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Host food quality and quantity differentially affect Ascogregarina barretti parasite burden, development and within-host competition in the mosquito Aedes triseriatus

Published online by Cambridge University Press:  29 August 2019

Katie M. Westby Open the ORCID record for Katie M. Westby [Opens in a new window] ,
Brenden M. Sweetman ,
Solny A. Adalsteinsson ,
Elizabeth G. Biro  and
Kim A. Medley
Katie M. Westby*
Affiliation:
Tyson Research Center, Washington University in St Louis, 6750 Tyson Valley Road, Eureka, MO 63025, USA
Brenden M. Sweetman
Affiliation:
Tyson Research Center, Washington University in St Louis, 6750 Tyson Valley Road, Eureka, MO 63025, USA
Solny A. Adalsteinsson
Affiliation:
Tyson Research Center, Washington University in St Louis, 6750 Tyson Valley Road, Eureka, MO 63025, USA
Elizabeth G. Biro
Affiliation:
Tyson Research Center, Washington University in St Louis, 6750 Tyson Valley Road, Eureka, MO 63025, USA
Kim A. Medley
Affiliation:
Tyson Research Center, Washington University in St Louis, 6750 Tyson Valley Road, Eureka, MO 63025, USA
*
Author for correspondence: Katie M. Westby, E-mail: katiewestby206@gmail.com
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Abstract

Host condition depends in large part on the quality and quantity of available food and heavily influences the outcome of parasite infection. Although parasite fitness traits such as growth rate and size may depend on host condition, whether host food quality or quantity is more important to parasite fitness and within-host interactions is poorly understood. We provided individual mosquito hosts with a standard dose of a gregarine parasite and reared mosquitoes on two food types of different quality and two quantities. We measured host size, total parasite count and area, and average size of parasites within each treatment. Food quality significantly influenced the number of parasites in a host; hosts fed a low-quality diet were infected with more parasites than those provided a high-quality diet. In addition, we found evidence of within-host competition; there was a negative relationship between parasite size and count though this relationship was dependent on host food quality. Host food quantity significantly affected total parasite area and parasite size; lower food quantity resulted in smaller parasites and reduced overall parasite area inside the host. Thus both food quality and quantity have the potential to influence parasite fitness and population dynamics.

Keywords

Aedes triseriatusAscogregarina barrettidetritusgregarineshost conditionmosquitotanninswith-in host competition
Type
Research Article
Information
Parasitology , Volume 146 , Issue 13 , November 2019 , pp. 1665 - 1672
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Copyright
Copyright © Cambridge University Press 2019 

