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Sacculina carcini impact on energy content of the shore crab Carcinus maenas L.

Published online by Cambridge University Press:  04 August 2022

Joana Campos Open the ORCID record for Joana Campos [Opens in a new window] ,
Felipe Ribas ,
Ana Bio ,
Vânia Freitas ,
Allan T. Souza  and
Henk W. van der Veer
Joana Campos*
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research of the University of Porto (CIIMAR-UP), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, 4450-208 Matosinhos, Portugal
Felipe Ribas
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research of the University of Porto (CIIMAR-UP), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, 4450-208 Matosinhos, Portugal
Ana Bio
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research of the University of Porto (CIIMAR-UP), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, 4450-208 Matosinhos, Portugal
Vânia Freitas
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research of the University of Porto (CIIMAR-UP), Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos, 4450-208 Matosinhos, Portugal
Allan T. Souza
Affiliation:
Institute of Hydrobiology, Biology Centre of the Czech Academy of Sciences, Na Sádkách 7, 370 05 České Budějovice, Czech Republic
Henk W. van der Veer
Affiliation:
Department of Coastal Systems, Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB Den Burg, Texel, The Netherlands
*
Author for correspondence: Joana Campos, E-mail: [email protected]
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Abstract

The impact of Sacculina carcini infection on the nutritional status of the shore crab Carcinus maenas was investigated in the western Dutch Wadden Sea for a period of 20 months. About 3.3% of the population was sacculinized, i.e. externally infected with S. carcini and only 0.7% presented scars of previous infection. The results of mixed linear models showed that sacculinized and non-sacculinized crabs had similar morphometric condition, while the energy density of parasitized crabs (externa excluded) was significantly reduced by about 4.3% overall, and by up to 5.8% in crabs under 40 mm carapace width. However, when Sacculina externa was included in the energy determinations, the difference in energy density decreased to 1.2%, while total energy content of the pair infected crab-parasite including externa was 30.8% higher than non-sacculinized crabs of similar size. The total energy content of ovigerous females (eggs included) was even higher, near doubling the energy of similar-sized crabs. The same way, total energy content of Sacculina externa was about 4 times lower than total energy of egg mass. The results suggest that the rhizocephalan parasite is efficient in consuming the energy that the host may allocate for growth and maintenance, but require future studies to disentangle the impact of the degree of internal infection and the implications for the dynamics of the population.

Keywords

Decapodaenergy densityparasitismrhizocephalanWadden Sea
Type
Research Article
Information
Parasitology , Volume 149 , Issue 12 , October 2022 , pp. 1536 - 1545
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Adelung, D (1971) Untersuchungen zur Hautungsphysiologie der dekapoden Krebse am Beispiel der Sandkrabbe Carcinus maenas. Helgolander Wissenschaftliche Meeresuntersuchungen 22, 66–119.CrossRefGoogle Scholar
Atkinson, RJA and Parsons, AJ (1973) Seasonal patterns of migration and locomotion rhythmicity in populations of Carcinus. Netherlands Journal of Sea Research 7, 81–93.CrossRefGoogle Scholar
Baeta, A, Cabral, HN, Neto, JM, Marques, JC and Pardal, MA (2005) Biology, population dynamics and secondary production of the green crab Carcinus maenas (L.) in a temperate estuary. Estuarine, Coastal and Shelf Science 65, 43–52.CrossRefGoogle Scholar
Bates, D, Mächler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Belgrad, AB and Griffen, BD (2015) Rhizocephalan infection modifies host food consumption by reducing host activity levels. Journal of Experimental Marine Biology and Ecology 466, 70–75.CrossRefGoogle Scholar
