Published August 31, 2019 | Version v1
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Role of temperature and carbonate system variability on a host-parasite system: Implications for the gigantism hypothesis

  • 1. Centro de Investigación e Innovación para el Cambio Climático (CiiCC), Facultad de Ciencias, Universidad Santo Tomás, Ejército 146, Santiago, Chile & Programa de Doctorado en Conservación y Gestión de la Biodiversidad, Facultad de Ciencias, Universidad Santo Tomás, Ejército 146, Santiago, Chile
  • 2. Departamento de Ecología y Biodiversidad, Facultad de Ciencias de la Vida, Universidad Andres Bello, República 440, Santiago, Chile
  • 3. Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile
  • 4. Departamento de Ciencias, Facultad de Artes Liberales, Universidad Adolfo Ibáñez, Santiago, Chile
  • 5. Centro de Investigación e Innovación para el Cambio Climático (CiiCC), Facultad de Ciencias, Universidad Santo Tomás, Ejército 146, Santiago, Chile

Description

García-Huidobro, M.R., Varas, O., George-Nascimento, M., Pulgar, J., Aldana, M., Lardies, M.A., Lagos, N.A. (2019): Role of temperature and carbonate system variability on a host-parasite system: Implications for the gigantism hypothesis. International Journal for Parasitology: Parasites and Wildlife 9: 7-15, DOI: 10.1016/j.ijppaw.2019.03.016, URL: http://dx.doi.org/10.1016/j.ijppaw.2019.03.016

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References

  • Aldana, M., Gonzalez, K., Loot, G., Pulgar, J., Marquet, P., 2009. First intemediate host of the digenean trematode Proctoeces lintoni (Fellodistomidae) in Chile. J. Parasitol. 95, 1408-1414.
  • Aldana, M., 2007. Variacion espacial de la interaccion hospedador-parasito: la importancia de la densidad poblacional de los hospedadores. Ph.D. dissertation.
  • Anguita, C., Simeone, A., 2015. Influence of seasonal food availability on the dynamics of seabird feeding flocks at a coastal upwelling area. PLoS One 10, e0131327.
  • Arakelova, E.S., Chebotareva, M.A., Zabelinskii, 2003. On adaptative changes of rate of oxygen consumption and lipid metabolism in Littorina saxatilis at parasitic invasions. J. Evol. Biochem. Physiol. 39, 519-528.
  • Arakelova, K.S., Chebotareva, M.A., Zabelinskii, S.A., 2004. Phisiology and lipid metabolism of Littorina saxatilis infected with trematodes. Dis. Aquat. Org. 60, 223-231.
  • Ballabeni, P., 1995. Parasitic-induced gigantism in a snail: a host adaptation? Funct. Ecol. 9, 887-893.
  • Baudoin, M., 1975. Host castration as a parasitic strategy. Evolution 29, 335-352.
  • Briones, C., Rivadeneira, M.M., Fernandez, M., Guinez, R., 2014. Geographical variation of shell thickness in the mussel Perumytilus purpuratus along the southeast pacific coast. Biol. Bull. 227, 221-231.
  • Beniash, E., Ivanina, A., Lieb, N.S., Kurochkin, I., Sokolova, I.M., 2010. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Mar. Ecol. Prog. Ser. 419, 95-108.
  • Bennington, C.C., Thayne, W.V., 1994. Use and misuse of mixed model analysis of variance in ecological studies. Ecology 75, 717-722.
  • Benitez, S., Lagos, N.A., Osores, S., Optiz, T., Duarte, C., Navarro, J.M., Lardies, M.A., 2018. High p CO2 levels affect metabolic rate, but not feeding behaviour and fitness, of farmed giant mussel Choromytilus chorus. Aquacult. Environ. Interact. 10, 267-278.
  • Calvo-Ugarteburu, G., McQuaid, C.D., 1998. Parasitism and invasive species: effects of digenetic trematodes on mussels. Mar. Ecol. Prog. Ser. 169, 149-163.
  • Castillo, N., Saaedra, L.M., Vargas, C.A., Gallardo-Escarate, C., Detree, C., 2017. Ocean acidification and pathogen exposure modulate the immune response of the edible mussel Mytilus chilensis. Fish Shellfish Immun 70, 149-155.
  • Castro-Rojas, M., Cid-Moya, K., George-Nascimento, M., 2015. Consumo de oxigeno en Perumytilus purpuratus segun el parasitismo por Digenea, y efectos de la temperatura y del ciclo de emersion-inmersion sobre la liberacion de cercarias. Rev. Biol. Mar.
