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The drivers and consequences of unstable Plasmodium dynamics: a long-term study of three malaria parasite species infecting a tropical lizard

  • Luisa Otero (a1), Jos J. Schall (a2), Virnaliz Cruz (a3), Kristen Aaltonen (a4) and Miguel A. Acevedo (a5)...

Understanding the consequences of environmental fluctuations for parasite dynamics requires a long-term view stretching over many transmission cycles. Here we studied the dynamics of three malaria parasites (Plasmodium azurophilum, P. leucocytica and P. floridense) infecting the lizard Anolis gundlachi, in the rainforest of Puerto Rico. In this malaria–anole system we evaluated temporal fluctuations in individual probability of infection, the environmental drivers of observed variation and consequences for host body condition and Plasmodium parasites assemblage. We conducted a total of 15 surveys including 10 from 1990 to 2002 and five from 2015 to 2017. During the early years, a lizard's probability of infection by all Plasmodium species appeared stable despite disturbances ranging from two hurricanes to short droughts. Over a longer timescale, probability of infection and overall prevalence varied significantly, following non-linear relationships with temperature and rainfall such that highest prevalence is expected at intermediate climate measures. A perplexing result was that host body condition was maximized at intermediate levels of rainfall and/or temperature (when risk of infection was highest), yet we found no significant decreases in body condition due to infection. Plasmodium parasite species composition varied through time with a reduction and near local extinction of P. floridense. Our results emphasize the need for long-term studies to reveal host–parasite dynamics, their drivers and consequences.

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Author for correspondence: Miguel A. Acevedo, E-mail:
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Altizer, S, Ostfeld, RS, Johnson, PTJ, Kutz, S and Harvell, CD (2013) Climate change and infectious diseases: from evidence to a predictive framework. Science 341, 514519.
Aron, JL and May, RM (1982) The population dynamics of malaria. In Anderson RM (ed.), The Population Dynamics of Infectious Diseases: Theory and Applications. Boston, MA: Springer, pp. 139179.
Beadell, JS, Ishtiaq, F, Covas, R, Melo, M, Warren, BH, Atkinson, CT, Bensch, S, Graves, GR, Jhala, YV, Peirce, MA, Rahmani, AR, Fonseca, DM and Fleischer, RC (2006) Global phylogeographic limits of Hawaii's avian malaria. Proceedings of the Royal Society of London B: Biological Sciences 273, 29352944.
Bensch, S, Waldenström, J, Jonzén, N, Westerdahl, H, Hansson, B, Sejberg, D and Hasselquist, D (2017) Temporal dynamics and diversity of avian malaria parasites in a single host species. Journal of Animal Ecology 76, 112122.
Betini, GS., Avgar, T and Fryxell, JM (2017) Why are we not evaluating multiple competing hypotheses in ecology and evolution? Royal Society Open Science 4, 160756.
Burnham, KP and Anderson, DR (2004) Multimodel inference: understanding AIC and BIC in model selection. Sociological Methods & Research 33, 261304.
Chamberlin, TC (1965) The method of multiple working hypotheses. Science 148, 754759.
Chiyaka, C, Tatem, AJ, Cohen, JM, Gething, PW, Johnston, G, Gosling, R, Laxminarayan, R, Hay, SI and Smith, DL (2013) The stability of malaria elimination. Science 339, 909910.
Clutton-Brock, T and Sheldon, BC (2010) Individuals and populations: the role of long-term, individual-based studies of animals in ecology and evolutionary biology. Trends in Ecology & Evolution 25, 562573.
Cox, RM and Calsbeek, R (2015) Survival of the fattest? Indices of body condition do not predict viability in the brown anole (Anolis sagrei). Functional Ecology 29, 404413.
Eisen, RJ and Wright, NM (2001) Landscape features associated with infection by a malaria parasite (Plasmodium mexicanum) and the importance of multiple scale studies. Parasitology 122, 507513.
Elliot, SL, Blanford, S and Thomas, MB (2002) Host–pathogen interactions in a varying environment: temperature, behavioural fever and fitness. Proceedings of the Royal Society of London B: Biological Sciences 269, 15991607.
Elliott, LP and Brook, BW (2007) Revisiting Chamberlin: multiple working hypotheses for the 21st century. BioScience 57, 608614.
Ewald, PW (1995) The evolution of virulence: a unifying link between parasitology and ecology. The Journal of Parasitology 81, 659669.
