Hostname: page-component-cd9895bd7-p9bg8 Total loading time: 0 Render date: 2024-12-28T01:29:20.941Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproductive compensation in female Palaemonetes argentinus (Decapoda: Natantia) due to Microphallus szidati (Trematoda) infection

Published online by Cambridge University Press:  23 October 2020

M. Parietti Open the ORCID record for M. Parietti [Opens in a new window] ,
M.J. Merlo ,
M. Natal  and
M.A. Méndez Casariego
M. Parietti*
Affiliation:
Laboratorio de Parasitología. Instituto de Investigaciones en Producción, Sanidad y Ambiente (IIPROSAM), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Juan B. Justo 2550 (7600), Mar del Plata, Argentina
M.J. Merlo
Affiliation:
Laboratorio de Parasitología. Instituto de Investigaciones en Producción, Sanidad y Ambiente (IIPROSAM), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Juan B. Justo 2550 (7600), Mar del Plata, Argentina
M. Natal
Affiliation:
Centro Marplatense de Investigaciones Matemáticas (CEMIM), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Funes 3250 (7600), Mar del Plata, Argentina
M.A. Méndez Casariego
Affiliation:
Laboratorio de Parasitología. Instituto de Investigaciones en Producción, Sanidad y Ambiente (IIPROSAM), Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, Juan B. Justo 2550 (7600), Mar del Plata, Argentina
*
Author for correspondence: M. Parietti, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasites may affect host demographic characteristics because they can directly or indirectly cause the death of their hosts and/or influence their reproduction. Parasitism is therefore recognized as a factor that influences the composition and structure of populations and communities. One of these behaviours is the compensatory response: the host can compensate for the parasite losses effect, modifying the reproductive effort to enhance fitness. Ovigerus female Palaemonetes argentinus was collected and sorted into two groups according to the degree of development of their embryos: newly spawned embryos and embryos ready to hatch. The number of embryos and their dry weight for each female were determined. All parts of the female body were checked for parasites. The females of P. argentinus were parasitized by Microphalus szidati. We found that parasitized females produce more embryos but had more egg loss during development and the percentage of embryonic loss was higher in the parasitized females than in non-parasitized. Parasitized females produced lighter eggs than those from uninfected females. This supports the compensatory reproduction hypothesis suggested for this species. Parasitism can change life history traits in a way that fecundity can be compensated; this co-evolution between host and parasites will be population or context dependent. Parasites are a functional part of any ecosystem and as our results show, deleting parasites in life history traits and reproduction studies in free living organisms could lead to an incomplete picture of the true processes that happen in nature.

Keywords

Fecundity compensationtrematodeparasitescrustaceanlife history traits
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e204
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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