  • Chapuis, E., 2009. Correlation between parasite prevalence and adult size in a trematodemollusc system: evidence for evolutionary gigantism in the freshwater snail Galba truncatula? J. Molluscan Stud. 75, 391-396.
  • Cremonte, F., Puebla, C., Tilleria, J., Videla, V., 2015. Histopathological survey of the mussel Mytilus chilensis (Mytilidae) and the clam Gari solida (Psammobiidae) from sourthern Chile. Lat. Am. J. Aquat. Res. 43, 248-254.
  • Cressler, E.C., Nelson, W.A., Day, T., McCaule, E., 2014. Starvation reveals the cause of infection-indiced castration and gigantism. Proc. R. Soc. B. 281, 20141087.
  • Dickson, A.G., Millero, F.J., 1987. A comparison of the equilibrium constants for the dissociate on of carbonic acid in seawater media- Deep Sea. Res. 34, 1733-1743.
  • Ebert, D., Carius, H.J., Little, T., Decaestecker, E., 2004. The evolution of virulence when parasites cause host castration and gigantism. Amm. Nat. 164, S19-S32.
  • Fernandez, J., Esch, G.W., 1991. Effect of parasitism on the growth rate of the pulmonate snail Helisoma ancepts. J. Parasitol. 77, 937-944.
  • Gaitan-Espitia, J., Bacigalupe, L., Optiz, T., Lagos, N.A., Osores, S., Lardies, M.A., 2017. Exploring physiological plasticity and local termal adaptation in an intertidal crab along a latitudinal cline. J. Therm. Biol. 68, 14-20.
  • Goater, T.M., Goater, C.P., Esch, G.W., 2014. Parasitism: the Diversity and Ecology of Animal Parasites, second ed. .
  • Gorbushin, A.M., 1997. Field evidence of trematode induced gigantism in Hydrobia spp. (Gastropoda: Prosobranchia). J. Mar. Biol. Assoc. U. K. 77, 785-800.
  • Gorbushin, A.M., Levakin, I.A., 1999. The effect of trematode on the growth of Onoba aculeus, Littorina saxatilis and L. abtusata (Gastropoda: Prosobranchia). J. Mar. Biol. Ass. U.K. 79, 273-279.
  • Haraldson, C., Anderson, L.G., Hassellov, M., Hulth, S., Olsson, K., 1997. Rapid, high precision potentiometric titration of alkalinity in ocean and sediment pore waters.
  • Deep Sea Res. 44, 2031-2044.
  • Hechinger, R., 2013. A metabolic and body-size scaling framework for parasite withinhost abundance, biomass, and energy flux. Am. Nat. 182, 234-248.
  • Henriquez, L.A., Daneri, G., Munoz, C.A., Montero, P., Veas, R., Palma, A.T., 2007.
  • Holmes, J.C., 1996. Parasites as threats to biodiversity in shrinking ecosystems. Biodivers. Concerv. 5, 975-983.
  • Keas, B.E., Esch, G.W., 1997. The effect of diet and reproductive matirity on the growth and reproduction of Helisoma anceps (Pulmonata) infected by Halipegus occidualis (Trematoda). J. Parasitol. 83, 96-104.
  • Kroeker, K.J., Kordas, R.l., Crim, R.N., Singh, G.G., 2010. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 13, 1419-1434.
  • Lafferty, K.D., Holt, D.H., 2003. How should environmental stress affect the population dynamics of disease? Ecol. Lett. 6, 654-664.
  • Lagos, N.A., Benitez, S., Duarte, C., Lardies, M.A., Broitman, B.R., Tapia, C., Tapia, P., Widdicombe, S., Vargas, C.A., 2016. Effects of temperature and ocean acidification on shell characteristics of Argopecten purpuratus: implications for scallop aquaculture in an upwelling-influenced area. Aquacult. Environ. Interact. 8, 357-370.
  • Lardies, M.A., Castilla, J.C., 2001. Latitudinal variation in the reproductive biology of the commensal crab Pinnaxodes chilensis (Decapoda: Pinnotheridae) along the Chilean coast. Mar. Bio. 139, 1125-1133.
  • Lauckner, G., 1983. Introduction: Bivalvia to Scaphopoda. In: Kinne, O. (Ed.), Bivalvia Diseases of Marine Animals. Biologische Anstalt Helgoland, Hamburg, pp. 477-977.
  • Leung, T.L.F., Poulin, R., 2008. Parasitism, commensalism, and mutualism: exploring the many shades of symbioses. Vie Milieu 58, 107-115.
