Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T16:21:30.110Z Has data issue: false hasContentIssue false
  • English
  • Français

Circadian rhythms of trematode parasites: applying mixed models to test underlying patterns

Published online by Cambridge University Press:  16 November 2017

Emily R. Hannon ,
Dana M. Calhoun ,
Sindhu Chadalawada  and
Pieter T.J. Johnson Open the ORCID record for Pieter T.J. Johnson [Opens in a new window]
Emily R. Hannon
Affiliation:
Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
Dana M. Calhoun
Affiliation:
Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
Sindhu Chadalawada
Affiliation:
Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
Pieter T.J. Johnson*
Affiliation:
Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA
*
Author for correspondence: Pieter T. J. Johnson, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Circadian rhythms of parasites and their hosts can influence processes such as transmission, pathology and life cycle evolution. For trematode parasites that depend on free-living infectious stages (i.e. cercariae) to move among host species, the timing of parasite release is hypothesized to increase the likelihood of contacting a host. Yet, a persistent challenge in studying such biorhythms involves selection of appropriate analytical techniques. Here, we extend a generalized linear mixed modelling (GLMM) framework to cosinor analyses, thereby allowing flexibility in the statistical distribution of the response variable, incorporation of multiple covariates and inclusion of hierarchical grouping effects. By applying this approach to 93 snails infected with trematode parasites from freshwater pond ecosystems, we detected non-random rhythms in six of eight species, with variation in both the timing of peak cercariae release (between 5:10 and 21:46 h) and its magnitude (between 13 and 386). The use of GLMM yielded more accurate and precise estimates of the cosinor parameters compared with classical least-squares (LS) based on a simulation-based sensitivity analysis. The sensitivity analysis revealed that the amplitude and rhythm-adjusted mean values from the LS models diverged from the true values at some limits. We highlight the importance of novel analytical approaches for evaluating parasite circadian rhythms and investigating their underlying mechanisms.

Keywords

Circadian rhythmcircular statisticscosinor analysisgeneralized linear mixed modellinghost–parasite evolutiontrematode
Type
Research Article
Information
Parasitology , Volume 145 , Issue 6 , May 2018 , pp. 783 - 791
Check for updates
Copyright
Copyright © Cambridge University Press 2017 