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References

Alto, BW, Kesavaraju, B, Juliano, SA and Philip Lounibos, L (2009) Stage-dependent predation on competitors: consequences for the outcome of a mosquito invasion. Journal of Animal Ecology 78, 928–936.Google Scholar
Bara, JJ, Clark, TM and Remold, SK (2014) Utilization of larval and pupal detritus by Aedes aegypti and Aedes albopictus. Journal of Vector Ecology 39, 44–47.Google Scholar
Bedhomme, S, Agnew, P, Sidobre, C and Michalakis, Y (2004) Virulence reaction norms across a food gradient. Proceedings Biological Sciences/The Royal Society 271, 739–744.Google Scholar
Beier, JC and Craig, GBJ (1985) Gregarine parasites of mosquitoes. Integrated Mosquito Control Methodologies 2, 167–184.Google Scholar
Bize, P, Jeanneret, C, Klopfenstein, A and Roulin, A (2008) What makes a host profitable? Parasites balance host nutritive resources against immunity. The American Naturalist 171, 107–118.Google Scholar
Brown, MJF, Loosli, R and Schmid-Hempel, P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91, 421–427.Google Scholar
Brunner, FS, Schmid-Hempel, P and Barribeau, SM (2014) Protein-poor diet reduces host-specific immune gene expression in Bombus terrestris. Proceedings of the Royal Society B: Biological Sciences 281. doi: 10.1098/rspb.2014.0128.Google Scholar
Burnham, KP and Anderson, DR (2002) Model Selection and Inference: A Practical Information-Theoretic Approach. 2nd ed. New York: Springer-Verlag. http://dx.doi.org/10.1007/b97636Google Scholar
Burnham, KP, Anderson, DR and Huyvaert, KP (2010) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behavioral Ecology and Sociobiology 65, 23–35.Google Scholar
Chylinski, C, Boag, B, Stear, MJ and Cattadori, IM (2009) Effects of host characteristics and parasite intensity on growth and fecundity of Trichostrongylus retortaeformis infections in rabbits. Parasitology 136, 117–123.Google Scholar
Comiskey, NM, Lowrie, RC and Wesson, DM (1999) Effect of nutrient levels and Ascogregarina taiwanensis (Apicomplexa: Lecudinidae) infections on the vector competence of Aedes albopictus (Diptera: Culicidae) for Dirofilaria immitis (Filarioidea: Onchocercidae). Journal of Medical Entomology 36, 55–61.Google Scholar
Cory, JS and Hoover, K (2006) Plant-mediated effects in insect-pathogen interactions. Trends in Ecology and Evolution 21, 278–286.Google Scholar
Costanzo, KS, Westby, KM and Medley, KA (2018) Genetic and environmental influences on the size-fecundity relationship in Aedes albopictus (Diptera: Culicidae): impacts on population growth estimates? PLoS ONE 18, 1–17. doi: 10.1371/journal.pone.0201465.Google Scholar
Daly, HV (1985) Insect morphometrics. Annual Review of Entomology 30, 415–438.Google Scholar
Daugherty, MP, Alto, BW and Juliano, SA (2000) Invertebrate carcasses as a resource for competing Aedes albopictus and Aedes aegypti (Diptera: Culicidae). Journal of Medical Entomology 37, 364–372.Google Scholar
David, JP, Rey, D, Pautou, MP and Meyran, JC (2000) Differential toxicity of leaf litter to dipteran larvae of mosquito developmental sites. Journal of Invertebrate Pathology 75, 9–18.Google Scholar
Davidson, EW, Larsen, A and Palmer, CM (2012) Potential influence of plant chemicals on infectivity of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms 101, 87–93.Google Scholar
de Roode, JC, Read, AF, Chan, BHK and Mackinnon, MJ (2003) Rodent malaria parasites suffer from the presence of conspecific clones in three-clone Plasmodium chabaudi infections. Parasitology 127, 411–418.Google Scholar
de Roode, JC, Helinski, MEH, Anwar, MA and Read, AF (2005) Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. The American Naturalist 166, 531–542.Google Scholar
Dube, WC, Hund, AK, Turbek, SP and Safran, RJ (2018) Microclimate and host body condition influence mite population growth in a wild bird-ectoparasite system. International Journal for Parasitology: Parasites and Wildlife 7, 301–308.Google Scholar
Earl, JE and Semlitsch, RD (2015) Effects of tannin source and concentration from tree leaves on two species of tadpoles. Environmental Toxicology and Chemistry 34, 120–126.Google Scholar
Ezenwa, VO (2004) Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. International Journal for Parasitology 34, 535–542.Google Scholar
Fish, D and Carpenter, SR (1982) Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology 63, 283–288.Google Scholar
Fredensborg, BL and Poulin, R (2005) Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061–1070.Google Scholar