  • Li, S., Liu, C., Huang, J., Liu, Y., Zheng, G., Xie, L., Zhang, R., 2015. Interactive effects of seawater acidification and elevated temperature on biomineralization and amino acid metabolism in the mussel Mytilus edulis. J. Exp. Biol. 218, 3623-3631.
  • Lienqueo, A.P., 2008. Parasitismo por trematodos en dos mitilidos intermareales (Semimytilus algosus y Perumytilus purpuratus). Lic. dissertation. Universidad Austral de Chile.
  • Lozada, E., Reyes, P., 1981. Reproductive biology of a population of Perumytilus purpuratus at el Tabo, Chile. Veliger 24, 147-154.
  • Marin, F., Le Roy, N., Marie, B., 2012. The formation and mineralization of mollusk shell. Front. Biosci. S4, 1099-1125.
  • McCarthy, H.O., Fitzpatrick, S.M., Irwin, S.W.B., 2004. Parasite alteration of host shape: a quantitative approach to gigantism helps elucidate evolutionary advantages.
  • McClelland, G., Bourns, T.K.R., 1969. Effects of Trichobilharzia ocellata on growth, reproduction, and survival of Lymnaea stagnalis. Exp. Parasitol. 24, 137-146.
  • Mehrbach, C., Culberson, C.H., Hawley, J.E., Pytkowicz, R.M., 1973. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18, 897-907.
  • Melzner, F., Stange, P., Trubenbach, K., Thomsen, J., Casties, I., Panknin, U., Gorb, S.N., Gutowaska, M.A., 2011. Food supply and seawater p CO2 impact calcification and internal shell dissolution in the blue mussel Mytilus edulis. PLoS Biol. 6, e24223.
  • Minchella, D.J., 1985. Host life-history variation in response to parasitism. Parasitology 90, 205-216.
  • Montenegro, D., Jones, B., Gonzalez, M.T., 2012. Report of pathogens and parasites in Perumytilus purpuratus from san Jorge Bay, Antofagasta, Chile. Rev. Biol. Mar.
  • Mischler, J., Johnson, P.T.J., McKenzie, V.J., Townsed, A.R., 2016. Parasite infection alters nitrogen cycling at the ecosystem scale. J. Anim. Ecol. 85, 817-828.
  • Morley, N.J., Lewis, J.W., 2013. Thermodynamics of cercarial development and emergence in trematodes. Parasitology 1211-1224.
  • Morley, N.J., 2011. Thermodynamics of cercarial survival and metabolism in a changing climate. Parasitology 138, 1442-1452.
  • Moore, J., 2002. Parasites and the Behavior of Animals. Oxford University Press, Oxford.
  • Mouritsen, K.N., Poulin, R., 2002. Parasitism, community structure and biodiversity in intertidal ecosystems. Parasitology 124, S101-S117.
  • Mouritsen, K.N., Jensen, K.T., 1994. The enigma of gigantism - effect of larval trematodes on growth, fecundity, egestion and locomotion in Hydrobia ulvae (Pennant) (Gastropoda: Prosobranchia). J. Exp. Mar. Biol. Ecol. 181, 53-66.
  • Munoz, G., Lopez, Z., Cardenas, L., 2013a. Morphological and molecular analyses of larval trematodes in the intertidal bivalve Perumytilus purpuratus from central Chile. J. Helminthol. 87, 356-363.
  • Munoz, G., Torres, P., Valdes, J., Rodriguez, A., 2013b. Spatio-temporal variation in the prevalence of trematodes in the bivalve Perumytilus purpurathus. Acta Parasitol. 58, 155-166.
  • Oliva, M., Valdivia, I.M., Cardenas, L., George-Nascimento, M., Gonzalez, K., Guinez, R.E., Cuello, D., 2010. Molecular and experimental evidence refuse the life cycle of Proctoeces lintoni (Fellodistomidae) in Chile. Pasitol. Res. 106, 737-740.
  • Osores, S.J.A., Lagos, N.A., San Martin, V., Manriquez, P.H., Vargas, C.A., Torres, R., Navarro, J.M., Poupin, M.J., Saldias, G.S., Lardies, M.A., 2017. Plasticity and interpopulation variability in physiological and life-history traits of the mussel Mytilus chilensis: a reciprocal transplant experiment. J. Exp. Mar. Biol. Ecol. 490, 1-12.
  • Palmer, A.R., 1992. Calcification in marine molluscs: how costly is it? Proc. Natl. Acad. Sci. U.S.A. 89, 1379-1382.
