some taxa have trunk spines to attach to their definitive hosts. These structures are generated before being used, thus a key question is how investment in attachment could optimally be allocated through the ontogeny. The number and arrangement of hooks and spines are never modified in the definitive host, but it is unclear whether these structures grow during adult development. A comparison of the size of trunk spines between cystacanths and adults of Corynosoma cetaceum and C. australe indicated that spines grow in both species, but only in females, which also had significantly larger spines than males. This sexual dimorphism did not result from pure allometry because the body of females was smaller, and did not grow more than that of males. However, having a longer lifespan, females would need to withstand the extreme flow conditions prevailing in marine mammals for longer, inducing different investment and development schedules for spines. Patterns of spine growth also differed between species: fore-trunk spines grew in both species, but hind-trunk spines did only in C. cetaceum. In conclusion, investment strategies on attachment may differ, not only between congeneric species of acanthocephalan, but also between sexes of the same species.

Keywords

AcanthocephalaCorynosoma australeCorynosoma cetaceumtrunk spineinvestment strategyontogenyattachment
Type
Research Article
Information
Parasitology , Volume 139 , Issue 7 , June 2012 , pp. 945 - 955
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amin, O. M., Heckmann, R. A., Mesa, R. and Mesa, E. (1995). Description and host relationships of cystacanths of Polymorphus spindlatus (Acanthocephala: Polymorphidae) from their paratenic fish hosts in Peru. Journal of Helminthology 62, 249–253.Google Scholar
Amin, O. M., Heckmann, R. A. and Van Ha, N. (2004). On the immature stages of Pallisentis (Pallisentis) celatus (Acanthocephala: Quadrigyridae) from occasional fish hosts in Vietnam. The Raffles Bulletin of Zoology 52, 593–598.Google Scholar
Amin, O. M. (1986). Acanthocephala from Lake Fishes in Wisconsin: Morphometric Growth of Neoechinorhynchus cylindratus (Neoechinorhynchidae) and taxonomic implications. Transactions of the American Microscopical Society 105, 375–380.CrossRefGoogle Scholar
Amin, O. M. (1987). Acanthocephala from Lake Fishes in Wisconsin: Morphometric growth of Pomphorhynchus bulbocolli (Pomphorhynchidae). Journal of Parasitology 73, 806–810.CrossRefGoogle Scholar
Aznar, F. J., Berón-Vera, B., Crespo, E. A. and Raga, J. A. (2002 b). Presence of genital spines in a male Corynosoma cetaceum Johnston and Best, 1942 (Acanthocephala). Journal of Parasitology 88, 403–404. doi: 10.1645/0022-3395(2002)088[0403:POGSIA]2.0.CO;2.CrossRefGoogle Scholar
Aznar, F. J., Bush, A. O., Balbuena, J. A. and Raga, J. A. (2001). Corynosoma cetaceum in the stomach of Franciscanas, Pontoporia blainvillei (Cetacea): An exceptional case of habitat selection by an acanthocephalan. Journal of Parasitology 87, 536–541.CrossRefGoogle ScholarPubMed
Aznar, F. J., Bush, A. O., Fernández, M. and Raga, J. A. (1999 a). Constructional morphology and mode of attachment of the trunk of Corynosoma cetaceum (Acanthocephala: Polymorphidae). Journal of Morphology 241, 237–249.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
Aznar, F. J., Bush, A. O. and Raga, J. A. (1999 b). Polymorphus arctocephali Smales, 1986, a synonym of Corynosoma cetaceum Johnston & Best, 1942 (Acanthocephala: Polymorphidae). Systematic Parasitology 44, 59–70. doi: 10.1023/A:1006161620990.CrossRefGoogle ScholarPubMed
Aznar, F. J., Bush, A. O. and Raga, J. A. (2002 a). Reduction and variability of trunk spines in the acanthocephalan Corynosoma cetaceum: the role of physical constraints on attachment. Invertebrate Biology 121, 104–114. doi: 10.1111/j.1744-7410.2002.tb00051.x.CrossRefGoogle Scholar