Gotelli, NJ and Ellison, AM (2004) A Primer of Ecological Statistics. Sunderland, MA: Sinauer Associates Inc.Google Scholar
Hartemink, NA, Randolph, SE, Davis, SA and Heesterbeek, JAP (2008) The basic reproduction number for complex disease systems: defining R(0) for tick-borne infections. The American Naturalist 171, 743–754.Google Scholar
Hättenschwiler, S and Vitousek, PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends in Ecology and Evolution 15, 238–243.Google Scholar
Holfeld, H (2000) Infection of the single-celled diatom Stephanodiscus alpinus by the chytrid Zygorhizidium: parasite distribution within host population, changes in host cell size, and host-parasite size relationship. Limnology and Oceanography 45, 1440–1444.Google Scholar
Irvine, RJ, Stien, A, Dallas, JF, Halvorsen, O, Langvatn, R and Albon, SD (2001) Contrasting regulation of fecundity in two abomasal nematodes of Svalbard reindeer (Rangifer tarandus platyrhynchus). Parasitology 122, 673–681.Google Scholar
Kingsolver, JG and Huey, RB (2008) Size, temperature, and fitness: three rules. Evolutionary Ecology Research 10, 251–268.Google Scholar
Kopp, EB and Medzhitov, R (2009) Infection and inflammation in somatic maintenance, growth and longevity. Evolutionary Applications 2, 132–141.Google Scholar
Lafferty, K and Holt, R (2003) How should environmental stress affect the population dynamics of diseases? Ecology Letters 6, 654–664.Google Scholar
Lagrue, C and Poulin, R (2008) Intra- and interspecific competition among helminth parasites: effects on Coitocaecum parvum life history strategy, size and fecundity. International Journal for Parasitology 38, 1435–1444.Google Scholar
Lantova, L and Volf, P (2014) Mosquito and sand fly gregarines of the genus Ascogregarina and Psychodiella (apicomplexa: Eugregarinorida, Aseptatorina) – overview of their taxonomy, life cycle, host specificity and pathogenicity. Infection, Genetics and Evolution 28, 616–627.Google Scholar
Lee, KP, Cory, JS, Wilson, K, Raubenheimer, D and Simpson, SJ (2006) Flexible diet choice offsets protein costs of pathogen resistance in a caterpillar. Proceedings of the Royal Society B: Biological Sciences 273, 823–829.Google Scholar
Lee, KP, Simpson, SJ and Wilson, K (2008) Dietary protein-quality influences melanization and immune function in an insect. Functional Ecology 22, 1052–1061.Google Scholar
Logan, A, Ruiz-González, MX and Brown, MJF (2005) The impact of host starvation on parasite development and population dynamics in an intestinal trypanosome parasite of bumble bees. Parasitology 130, 637–642.Google Scholar
Mercer, DR (1993) Effect of tannic acid concentration on the development of the Western treehole mosquito, Aedes sierrensis (Diptera: Culicidae). Journal of Chemical Ecology 19, 1119–1127.Google Scholar
Mercer, DR and Anderson, JR (1994) Tannins in treehole habitats and their effects on Aedes sierrensis (Diptera: Culicidae) production and parasitism by Lambornella clarki (Ciliophora: Tetrahymenidae). Journal of Medical Entomology 31, 159–167.Google Scholar
Mideo, N (2009) Parasite adaptations to within-host competition. Trends in Parasitology 25, 261–268.Google Scholar
Munstermann, LE and Wesson, DM (1990) First record of Ascogregarina taiwanensis (Apicomplexa: Lecudinae) in North American Aedes albopictus. Journal of the American Mosquito Control Association 6, 235–243.Google Scholar
Murrell, EG and Juliano, SA (2008) Detritus type alters the outcome of interspecific competition between Aedes aegypti and Aedes albopictus (Diptera: Culicidae). Journal of Medical Entomology 45, 375–383.Google Scholar
Murrell, EG and Juliano, SA (2013) Predation resistance does not trade off with competitive ability in early-colonizing mosquitoes. Oecologia 173, 1033–1042.Google Scholar
Patterson, S and Viney, M (2002) Host immune responses are necessary for density dependence in nematode infections. Parasitology 125, 283–292.Google Scholar
Pulkkinen, K and Ebert, D (2004) Host starvation decreases parasite load and mean host size in experimental populations. Ecology 85, 823–833.Google Scholar
Rowe, A, McMaster, K, Emery, D and Sangster, N (2008) Haemonchus contortus infection in sheep: parasite fecundity correlates with worm size and host lymphocyte counts. Veterinary Parasitology 153, 285–293.Google Scholar
Sasall, P and Morand, S (1998) Comparative analysis: a tool for studying monogenean ecology and evolution. International Journal for Parasitology 28, 1637–1644.Google Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH image to ImageJ: 25 years of image analysis. Nature Methods 9, 671–675.Google Scholar