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

Abdul-Salam, J and Sreelatha, BS (2004) Description and surface topography of the cercaria of Austrobilharzia sp. (Digenea: Schistosomatidae). Parasitology International 53, 11–21.Google Scholar
Ahmed, AAM, Ibrahim, NA and Idris, MA (2006) Laboratory studies on the prevalence and cercarial rhythms of trematodes from Bulinus truncates and Biomphalaria pfeifferi snails from Khartoum State, Sudan. Sultan Qaboos University Medical Journal 6, 65–69.Google Scholar
Aoki, Y, Fujimaki, Y and Isao, T (2011) Basic studies on filarial and filiariasis. Tropical Medicine and Health 39(Suppl. 2), 51–55.Google Scholar
Barnett, AG, Baker, PJ and Dobson, AJ (2014) Season: analyzing seasonal data R functions. Version 0.3-5. Available at https://cran.r-project.org/web/packages/season/season.pdf.Google Scholar
Bolker, BM, Brooks, ME, Clark, CJ, Geange, SW, Poulsen, JR, Stevens, MHH and White, JS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution 24, 127–135.Google Scholar
Burnham, KP and Anderson, DR (2004) Multimodel inference – understanding AIC and BIC in model selection. Sociological Methods & Research 33, 261–304.Google Scholar
Combes, C (2001) Parasitism. Chicago, IL: University of Chicago Press.Google Scholar
Cornelissen, G (2014) Cosinor-based rhythmometry. Theoretical Biology & Medical Modelling 11, 1–24.Google Scholar
Cort, WW (1922) A study of the escape of cercariae from their snail hosts. Journal of Parasitology 8, 177–184.Google Scholar
Craig, JM and Scott, AL (2014) Helminths in the lungs. Parasite Immunology 36, 463–474.Google Scholar
Davies, D and de Núñez, MO (2012) The life cycle of Australapatemon magnacetabulum (Digenea: Strigeidae) from northwestern Argentina. Journal of Parasitology 98, 778–783.Google Scholar
Dreyer, G, Pimentael, A, Medeiros, Z, Béliz, F, Moura, I, Coutinho, A, Andrade, LD, Rocha, A, Silva, LM and Piessens, WF (1996) Studies on the periodicity and intravascular distribution of Wuchereria bancrofti microfilariae in paired samples of capillary and venous blood from Recife, Brazil. Tropical Medicine & International Health 1, 264–272.Google Scholar
Faltynkova, A, Karvonen, A, Jyrkka, M and Valtonen, ET (2009) Being successful in the world of narrow opportunities: transmission patterns of the trematode Ichthyocotylurus pileatus. Parasitology 136, 1375–1382.Google Scholar
Farrance, I and Frenkel, R (2014) Uncertainty in measurement: a review of Monte Carlo simulation using Microsoft Excel for the calculation of uncertainties through functional relationships, including uncertainties in empirically derived constants. Clinical Biochemist Reviews 35, 37–61.Google Scholar
Favre, TC, Bogéa, T, Rotenberg, L, Silva, HS and Pieri, OS (1997) Circadian rhythms in the cercarial emergence of Schistosoma mansoni by Biomphalaria tenagophila at outdoors: a comparative study with Biomphalaria glabrata. Biological Rhythm Research 28, 348–357.Google Scholar
Fenwick, A (2012) The global burden of neglected tropical diseases. Public Health 126, 233–236.CrossRefGoogle ScholarPubMed
Fingerut, JT, Zimmer, CA and Zimmer, RK (2003) Patterns and processes of larval emergence in an estuarine parasite system. The Biological Bulletin 205, 110–120.Google Scholar
Fraker, ME (2008) The influence of the circadian rhythm of green frog (Rana clamitans) tadpoles on their antipredator behavior and the strength of the nonlethal effects of predators. The American Naturalist 171, 545–552.Google Scholar
Fried, B and Ponder, EL (2003) Effects of temperature on survival, infectivity and in vitro encystment of the cercariae of Echinostoma caproni. Journal of Helminthology 77, 235–238.Google Scholar
Greene, W (2008) Functional forms for the negative binomial model for count data. Economics Letters 99, 585–590.Google Scholar
Harding, B, Tremblay, C and Cousineau, D (2014) Standard errors: a review and evaluation of standard error estimators using Monte Carlo simulations. The Quantitative Methods for Psychology 10, 107–123.Google Scholar
Hawking, F (1967) The 24-hour periodicity of microfilariae: biological mechanisms responsible for its production and control. Proceedings of the Royal Society of London B 169, 59–76.Google Scholar
Johnson, AD (1968) Life history of Alaria marcianae (La Rue, 1917) Walton, 1949 (Trematoda: Diplostomatidae). Journal of Parasitology 54, 324–332.Google Scholar
Johnson, PTJ, Dobson, A, Lafferty, KD, Marcogliese, DJ, Memmott, J, Orlofske, SA, Poulin, R and Thieltges, DW (2010) When parasites become prey: ecological and epidemiological significance of eating parasites. Trends in Ecology & Evolution 25, 362–371.Google Scholar