Aznar, F. J., Cappozzo, H. L., Taddeo, D., Montero, F. E. and Raga, J. A. (2004). Recruitment, population structure, and habitat selection of Corynosoma australe (Acanthocephala) in South American fur seals, Arctocephalus australis, from Uruguay. Canadian Journal of Zoology 82, 726–733. doi: 10.1139/Z04-044.CrossRefGoogle Scholar
Aznar, F. J., Hernández-Orts, J., Suárez, A. A., García-Varela, M., Raga, J. A. and Cappozzo, H. L. (2012). Assessing host-parasite specificity through coprological analysis: a case study with species of Corynosoma (Acanthocephala: Polymorphidae) from marine mammals. Journal of Helminthology. doi: 10.1017/S0022149X11000149.CrossRefGoogle ScholarPubMed
Aznar, F. J., Pérez-Ponce de León, G. and Raga, J. A. (2006). Status of Corynosoma (Acanthocephala: Polymorphidae) based on anatomical, ecological, and phylogenetic evidence, with the erection of Pseudocorynosoma n. gen. Journal of Parasitology 92, 548–564. doi: 10.1645/GE-715R.1.CrossRefGoogle ScholarPubMed
Castro, M. and Martínez, R. (2004). Process of the development of Corynosoma obtuscens (Acanthocephala: Polymorphidae) in Canis familiaris and its possible involvement in public health. Parasitología Latinoamericana 59, 26–30.CrossRefGoogle Scholar
Cock, A. G. (1966). Genetical aspects of metrical growth and form in animals. The Quarterly Review of Biology 41, 131–190.CrossRefGoogle ScholarPubMed
Crompton, D. W. T. and Whitfield, P. J. (1986). The course of infection and egg production of Polymorphus minutus (Acanthocephala) in domestic ducks. Parasitology 58, 231–246.CrossRefGoogle Scholar
Engqvist, L. (2005). The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Animal Behaviour 70, 967–971. doi: 10.1016/j.anbehav.2005.01.016.CrossRefGoogle Scholar
Garland, T. Jr. and Adolph, S. C. (1994). Why not to do two-species comparative studies: Limitations on inferring adaptation. Physiological Zoology 67, 797–828.CrossRefGoogle Scholar
Gaskin, D. E. (1978). Form and function in the digestive tract and associated organs in Cetacea, with a consideration of metabolic rates and specific energy budgets. Oceanography and Marine Biology: An Annual Review 16, 313–345.Google Scholar
Hall-Aspland, S., Rogers, T., Canfield, R. and Tripovich, J. (2011). Food transit times in captive leopard seals (Hydrurga leptonyx). Polar Biology 34, 95–99. doi: 10.1007/s00300-010-0862-4.CrossRefGoogle Scholar
Karasov, W. H. and Diamond, J. M. (1985). Digestive adaptations for fueling the cost of endothermy. Science 228, 202–204. doi: 10.1126/science.3975638.CrossRefGoogle ScholarPubMed
Kastelein, R. A., Hardeman, J. and Boer, H. (1997 a). Food consumption and body weight of harbour porpoises (Phocoena phocoena). In The Biology of the harbour porpoise (ed. Read, A. J., Wiepkema, P. R. and Nachtigall, P. E.), pp. 217–233. De Spil Publishers, Woerden.Google Scholar
Kastelein, R. A., Nieuwstraten, S. H. and Verstegen, M. W. A. (1997 b). Passage time of carmine red dye through the digestive tract of harbour porpoises (Phocoena phocoena). In The Biology of the Harbour Porpoise (ed. Read, A. J., Wiepkema, P. R. and Nachtigall, P. E.), pp. 265–275. De Spil Publishers, Woerden, The Netherlands.Google Scholar
Klingenberg, C. P. (1996). Multivariate Allometry. In Advances in Morphometrics, (ed. Marcus, L. F., Corti, M., Loy, A., Naylor, G. J. P. and Slice, D. E.), pp. 23–49. NATO ASI Series A: Life Sciences, Vol. 284, New York, USA.CrossRefGoogle Scholar
Koehl, M. A. R. (1984). How do benthic organisms withstand moving water? American Zoologist 24, 57–70. doi: 10.1093/icb/24.1.57.CrossRefGoogle Scholar
Koehl, M. A. R. (1996) When does morphology matter? Annual Review of Ecology and Systematics 27, 501–542. doi: 10.1146/annurev.ecolsys.27.1.501.CrossRefGoogle Scholar
Parshad, V. R. and Crompton, D. W. T. (1981). Aspects of acanthocephalan reproduction. Advances in Parasitology 19, 73–138. doi: 10.1016/S0065-308X(08)60266-3.CrossRefGoogle ScholarPubMed