Fallon, SM, Ricklefs, RE, Latta, SC and Bermingham, E (2004) Temporal stability of insular avian malarial parasite communities. Proceedings of the Royal Society of London B: Biological Sciences 271, 493500.
Galen, SC, Borner, J, Martinsen, ES, Schaer, J, Austin, CC, West, CJ and Perkins, SL (2018) The polyphyly of Plasmodium: comprehensive phylogenetic analyses of the malaria parasites (order Haemosporida) reveal widespread taxonomic conflict. Royal Society Open Science 5, 171780.
Garamszegi, LZ (2011) Climate change increases the risk of malaria in birds. Global Change Biology 17, 17511759.
Gorman, GC and Licht, P (1974) Seasonality in ovarian cycles among tropical Anolis lizards. Ecology 55, 360369.
Granthon, C and Williams, DA (2017) Avian malaria, body condition, and blood parameters in four species of songbirds. The Wilson Journal of Ornithology 129, 492508.
Gupta, S and Day, KP (1994) A strain theory of malaria transmission. Parasitology Today 10, 476481.
Hackett, LW (1937) Malaria in Europe. An ecological study. London, UK: Oxford University Press.
Harvell, CD, Mitchell, CE, Ward, JR, Altizer, S, Dobson, AP, Ostfeld, RS and Samuel, MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 21582162.
Hertz, PE, Huey, RB and Stevenson, RD (1993) Evaluating temperature regulation by field-active ectotherms: the fallacy of the inappropriate question. The American Naturalist 142, 796818.
Huey, RB and Webster, TP (1976) Thermal biology of Anolis lizards in a complex fauna: the Christatellus group on Puerto Rico. Ecology 57, 985994.
Klein, TA, Young, DG and Telford, JS (1987) Vector incrimination and experimental transmission of Plasmodium floridense by bites of infected Culex (melanoconion) erraticus. Journal of the American Mosquito Control Association 3, 165175.
LaPointe, DA, Goff, ML and Atkinson, CT (2010) Thermal constraints to the sporogonic development and altitudinal distribution of avian malaria Plasmodium relictum in Hawai'i. Journal of Parasitology 96, 318324.
Lively, CM, de Roode, JC, Duffy, MA, Graham, AL and Koskella, B (2014) Interesting open questions in disease ecology and evolution. The American Naturalist 184, S1S8.
Losos, JB (2011) Lizards in an Evolutionary Tree: Ecology and Adaptive Radiation of Anoles. Oakland, CA: Univ. of California Press.
Macdonald, G (1952) The analysis of equilibrium in malaria. Tropical Diseases Bulletin 49, 813829.
Martinsen, ES, Sidor, IF, Flint, S, Cooley, J and Pokras, MA (2017) Documentation of malaria parasite (Plasmodium spp.) infection and associated mortality in a common loon (Gavia immer). Journal of Wildlife Diseases 53, 859863.
McKenzie, FE, Smith, DL, O'Meara, WP and Riley, EM (2008) Strain theory of malaria: the first 50 years. Advances in Parasitology 66, 146.
Mideo, N and Day, T (2008) On the evolution of reproductive restraint inmalaria. Proceedings of the Royal Society of London B 275, 12171224.
Mordecai, EA, Paaijmans, KP, Johnson, LR, Balzer, C, Ben-Horin, T, de Moor, E, McNally, A, Pawar, S, Ryan, SJ, Smith, TC and Lafferty, KD (2013) Optimal temperature for malaria transmission is dramatically lower than previously predicted. Ecology Letters 16, 2230.
Paaijmans, KP, Blanford, S, Bell, AS, Blanford, JI, Read, AF and Thomas, MB (2010) Influence of climate on malaria transmission depends on daily temperature variation. Proceedings of the National Academy of Sciences 107, 1513515139.
Pascual, M, Ahumada, JA, Chaves, LF, Rodó, X and Bouma, M (2006) Malaria resurgence in the East African highlands: temperature trends revisited. Proceedings of the National Academy of Sciences 103, 58295834.
Peig, J and Green, AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118, 18831891.
Perkins, SL (2000) Species concepts and malaria parasites: detecting a cryptic species of Plasmodium. Proceedings of the Royal Society of London B: Biological Sciences 267, 23452350.
Petraitis, P (2013) Multiple Stable States in Natural Ecosystems. OUP, Oxford.
R core Team (2013) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
Reagan, DP (1992) Congeneric species distribution and abundance in a three-dimensional habitat: the rain forest anoles of Puerto Rico. Copeia 1992, 392403.