Johnson, PTJ, Preston, DL, Hoverman, JT and Richgels, KLD (2013) Biodiversity reduces disease through predictable changes in host community competence. Nature 494, 230–234.Google Scholar
Kanev, I, Fried, B, Dimitrov, V and Radev, V (1995) Redescription of Echinostoma trivolvis (Cort, 1914) (Trematoda: Echinostomatidae) with a discussion on its identity. Systematic Parasitology 32, 61–70.Google Scholar
Kaplan, AT, Rebhal, S, Lafferty, KD and Kuris, AM (2009) Small estuarine fishes feed on large trematode cercariae: lab and field investigations. Journal of Parasitology 95, 477–480.Google Scholar
Karvonen, A, Paukku, S, Valtonen, ET and Hudson, PJ (2003) Transmission, infectivity and survival of Diplostomum spathaceum cercariae. Journal of Parasitology 127, 217–224.Google Scholar
Kavaliers, M (1981) Circadian and ultradien activity rhythms of a freshwater gastropod, Helisoma trivolvis: the effects of social factors and eye removal. Behavioral and Neural Biology 32, 350–363.Google Scholar
Keeler, SP and Huffman, JE (2009) Echinostomes in the second intermediate host. In Fried, B and Toledo, R (eds). The Biology of Echinostomes, New York, NY: Springer Science, pp. 61–87.Google Scholar
Khan, AM, Dutta, P, Das, S, Pathak, AK, Sarmah, P, Hussain, ME and Mahanta, J (2015) Microfilarial periodicity of Wuchereria bancrofti in Assam, Northeast India. Journal of Vector Borne Diseases 52, 208–212.Google Scholar
Komatsu, S, Daisuke, K, Paller, BGV and Uga, S (2014) Dynamics of Centrocestus armatus transmission in endemic river in Hyogo Prefecture, Japan. Tropical Medicine and Health 42, 35–42.Google Scholar
Kuris, AM and Lafferty, KD (1994) Community structure: larval trematodes in snail hosts. Annual Review of Ecology and Systematics 25, 189–217.Google Scholar
Lang, BZ (1968) The life cycle of Cephalogonimus americanus Stafford 1902 (trematoda: Cephalogonimidae). Journal of Parasitology 54, 945–949.Google Scholar
Lee, JH, Han, G and Giuliano, AR (2012) Analysis of overdispersed count data: application to the human papillomavirus infection in men (HIM) study. Epidemiology & Infection 140, 1087–1094.Google Scholar
Lee Gierke, C, Cornelissen, G and Lindgren, J (2013) CAT: Chronomics Analysis Toolkit. University of Minnesota. Available at http://564394709114639785.weebly.com/installing-cat.html.Google Scholar
Lu, D, Wang, T, Rudge, JW, Donnelly, CA, Fang, G and Websteer, JP (2009) Evolution in a multi-host parasite: chronobiological circadian rhythm and population genetics of Schistosoma japonicum cercariae indicates contrasting definitive host reservoirs by habitat. International Journal of Parasitology 39, 1581–1588.Google Scholar
Mintsa-Nguéma, R, Mone, H, Ibikounle, M, Mengue-Ngou-Milama, K, Kombila, M and Mouahid, G (2014) Cercarial emergence pattern of Schistosoma haematobium from Libreville, Gabon. Parasitology 21, 1–5.Google Scholar
Mouahid, G, Idris, MA, Verneau, O, Théron, A and Shaban, MMA (2012) A new chronotype of Schistosoma mansoni: adaptive significance. Tropical Medicine & International Health 17, 727–732.Google Scholar
Mouritsen, KN (2002) The Hydrobia ulvae-Maritrema subdolum association: influence of temperature, salinity, light, water-pressure and secondary host exudates on cercarial emergence and longevity. Journal of Helminthology 76, 341.Google Scholar
N'Goran, E, Brémond, P, Sellin, E, Sellin, B and Théron, A (1997) Intraspecific diversity of Schistosoma haematobium in West Africa: chronobiology of cercarial emergence. Acta Tropica 66, 35–44.Google Scholar
Núñez, MO, Davies, D and Spatz, L. (2011) The life cycle of Zygocotyle lunata (Trematoda, Paramphistomoidea) in the subtropical region of South America. Revista Mexicana de Biodiversidad 82, 581–588.Google Scholar
Oishi, T, Nagai, K, Harada, Y, Naruse, M, Ohtani, M, Kawano, E and Tamotsu, S (2004) Circadian rhythms in amphibians and reptiles: ecological implications. Biological Rhythm Research 35, 105–120.Google Scholar
Orlofske, SA, Jadin, RC, Preston, DL and Johnson, PTJ (2012) Parasite transmission in complex communities: predators and alternative hosts alter pathogenic infections in amphibians. Ecology 93, 1247–1253.Google Scholar
Orlofske, SA, Jadin, RC and Johnson, PTJ (2015) It's a predator-eat-parasite world: how characteristics of predator, parasite and environment affect consumption. Oecologia 178, 537–547.Google Scholar