Petrochenko, V. I. (1956). Acanthocephala of Domestic and Wild Animals.Vol. I. Izdatel'stvo Akademii Nauk SSSR, Moscow. English translation by Israel Program for Scientific Translations Ltd., 1971.Google Scholar
Petrochenko, V. I. (1958). Acanthocephala of Domestic and Wild Animals.Vol II. Izdatel'stvo Akademii Nauk SSSR, Moscow. English translation by Israel Program for Scientific Translations Ltd., 1971.Google Scholar
Podesta, R. B. and Holmes, J. C. (1970). The life cycles of three Polymorphids (Acanthocephala) occurring as juveniles in Hyalella azteca (Amphipoda) at Cooking Lake, Alberta. Journal of Parasitology 56, 1118–1123.CrossRefGoogle Scholar
Poulin, R. (2007). Investing in attachment: evolution of anchoring structures in acanthocephalan parasites. Biological Journal of the Linnean Society 90, 637–645. doi: 10.1111/j.1095-8312.2006.00754.x.CrossRefGoogle Scholar
Poulin, R. (2009). Interspecific allometry of morphological traits among trematode parasites: selection and constraints. Biological Journal of the Linnean Society 96, 533–540. doi: 10.1111/j.1095-8312.2008.01163.x.CrossRefGoogle Scholar
Poulin, R., Wise, M. and Moore, J. (2003). A comparative analysis of adult body size and its correlates in acanthocephlan parasites. International Journal for Parasitology 33, 799–805. doi: 10.1016/S0020-7519(03)00108-5.CrossRefGoogle ScholarPubMed
Randhawa, H. S. and Poulin, R. (2010). Evolution of interspecific variation in size of attachment structures in the large tapeworms genus Acanthobothrium (Tetraphyllidae: Onchobothriidae). Parasitology 137, 1707–1720. doi: 10.1017/S0031182010000569.CrossRefGoogle Scholar
Sardella, N. H., Mattiucci, S., Timi, J. T., Bastida, R. O., Rodríguez, D. H. and Nascetti, G. (2005). Corynosoma australe Johnston, 1937 and C. cetaceum Johnston & Best,1942 (Acanthocephala: Polymorphidae) from marine mammals and fishesin Argentinian waters: allozyme markers and taxonomic status. Systematic Parasitology 61, 143–156. doi: 10.1007/s11230-005-3131-0.CrossRefGoogle Scholar
Schmidt, G. D. (1985). Development and life cycles. In Biology of the Acanthocephala, (ed. Crompton, D. W. T. and Nickol, B. B.), pp. 273–286. Cambridge University Press, Cambridge, UK.Google Scholar
Schulze, K. (2006). Imaging and modeling of digestion in the stomach and the duodenum. Journal of Neurogastroenterology and Motility 18, 172–183. doi: 10.1111/j.1365-2982.2006.00759.x.CrossRefGoogle ScholarPubMed
Sinisalo, S., Poulin, R., Högmander, H., Juuti, T. and Valtonen, E. T. (2004). The impact of sexual selection on Corynosoma magdaleni (Acanthocephala) infrapopulations in Saimaa ringed seals (Phoca hispida saimensis). Parasitology 128, 179–185. doi: 10.1017/S003118200300430X.CrossRefGoogle ScholarPubMed
Sorci, G., Morand, S. and Hugot, J. P. (1997). Host parasite coevolution: comparative evidence for covariation of life history traits in Primates and oxyurid parasites. Proceedings of the Royal Society of London, B 264, 285–289.CrossRefGoogle ScholarPubMed
Taraschewski, H. (2000). Host-parasite interactions in Acanthocephala: a morphological approach. Advances in Parasitology 46, 1–179.CrossRefGoogle ScholarPubMed
Valtonen, E. T. and Helle, E. (1982). Experimental infection of laboratory rats with Corynosoma semerme (Acanthocephala). Parasitology 85, 9–19. doi: 10.1017/S0031182000054093.CrossRefGoogle ScholarPubMed
Van Cleave, H. J. (1952). Some host-parasite relationships of the Acanthocephala, with special reference to the organs of attachment. Experimental Parasitology 1, 305–330.CrossRefGoogle Scholar
Williams, T. M., Haun, J., Davis, R. W., Fuiman, L. A. and Kohin, S. (2001). A killer appetite: metabolic consequences of carnivory in marine mammals. Comparative Biochemistry and Physiology Part A 129, 758–796.CrossRefGoogle ScholarPubMed