Campos, J, Ribas, F, Bio, A, Freitas, V, Souza, AT and van der Veer, HW (2021) Body condition and energy content of shore crab Carcinus maenas in a temperate coastal system: temporal variability. Marine Ecology Progress Series 667, 99–112.CrossRefGoogle Scholar
Coates, CJ and Söderhäll, K (2021) The stress-immunity axis in shellfish. Journal of Invertebrate Pathology 186, 107492.CrossRefGoogle ScholarPubMed
Costa, S, Bessa, F and Pardal, MA (2013) The parasite Sacculina carcini Thompson, 1836 (Cirripedia, Rhizocephala) in the crab Carcinus maenas (Linnaeus, 1758) (Decapoda, Portunidae): influence of environmental conditions, colour morphotype and sex. Crustaceana 86, 34–47.CrossRefGoogle Scholar
Cummins, KW and Wuycheck, JC (1971) Caloric equivalents for investigations in ecological energetics. Verhandlungen der Internationalen Vereinigung fur Theoretische und Angewandte Limnologie 18, 1–158.Google Scholar
Darling, JA, Bagley, MJ, Roman, J, Tepolt, CK and Geller, JB (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Molecular Ecology 17, 4992–5007.CrossRefGoogle ScholarPubMed
Day, JH (1935) The life-history of Sacculina. Quarterly Journal of Microscopical Science 77, 549–583.Google Scholar
Delacre, M, Lakens, D and Leys, C (2017) Why psychologists should by default use Welch's t-test instead of Student's t-test. International Review of Social Psychology 30, 92–101.Google Scholar
Delage, Y (1884) Evolution de la Sacculine (Sacculina carcini Thomps.). Crustacé endoparasite de l'ordre nouveau des Kentrogonides. Archives de Zoologie Expérimentale et Générale 2, 417–736.Google Scholar
Elner, RW (1980) The influence of temperature, sex and chela size in the foraging strategy of the shore crab, Carcinus maenas (L.). Marine and Freshwater Behaviour and Physiology 7, 15–24.CrossRefGoogle Scholar
Garbary, DJ, Miller, AG, Williams, J and Seymour, NR (2014) Drastic decline of an extensive eelgrass bed in Nova Scotia due to the activity of the invasive green crab (Carcinus maenas). Marine Biology 161, 3–15.CrossRefGoogle Scholar
Glenner, H and Høeg, JT (1995) A new motile, multicellular stage involved in host invasion by parasitic barnacles (Rhizocephala). Nature 377, 147–149.CrossRefGoogle Scholar
Glenner, H and Werner, M (1998) Increased susceptibility of recently moulted Carcinus maenas (L.) to attack by the parasitic barnacle Sacculina carcini Thompson 1836. Journal of Experimental Marine Biology and Ecology 228, 29–32.CrossRefGoogle Scholar
Glenner, H, Høeg, JT, O'Brien, JJ and Sherman, TD (2000) Invasive vermigon stage in the parasitic barnacles Loxothylacus texanus and L. panopaei (Sacculinidae): closing of the rhizocephalan life-cycle. Marine Biology 136, 249–257.CrossRefGoogle Scholar
Goddard, JHR, Torchin, ME, Kuris, AM and Lafferty, K (2005) Host specificity of Sacculina carcini, a potential biological control agent of the introduced European green crab Carcinus maenas in California. Biological Invasions 7, 895–912.CrossRefGoogle Scholar
Heath, JR (1971) Seasonal changes in a population of Sacculina carcini Thompson (Crustacea: Rhizocephala) in Scotland. Journal of Experimental Marine Biology and Ecology 6, 15–22.CrossRefGoogle Scholar
Hlavac, M (2018) stargazer: Well-Formatted Regression and Summary Statistics Tables. R package version 5.2.2. Available at https://CRAN.R-project.org/package=stargazer.Google Scholar
Høeg, JT (1995) The biology and life cycle of the Rhizocephala (Cirripedia). Journal of the Marine Biology Association of the United Kingdom 75, 517–550.CrossRefGoogle Scholar
Høeg, JT and Lützen, J (1995) Life cycle and reproduction in the Cirripedia Rhizocephala. Oceanography and Marine Biology – an Annual Review 33, 427–485.Google Scholar
Høeg, JT, Glenner, H and Shields, JD (2005) Cirripedia Thoracica and Rhizocephala (barnacles). In Rohde, K (ed.), Marine Parasitology. Wallingford, UK: CABI Publishing and Collingwood, Victoria, Australia: CSIRO Publishing, pp. 154–165.Google Scholar
Hunter, E and Naylor, E (1993) Intertidal migration by the shore crab Carcinus maenas. Marine Ecology Progress Series 101, 131–138.CrossRefGoogle Scholar