Parker, GA, Chubb, JC, Ball, MA and Roberts, GN (2003) Evolution of complex life cycles in helminth parasites. Nature 425, 480–484.Google Scholar
Paull, SH and Johnson, PTJ (2014) Experimental warming drives a seasonal shift in the timing of host-parasite dynamics with consequences for disease risk. Ecology Letters 17, 445–453.Google Scholar
R Core Team (2016) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.R-project.org/.Google Scholar
Refinetti, R, Cornelissen, G and Halberg, F (2007) Procedures for numerical analysis of circadian rhythms. Biological Rhythm Research 38, 275–325.Google Scholar
Revelle, W (2016) Psych: Procedures for Personality and Psychological Research. Evanston, Illinois, USA: Northwestern University. Version 1.5.8. Available at http://CRAN.R-project.org/package=psych.Google Scholar
Ripley, B, Venables, B, Bates, DM, Hornik, K, Gebhardt, A and Firth, D (2016) Package ‘MASS’. Version 7.3-45. CRAN repository. Available at https://cran.r-project.org/web/packages/MASS/MASS.pdf.Google Scholar
Sachs, M (2014) Cosinor: Tools for estimating and predicting the cosinor model. Version 1.1. Available at https://CRAN.R-project.org/package=cosinor.Google Scholar
Schell, SC (1985) Handbook of Trematodes of North America North of Mexico. Moscow, ID: Idaho Research Foundation.Google Scholar
Shaw, DJ, Grenfell, BT and Dobson, AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.Google Scholar
Silva, HS, Rotenberg, L, Bogéa, T, Favre, TC and Pieri, O (1995) Longitudinal study of circadian rhythms in the cercarial emergence of Schistosoma mansoni from Biomphalaria glabrata. Memórias do Instituto Oswaldo Cruz 90, 459–461.Google Scholar
Skaug, H, Fournier, D, Bolker, B, Magnusson, A and Nielsen, A (2016) Generalized linear mixed models using ‘AD Model Builder’. Version 0.8.3.3. Available at http://glmmadmb.r-forge.r-project.org.Google Scholar
Soldánová, M, Selbach, C and Sures, B (2016) The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLoS One 11, e0149678.Google Scholar
Steinauer, ML, Mwangi, IN, Maina, GM, Kinuthia, JM, Mutuku, MW, Agola, EL, Mungai, B, Mkoji, GM and Loker, ES (2008) Interactions between natural populations of human and rodent schistosomes in the Lake Victoria region of Kenya: a molecular epidemiological approach. PLoS Neglected Tropical Diseases 2, e222.Google Scholar
Su, J, Zhou, F and Lu, D (2013) A circular analysis of chronobiology of Schistosoma japonicum cercarial emergence from hilly areas of Anhui, China. Experimental Parasitology 135, 421–425.Google Scholar
Sulieman, Y, Pengskul, T and Guo, Y (2013) Development and effects of Schistosoma japonicum (Trematoda) on its intermediate host, Oncomelania hupensis (Gastropoda). Iranian Journal Parasitology 8, 212–218.Google Scholar
Symonds, MRE and Moussalli, A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike's information criterion. Behavioral Ecology and Sociobiology 65, 13–21.Google Scholar
Théron, A (2015) Chronobiology of trematode cercarial emergence: from data recovery to epidemiological, ecological and evolutionary implications. Advances in Parasitology 88, 123–164.Google Scholar
Thieltges, DW, Jensen, KT and Poulin, R (2008) The role of biotic factors in the transmission of free-living endohelminth stages. Journal of Parasitology 135, 407–426.Google Scholar
Valle, C, Pellegrino, J and Alvarenga, N (1973) Rhythmic emergence of Schistosoma mansoni cercariae from Biomphalaria glabrata: influence of temperature. Journal of the São Paulo Institute of Tropical Medicine 15, 195–201.Google Scholar
Wang, C, Lu, D, Guo, C, Li, Y, Gao, Y, Bian, C and Su, J (2014) Compatibility of Schistosoma japonicum from the hilly region and Oncomelania hupensis hupensis from the marshland region within Anhui, China. Parasitology Research 113, 4477–4484.Google Scholar
Wang, S, Zhu, Y, Ge, Q, Yang, M, Huang, J, Huang, W, Zhuge, H and Lu, D (2015) Effect of photoperiod change on chronobiology of cercarial emergence of Schistosoma japonicum derived from hilly and marshy regions of China. Experimental Parasitology 159, 227–232.Google Scholar
Williams, CL, Wessels, WS and Gilbertson, DE (1984) Comparison of the rhythmic emergence of Schistosoma mansoni cercariae from Biomphalaria glabrata in different lighting regimens. Journal Parasitology 70, 450–452.Google Scholar
Zuur, AF, Leno, EN, Walker, NJ, Saveliev, AA and Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. New York, NY: Springer.Google Scholar
Supplementary material: File

Hannon et al supplementary materials

Appendix

Download Hannon et al supplementary materials(File)
File 8.6 MB