Baeza, JA and Fernández, M (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): The relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Functional Ecology 16, 241–251.CrossRefGoogle Scholar
Bauer, RT (2004) Remarkable shrimps: Adaptations and natural history of the carideans. Norman, OK, University of Oklahoma Press.Google Scholar
Best, A, White, A and Boots, M (2008) Maintenance of host variation in tolerance to pathogens and parasites. Proceedings of the National Academy of Sciences U.S.A. 105, 20786–20791.CrossRefGoogle ScholarPubMed
Bush, AO, Lafferty, KD, Lotz, JM and Shostak, AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology 83, 575–583. 7CrossRefGoogle Scholar
Caceci, T, Carlson, CB, Coth, TE and Smith, SA (1996) In vitro embryogenesis of Macrobrachium rosenbergii larvae following in vivo fertilization. Aquaculture 147, 169–175.CrossRefGoogle Scholar
Chadwick, W and Little, TJ (2005) A parasite-mediated life-history shift in Daphnia magna. Proceedings of the Royal Society B 272, 505–509.CrossRefGoogle ScholarPubMed
Devin, S, Piscart, C, Beisel, JN and Moreteau, JC (2004) Life history traits of the invader Dikerogammarus villosus (Crustacea: Amphipoda) in the Moselle River, France. International Review of Hydrobiology 89(1), 21–34.CrossRefGoogle Scholar
Duffield, KR, Bowers, EK, Sakaluk, SK and Sadd, BM (2017) A dynamic threshold model for terminal investment. Behavioral Ecology and Sociobiology 71(12), 185.CrossRefGoogle ScholarPubMed
Einum, S and Fleming, IA (2000) Highly fecund mothers sacrifice offspring survival to maximize fitness. Nature 405(6786), 565–567.CrossRefGoogle ScholarPubMed
Fisher, WS (1983) Eggs of Palaemon macrodactylus: II. Association with aquatic bacteria. The Biological Bulletin 164, 201–213.CrossRefGoogle Scholar
Forbes, MRL (1993) Parasitism and host reproductive effort. Oikos 67, 444–450.CrossRefGoogle Scholar
Giovagnolli, A, Ituarte, RB and Spivak, ED (2014) Effects of removal from the mother and salinity on embryonic development of Palaemonetes argentinus (Decapoda: Caridea: Palaemoneidae). Journal of Crustacean Biology 34, 174–181.CrossRefGoogle Scholar
Heins, D (2012) Fecundity compensation in the three-spined stickleback Casterosteus aculeatus infected by the diphyllobothriidean cestode Schistocephalus solidus. Biological Journal of the Linnean Society 106, 807–819.CrossRefGoogle Scholar
Ituarte, R (2008) Efectos de la salinidad sobre la reproducción y el desarrollo del camarón de agua dulce palaemonetes argentinus. Phd thesis, Universidad Nacional de Mar del PlataGoogle Scholar
Ituarte, RB, Spivak, ED and Anger, K (2007) Intraspecific variability in life-history traits of a “freshwater shrimp”. Palaemonetes argentinus. Annales de Limnologie- International Journal of Limnology 43(4), 293–302.CrossRefGoogle Scholar
Ituarte, RB, Spivak, ED, Camiolo, M and Anger, K (2010) Effects of salinity on the reproductive cycle of female freshwater shrimp, Palaemonetes argentinus. Journal of Crustacean Biology 30, 186–193.CrossRefGoogle Scholar
Korpelainen, H (1986) The effects of temperature and photoperiod on life history parameters of Daphnia magna (Crustacea: Cladocera). Freshwater Biology 16, 615–620.CrossRefGoogle Scholar
Krist, M (2001) Variation in fecundity among populations of snails is predicted by prevalence of castrating parasites. Evolutionary Ecology Research 3, 191–197.Google Scholar
Kutzer, MAM and Armitage, SAO (2016) Maximising fitness in the face of parasites: A review of host tolerance. Zoology 119, 281–289.CrossRefGoogle ScholarPubMed
Lafferty, KD (1993) The marine snail, Cerithidea californica, matures at smaller sizes where parasitism is high. Oikos 68(1), 3–11.CrossRefGoogle Scholar
Lefevre, T, Roche, B, Poulin, R, Hurd, H, Renaud, F and Thomas, F (2008) Exploiting host compensatory responses: The ‘must’ of manipulation? Trends in Parasitology 24, 435–439.CrossRefGoogle Scholar
Martorelli, SR (1986) Estudio sistemático y biológico de un digeneo perteneciente a la familia Microphallidae travassos, 1920. I: Microphallus szidati sp. nov. Parásito intestinal de Rallus sanguinolentus sanguinolentus (Aves: Rallidae) e Himantopus melanurus (Aves: Recurvirostridae). Revista Ibérica de Parasitología 46, 373–378.Google Scholar