Reagan, DP and Waide, RB (1996) The Food Web of a Tropical Rain Forest. Chicago, IL: University of Chicago Press.
Roberts, CW, Walker, W and Alexander, J (2001) Sex-associated hormones and immunity to protozoan parasites. Clinical Microbiology Reviews 14, 476488.
Rohr, JR, Dobson, AP, Johnson, PTJ, Kilpatrick, AM, Paull, SH, Raffel, TR, Ruiz-Moreno, D and Thomas, MB (2011) Frontiers in climate change–disease research. Trends in Ecology & Evolution 26, 270277.
Schall, JJ (2002) Parasite virulence. In Lewis EE, Campbell JF and Sukhdeo MVK (eds), The Behavioural Ecology of Parasites. New York, NY: CABI, pp. 283313.
Schall, JJ and Bromwich, CR (1994) Interspecific interactions tested: two species of malarial parasite in a West African lizard. Oecologia 97, 326332.
Schall, JJ and Denis, KMS (2013) Microsatellite loci over a thirty-three year period for a malaria parasite (Plasmodium mexicanum): bottleneck in effective population size and effect on allele frequencies. Parasitology 140, 2128.
Schall, JJ and Pearson, AR (2000) Body condition of a Puerto Rican anole, Anolis gundlachi: effect of a malaria parasite and weather variation. Journal of Herpetology 34, 489491.
Schall, J, Pearson, AR and Perkins, SL (2000) Prevalence of malaria parasites (Plasmodium floridense and Plasmodium azurophilum) infecting a Puerto Rican lizard (Anolis gundlachi): a nine-year study. Journal of Parasitology 86, 511515.
Schall, J, Staats, CM and Gatten, RE Jr (2002) Virulence of lizard malaria: three species of Plasmodium infecting Anolis sabanus, the endemic anole of Saba, Netherlands Antilles. Copeia 2002, 3943.
Seppälä, O, Liljeroos, K, Karvonen, A and Jokela, J (2008) Host condition as a constraint for parasite reproduction. Oikos 117, 749753.
Smith, DL, Battle, KE, Hay, SI, Barker, CM, Scott, TW and McKenzie, FE (2012) Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathogens 8, e1002588.
Snow, RW, Sartorius, B, Kyalo, D, Maina, J, Amratia, P, Mundia, CW, Bejon, P and Noor, AM (2017) The prevalence of Plasmodium falciparum in sub-Saharan Africa since 1900. Nature 550, 515518.
Soares, L, Latta, SC and Ricklefs, RE (2017) Dynamics of avian haemosporidian assemblages through millennial time scales inferred from insular biotas of the West Indies. Proceedings of the National Academy of Sciences 201702512.
Telford, SR (2016) Hemoparasites of the Reptilia: Color Atlas and Text. Boca Raton, FL: CRC Press.
van Riper, C, van Riper, SG, Goff, ML and Laird, M (1986) The epizootiology and ecological significance of malaria in Hawaiian land birds. Ecological Monographs 56, 327344.
Vardo, AM, Wargo, AR and Schall, JJ (2005) PCR detection of lizard malaria parasites: prevalence of plasmodium infections with low-level parasitemia differs by site and season. Journal of Parasitology 91, 15091511.
Vasseur, DA, DeLong, JP, Gilbert, B, Greig, HS, Harley, CDG, McCann, KS, Savage, V, Tunney, TD and O'Connor, MI (2014) Increased temperature variation poses a greater risk to species than climate warming. Proceedings of the Royal Society of London B: Biological Sciences 281, 20132612.
Venables, WN and Ripley, BD (2013) Modern Applied Statistics with S-PLUS. New York, NY: Springer Science & Business Media.
Wilkinson, LC, Handel, CM, Van Hemert, C, Loiseau, C and Sehgal, RNM (2016) Avian malaria in a boreal resident species: long-term temporal variability, and increased prevalence in birds with avian keratin disorder. International Journal for Parasitology 46, 281290.
Wolinska, J and King, KC (2009) Environment can alter selection in host–parasite interactions. Trends in Parasitology 25, 236244.
Wunderlich, F, Mossmann, H, Helwig, M and Schillinger, G (1988) Resistance to Plasmodium chabaudi in B10 mice: influence of the H-2 complex and testosterone. Infection and Immunity 56, 24002406.
Zuk, M and McKean, KA (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26, 10091024.
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