  • Perez, C.A., Lagos, N.A., Saldias, G.S., Waldbusser, G., Vargas, C.A., 2016. Riverine discharges impact physiological traits and carbon sources for Shell carbonate in the marine intertidal mussel Perumytilus purpuratus. Limnol. Oceanogr. 61, 969-983.
  • Pierrot, D., Lewis, E., Wallace, D.W.R., 2006. MS Excel Program Development for CO2 System Calculations. ORNL/CDIAC-105a. Carbon Dioxide Information Analysis Center. Oak ridge national laboratory, US Department of Energy, Oak ridge, TN.
  • Poulin, R., 2006. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143-151.
  • Prado, L., Castilla, J.C., 2006. The bioengineer Perumytilus purpuratus (Mollusca: Bivalvia) in central Chile: biodiversity, habitat structural complexity and environmental heterogeneity. J. Mar. Biol. Ass. U.K. 86, 417-421.
  • Ramajo, L., Prado, L., Rodriguez-Navarro, A.B., Lardies, M.A., Duarte, C.M., Lagos, N., 2016. Plasticity and trade-offs in physiological traits of intertidal mussels subjected to freshwater-induced environmental variation. Mar. Ecol. Prog. Ser. 553, 93-109.
  • Reimer, O., Tedengren, M., 1996. Phenotypical improvement of morphological defences in the mussel Mytilus edulis induced by exposure to the predator Asterias rubens. Oikos 75, 383-390.
  • Rothschild, A., Rothschild, M., 1939. Some observation on the growth of Peringia ulvae (Pennant) 1777 in the laboratory. Novit. Zool. 41, 240-247.
  • Roff, D.A., 2002. The Evolution of Life Histories: Theory and Analysis. Chapman and Hall, New York.
  • Sorensen, R.E., Minchella, D.J., 2001. Snail-trematode life history interactions: past trends and future directions. Parasitology 123, S3-S18.
  • Sousa, W.P., 1983. Host life history and the effect of parasitic castration on growth: a field study of Cerithidea californica Haldeman (Gastropoda: Prosobranchia) and its trematode parasites. J. Exp. Mar. Biol. Ecol. 73, 273-296.
  • Stearns, S.C., 2002. Life-history tactics: a review of the ideas. Q. Rev. Biol. 51, 3-47.
  • Sturrock, B.M., 1966. The influence of infection with Schistocoma mansoni on the growth rate and reproduction of Biomphalaria pfeifferi. Ann. Trop. Med. Parasitol. 60, 187-197.
  • Taskinen, J., 1998. Influence of trematode parasitism on the growth of a bivalve host in the field. Int. J. Parasitol. 28, 599-602.
  • Thieltges, D.W., Rick, J., 2006. Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Dis. Aquat. Org. 73, 63-68.
  • Thorhill, J.A., Jones, J.T., Kusel, J.R., 1986. Increased oviposition and growth in immature Biomphalaria glabrata after exposure to Schistosoma mansoni. Parasitology 93, 443-450.
  • Tielens, A.G.M., 1994. Energy generation in parasitic helminths. Parasitol. Today 9, 346-352.
  • Torres, R., Pantoja, S., Harada, N., Gonzalez, H.E., Daneri, G., Frangopulos, M., Rutlant, J.A., Duarte, C.M., Ruiz-Halpern, S., Mayol, E., Fukasawa, M., 2011. Air-sea CO2 fluxes along the coast of Chile: from CO2 outgassing in central northern upwelling waters to CO2 uptake in southern Patagonian fjords. J. Geophys. Res. 116, C09006.
  • Vennatta, J.T., Minchella, D.J., 2018. Parasites and their impact on ecosystem nutrient cycling. Trends Parasitol. 34, 452-455.
  • Watson, S.A., Peck, L., Tyler, P., Southgate, P., Tan, K., Day, R., Morley, S., 2012. Marine invertebrate skeleton size varies with latitude, temperature, and carbonate saturation: implications for global change and ocean acidification. Glob. Change. Bio.l 10, 3026-3038.
  • Weiner, S., Dove, P.M., 2003. An overview of biomineralization processes and the problem of the vital effect. Rev. Miner. Geochem. 54, 1-29.
  • Yao, C.-L., Somero, G.N., 2014. The impact of ocean warming on marine organisms. Chin. Sci. Bull. 59, 468-479.
  • Zar, J.H., 1996. Biostatistical Analysis, third ed. Prentice-Hall Inc, Englewood Cliffs, NJ.