Martorelli, SR (1988) El ciclo biológico de Levinseniella cruzi Travassos, 1920 (Digenea, Microphallidae) parásita de los ciegos cólicos de rollandia rolland chilensis (Aves, Podicipedidae) e himantopus melanurus (Aves, Recurvirostridae). Iheringia 68, 49–62.Google Scholar
Martorelli, SR, Marcotegui, PS and Alda, MP (2006) Procesos de enquistamiento y encapsulación de las metacercarias de Microphalus szidati en el Camarón Palaemonetes argentinus. In IV Congreso Iberoamericano Virtual de Acuicultura (CIVA), 973–988.Google Scholar
McCurdy, DG, Forbes, MR and Boates, JS (2000) Male amphipods increase their mating effort before behavioural manipulation by trematodes. Canadian Journal of Zoology 78(4), 606–612.CrossRefGoogle Scholar
Merlo, MJ, Parietti, M and Ituarte, RB (2016) Influence of Microphallus szidati Martorelli, 1986 (Trematoda) on the fecundity of the second intermediate host, Palaemonetes argentinus Nobili, 1901 (Decapoda: Natantia). Journal of Crustacean Biology 36, 94–98.CrossRefGoogle Scholar
Minchella, DJ (1985) Host life-history variation in response to parasitism. Parasitology 90, 205–216.CrossRefGoogle Scholar
Minchella, DJ and Loverde, PT (1981) A cost of increased early reproductive effort in the snail Biomphalaria glabrata. The American Naturalist 118, 876–881.CrossRefGoogle Scholar
Parietti, M, Merlo, MJ and Etchegoin, JA (2015) Population dynamic of two digenean species parasitizing the grass shrimp Palaemonetes argentinus Nobili 1901 (Decapoda: Palaemonidae) in a lentic environment from Argentina. Acta Parasitológica 60, 124–129.Google Scholar
Parker, BJ, Barribeau, SM, Laughton, AM, de Roode, JC and Gerardo, NM (2011) Non-immunological defense in an evolutionary framework. Trends in Ecology & Evolution 26(5), 242–248.CrossRefGoogle Scholar
Polak, M and Starmer, WT (1998) Parasite-induced risk of mortality elevates reproductive effort in male Drosophila. Proceedings of the Royal Society B: Biological Sciences 265, 2197–2201.CrossRefGoogle ScholarPubMed
R Development Core Team (2018) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available at https://www.gbif.org/es/tool/81287/r-a-language-and-environment-for-statistical-computing.Google Scholar
Rollingson, N and Hutchings, JA (2013) The relationship between offspring size and fitness: Integrating theory and empiricism. Ecology 94(2), 315–324.CrossRefGoogle Scholar
Santangelo, JM, Soares, BN, Paes, T, Maia-Barbosa, P, Tollrian, R and Bozelli, RL (2018) Effects of vertebrate and invertebrate predators on the life history of Daphnia similis and Moina macrocopa (Crustacea: Cladocera). Annales de Limnologie-International Journal of Limnology 54, 25.CrossRefGoogle Scholar
Scharsack, JP, Franke, F, Erin, NI, Kuske, A, Büscher, J, Stolz, H, Samonte, IE, Kurtz, J and Kalbe, M (2016) Effects of environmental variation on host–parasite interaction in three-spined sticklebacks (Gasterosteus aculeatus). Zoology 119, 375–402.CrossRefGoogle Scholar
Schultz, ET, Topper, M and Heins, DC (2006) Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: Parasite adaptation, host adaptation, or side effect? Oikos 114(2), 303–310.CrossRefGoogle Scholar
Schwanz, LE (2008) Chronic parasitic infection alters reproductive output in deer mice. Behavioral Ecology and Sociobiology 62, 1351–1358.CrossRefGoogle Scholar
Smith, C and Fretwell, S (1974) The optimal balance between size and number of offspring. American Naturalist 108, 499–506.CrossRefGoogle Scholar
Spivak, ED (1997) Life history of a brackish-water population of Palaemonetes argentinus (Decapoda: Caridea) in Argentina. Annales de Limnologie – International Journal of Limnology 33, 179–190.CrossRefGoogle Scholar
Thornhill, JA, Jones, JT and Kusel, JR (1986) Increased oviposition and growth in immature Biomphalaria glabrata after exposure to Schistosoma mansoni. Parasitology 93, 443–450.CrossRefGoogle ScholarPubMed
Vale, PF and Little, TJ (2012) Fecundity compensation and tolerance to a sterilizing pathogen in Daphnia. Journal of Evolutionary Biology 25, 1888–1896.CrossRefGoogle ScholarPubMed