Jensen, AR, Schneider, MR, Høeg, JT, Glenner, H and Lützen, J (2019) Variation in juvenile stages and success of male acquisition in Danish and French populations of the parasitic barnacle Sacculina carcini (Cirripedia: Rhizocephala) parasitizing the shore crab Carcinus maenas. Marine Biology Research 15, 191–203.Google Scholar
Kashenko, SD and Korn, OM (2002) Effects of temperature and salinity on the larvae of two species of rhizocephalan (Crustacea: Cirripedia). Invertebrate Reproduction and Development 29, 150–155.Google Scholar
Katwijk, M and Hermus, DCR (2000) Effects of water dynamics on Zostera marina: Transplantation experiments in the intertidal Dutch Wadden Sea. Marine Ecology Progress Series 208, 107–118.CrossRefGoogle Scholar
Klassen, G and Locke, AA (2007) Biological synopsis of the European green crab, Carcinus maenas. Fisheries and Oceans Canada, 1–75pp.Google Scholar
Kristensen, T, Nielsen, AI, Jørgensen, AI, Mouritsen, KN, Glenner, H, Christensen, JT, Lützen, J and Høeg, JT (2012) The selective advantage of host feminization: a case study of the green crab Carcinus maenas and the parasitic barnacle Sacculina carcini. Marine Biology 159, 2015–2023.CrossRefGoogle Scholar
Lafferty, KD and Kuris, AM (2009) Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology 25, 564–572.CrossRefGoogle ScholarPubMed
Larsen, MH, Hoeg, JK and Mouritsen, KN (2013) Influence of infection by Sacculina carcini (Cirripedia, Rhizocephala) on consumption rate and prey size selection in the shore crab Carcinus maenas. Journal of Experimental Marine Biology and Ecology 446, 209–215.CrossRefGoogle Scholar
Lowe, S, Browne, M, Boudjelas, S and De Poorter, M (2000) 100 of the World's worst invasive alien species. A selection from the Global Invasive Species Database. The Invasive Species Specialist Group (ISSG) of the World Conservation Union (IUCN), 12pp.Google Scholar
Lützen, J (1984) Growth, reproduction and life span in Sacculina carcini Thompson (Cirripedia, Rhizocephala) in the Isefjord, Denmark. Sarsia 69, 91–106.Google Scholar
Lützen, J, Jensen, KH and Glenner, H (2018) Life history of Sacculina carcini Thompson, 1836 (Cirripedia: Rhizocephala: Sacculinidae) and the intermoult cycle of its host, the shore crab Carcinus maenas (Linnaeus, 1758) (Decapoda: Brachyura: Carcinidae). Journal of Crustacean Biology 38, 413–419.Google Scholar
Mathieson, S, Berry, AJ and Kennedy, S (1998) The parasitic rhizocephalan barnacle Sacculina carcini in crabs of the Forth Estuary, Scotland. Journal of the Marine Biology Association of the United Kingdom 78, 665–667.CrossRefGoogle Scholar
McGaw, I and Naylor, E (1992) Salinity preference of the shore crab Carcinus maenas in relation to coloration during intermoult and to prior acclimation. Journal of Experimental Marine Biology and Ecology 155, 145–159.CrossRefGoogle Scholar
Mouritsen, KN and Jensen, T (2006) The effect of Sacculina carcini infections on the fouling, burying behaviour and condition of the shore crab, Carcinus maenas. Marine Biology Research 2, 270–275.CrossRefGoogle Scholar
Mouritsen, KN, Geyti, SNS, Lützen, J, Høeg, JT and Glenner, H (2018) Population dynamics and development of the rhizocephalan Sacculina carcini, parasitic on the shore crab Carcinus maenas. Diseases of Aquatic Organisms 131, 199–211.CrossRefGoogle ScholarPubMed
Nakagawa, S, Johnson, PCD and Schielzeth, H (2017) The coefficient of determination R 2 and intra-class correlation coefficient from generalized linear mixed-effects models revisited and expanded. Journal of the Royal Society Interface 14, 20170213.CrossRefGoogle ScholarPubMed
O'Brien, J and Van Wyk, P (1985) Effects of crustacean parasitic castrators (epicaridean isopods and rhizocephalan barnacles) on growth of crustacean hosts. In Wenner, A (ed.), Factors in Adult Growth, London, UK: CRC Press (Taylor & Francis), Crustacean Issues 3, pp. 191–218.Google Scholar
Øksnebjerg, B (2000) The Rhizocephala (Crustacea: cirripedia) of the Mediterranean and Black Seas: taxonomy, biogeography, and ecology. Israel Journal of Zoology 46, 1–102.CrossRefGoogle Scholar
Paine, RT (1964) Ash and calorie determinations of sponge and opisthobranch tissue. Ecology 45, 384–387.CrossRefGoogle Scholar