Seppälä, O, Liljeroos, K, Karvonen, A and Jokela, J (2008) Host condition as a constraint for parasite reproduction. Oikos 117, 749–753.Google Scholar
Siegel, JP, Novak, RJ and Maddox, JV (1992) Effects of Ascogregarina barretti (Eugregarinida: Lecudinidae) infection on Aedes triseriatus (Diptera: Culicidae) in Illinois. Journal of Medical Entomology 29, 968–973.Google Scholar
Siva-Jothy, MT, Moret, Y and Rolff, J (2005) Insect Immunity: An Evolutionary Ecology Perspective. doi: 10.1016/S0065-2806(05)32001-7.Google Scholar
Soghigian, J and Livdahl, T (2017) Differential response to mosquito host sex and parasite dosage suggest mixed dispersal strategies in the parasite Ascogregarina taiwanensis. PLoS ONE 12, 1–14.Google Scholar
Soghigian, J, Valsdottir, LR and Livdahl, TP (2017) A parasite's modification of host behavior reduces predation on its host. Ecology and Evolution 7, 1453–1461. doi: 10.1002/ece3.2748.Google Scholar
Sota, T (1993) Performance of Aedes albopictus and A. riversi larvae (Diptera: Culicidae) in waters that contain tannic acid and decaying leaves: Is the treehole species better adapted to treehole water? Annals of the Entomological Society of America 86, 450–457.Google Scholar
Stoler, AB, Berven, KA and Raffel, TR (2016) Leaf litter inhibits growth of an amphibian fungal pathogen. EcoHealth 13, 392–404.Google Scholar
Suwanchaichinda, C and Paskewitz, SM (1998) Effects of larval nutrition, adult body size, and adult temperature on the ability of Anopheles gambiae (Diptera: Culicidae) to melanize Sephadex beads. Journal of Medical Entomology 35, 157–161.Google Scholar
Taniguchi, Y and Nakano, S (2000) Condition-specific competition: implications for the altitudinal distribution of stream fishes. Ecology 81, 2027–2039.Google Scholar
Taylor, AD (1988) Host effects on larval competition in the gregarious parasitoid Bracon hebetor. Journal of Animal Ecology 57, 163–172.Google Scholar
Telang, A, Qayum, AA, Parker, A, Sacchetta, BR and Byrnes, GR (2012) Larval nutritional stress affects vector immune traits in adult yellow fever mosquito Aedes aegypti (Stegomyia aegypti). Medical and Veterinary Entomology 26, 271–281.Google Scholar
Tompkins, DM and Hudson, PJ (1999) Regulation of nematode fecundity in the ring-necked pheasant (Phasianus colchicus): not just density dependence. Parasitology 118, 417–423.Google Scholar
Tsai, ML, Li, JJ and Dai, CF (2001) How host size may constrain the evolution of parasite body size and clutch size. The parasitic isopod Ichthyoxenus fushanensis and its host fish, Varicorhinus bacbatulus, as an example. Oikos 92, 13–19.Google Scholar
Tseng, M and Myers, JH (2014) The relationship between parasite fitness and host condition in an insect-virus system. PLoS ONE 9, e106401.Google Scholar
Vale, PF, Choisy, M and Little, TJ (2013) Host nutrition alters the variance in parasite transmission potential. Biology Letters 9, 20121145.Google Scholar
Venesky, MD, Wilcoxen, TE, Rensel, MA, Rollins-Smith, L, Kerby, JL and Parris, MJ (2012) Dietary protein restriction impairs growth, immunity, and disease resistance in southern leopard frog tadpoles. Oecologia 169, 23–31.Google Scholar
Wale, N, Sim, DG and Read, AF (2017) A nutrient mediates intraspecific competition between rodent malaria parasites in vivo. Proceedings of the Royal Society B: Biological Sciences 284. doi: 10.1098/rspb.2017.1067.Google Scholar
Walker, ED and Merritt, RW (1988) The significance of leaf detritus to mosquito (Diptera: Culicidae) productivity from treeholes. Environmental Entomology 17, 199–206.Google Scholar
Walker, ED, Poirier, SJ and Veldman, WT (1987) Effects of Ascogregarina barretti (Eugregarinida: Lecudinidae) infection on emergence success, development time, and size of Aedes triseriatus (Diptera: Culicidae) in microcosms and tires. Journal of medical entomology 24, 303–309.Google Scholar
Wedekind, C, Christen, M, Schärer, L and Treichel, N (2000) Relative helminth size in crustacean hosts: in vivo determination, and effects of host gender and within-host competition in a copepod infected by a cestode. Aquatic Ecology 34, 279–285.Google Scholar
Yee, DA and Juliano, SA (2006) Consequences of detritus type in an aquatic microsystem: effects on water quality, micro-organisms and performance of the dominant consumer. Freshwater Biology 51, 448–459.Google Scholar
Zuk, M and Stoehr, AM (2002) Immune defense and host life history. The American Naturalist 160, S9–S22.Google Scholar
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