Powell, A and Rowley, AF (2008) Tissue changes in the shore crab Carcinus maenas as a result of infection by the parasitic barnacle Sacculina carcini. Diseases of Aquatic Organisms 80, 75–79.CrossRefGoogle ScholarPubMed
Rainbow, PS, Ford, MP and Heppelwhite, I (1979) Absence of gregarious settling behaviour by female larvae of British parasitic rhizocephalan barnacles. Journal of the Marine Biology Association of the United Kingdom 59, 591–196.CrossRefGoogle Scholar
Ramult, M (1935) Observations on the embryonic and larval development of Sacculina (Rhizocephala) in changed osmotic conditions of medium. Bulletin of the Polish Academy of Sciences B11, 87–109.Google Scholar
Rasmussen, E (1959) Behaviour of sacculinized shore crabs (Carcinus maenas Pennant). Nature 183, 479–480.CrossRefGoogle Scholar
R Core Team (2020) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. ISBN 3-900051-07-0, Available at http://www.R-project.org/.Google Scholar
Reinhard, EG (1956) Parasitic castration of Crustacea. Experimental Parasitology 5, 79–107.CrossRefGoogle ScholarPubMed
Roman, J and Palumbi, SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Molecular Ecology 13, 2891–2898.CrossRefGoogle ScholarPubMed
Rowley, AF, Davies, CE, Malkin, SH, Bryan, CC, Thomas, JE, Batista, FM and Coates, CJ (2020) Prevalence and histopathology of the parasitic barnacle, Sacculina carcini in shore crabs, Carcinus maenas. Journal of Invertebrate Pathology 171, 107338.CrossRefGoogle ScholarPubMed
Shen, CJ (1935) An investigation of the post-larval development of the shore crab Carcinus maenas, with special reference to external secondary sexual characters. Proceedings of the Zoological Society of London 1, 1–33.CrossRefGoogle Scholar
Squires, HJ (1990) Decapod Crustacea of the Atlantic coast of Canada. Canadian Bulletin of Fisheries and Aquatic Sciences 221, 532pp.Google Scholar
Thresher, RE, Werner, M, Høeg, JT, Svane, I, Glenner, H, Murphy, NE and Wittwer, C (2000) Developing the options for managing marine pests: specificity trials on the parasitic castrator, Sacculina carcini, against the European crab, Carcinus maenas, and related species. Journal of Experimental Marine Biology and Ecology 254, 37–51.CrossRefGoogle ScholarPubMed
Tolley, SG, Winstead, JT, Haynes, L and Volety, AK (2006) Influence of salinity on prevalence of the parasite Loxothylacus panopaei in the xanthid Panopeus obesus in SW Florida. Diseases of Aquatic Organiss 70, 243–250.CrossRefGoogle ScholarPubMed
Topley, B, Hume, J and Hartley, HB (1928) The kinetics of the decomposition of calcium carbonate hexahydrate. Proceedings of the Royal Society A 120, 211–222.Google Scholar
Torchin, ME, Lafferty, KD and Kuris, AM (2001) Release from natural enemies and invasion success: increased performance of green crabs in the absence of parasites. Biological Invasions 3, 333–345.CrossRefGoogle Scholar
Walker, G, Clare, A, Rittschof, D and Mensching, D (1992) Aspects of the life-cycle of Loxothylacus panopaei (Gissler), a sacculinid parasite of the mud crab Rhithropanopeus harrisii (Gould): a laboratory study. Journal of Experimental Marine Biology and Ecology 157, 181–193.CrossRefGoogle Scholar
Waser, AM, Goedknegt, MA, Dekker, R, McSweeney, N, Witte, JIJ, van der Meer, J and Thieltges, DW (2016) Tidal elevation and parasitism: patterns of infection by the rhizocephalan parasite Sacculina carcini in shore crabs Carcinus maenas. Marine Ecology Progress Series 545, 215–225.CrossRefGoogle Scholar
Werner, M (2001) Prevalence of the parasite Sacculina carcini Thompson 1836 (Crustacea, Rhizocephala) on its host crab Carcinus maenas (L.) on the west coast of Sweden. Ophelia 55, 101–110.CrossRefGoogle Scholar
Young, AM and Elliott, JA (2020) Life history and population dynamics of green crabs (Carcinus maenas). Fishes 5, 4.CrossRefGoogle Scholar
Zetlmeisl, C, Hermann, J, Petney, T, Glenner, H, Griffiths, C and Taraschewski, H (2011) Parasites of the shore crab Carcinus maenas (L.): implications for reproductive potential and invasion success. Parasitology 138, 394–401.CrossRefGoogle ScholarPubMed