Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T03:12:18.713Z Has data issue: false hasContentIssue false
  • English
  • Français

Temperature-related parasite infection dynamics: the case of proliferative kidney disease of brown trout

Published online by Cambridge University Press:  23 August 2017

NICOLE STREPPARAVA Open the ORCID record for NICOLE STREPPARAVA [Opens in a new window] ,
HELMUT SEGNER ,
ALBERT ROS ,
HANNA HARTIKAINEN ,
HEIKE SCHMIDT-POSTHAUS  and
THOMAS WAHLI
NICOLE STREPPARAVA*
Affiliation:
Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty, Centre for Fish and Wildlife Health, University of Bern, Länggassstrasse 122, 3012 Bern, Switzerland
HELMUT SEGNER
Affiliation:
Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty, Centre for Fish and Wildlife Health, University of Bern, Länggassstrasse 122, 3012 Bern, Switzerland
ALBERT ROS
Affiliation:
Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty, Centre for Fish and Wildlife Health, University of Bern, Länggassstrasse 122, 3012 Bern, Switzerland LAZBW, Fischereiforschungsstelle, Argenweg 50/1, 88085 Langenargen, Germany
HANNA HARTIKAINEN
Affiliation:
ETH and Eawag, Institute for Integrative Biology, Ueberlandstrasse 133, 8600 Duebendorf, Switzerland
HEIKE SCHMIDT-POSTHAUS
Affiliation:
Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty, Centre for Fish and Wildlife Health, University of Bern, Länggassstrasse 122, 3012 Bern, Switzerland
THOMAS WAHLI
Affiliation:
Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty, Centre for Fish and Wildlife Health, University of Bern, Länggassstrasse 122, 3012 Bern, Switzerland
*
*Corresponding author: Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty, Centre for Fish and Wildlife Health, University of Bern, Länggassstrasse 122, 3012 Bern, Switzerland. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Climate change, in particular rising temperature, is suspected to be a major driver for the emergence of many wildlife diseases. Proliferative kidney disease of salmonids, caused by the myxozoan Tetracapsuloides bryosalmonae, was used to evaluate how temperature dependence of host–parasite interactions modulates disease emergence. Brown trout (Salmo trutta fario) kept at 12 and 15 °C, were experimentally infected with T. bryosalmonae. Parasite development in the fish host and release of spores were quantified simultaneously to unravel parasite transmission potential from the vertebrate to the invertebrate host. A change to a stable plateau in infection intensity of the kidney coincided with a threshold at which spore shedding commenced. This onset of parasite release was delayed at the low temperature in accordance with reaching this infection intensity threshold, but the amount of spores released was irrespective of temperature. The production of parasite transmission stages declined with time. In conclusion, elevated temperature modifies the parasite transmission opportunities by increasing the duration of transmission stage production, which may affect the spread and establishment of the parasite in a wider range of rivers.

Keywords

brown trouthost–parasite interactionparasite kineticsparasite sheddingproliferative kidney diseasetemperatureTetracapsuloides bryosalmonae
Type
Research Article
Information
Parasitology , Volume 145 , Issue 3 , March 2018 , pp. 281 - 291
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

Adlard, R. D., Miller, T. L. and Smit, N. J. (2015). The butterfly effect: parasite diversity, environment, and emerging disease in aquatic wildlife. Trends in Parasitology 31, 160–166.Google Scholar
Anacker, R. L. and Ordal, E. J. (1959). Studies on the myxobacterium Chondrococcus columnaris. II. Bacteriocins. Journal of Bacteriology 78, 33–40.CrossRefGoogle ScholarPubMed
Bailey, C., Segner, H., Casanova-Nakayama, A. and Wahli, T. (2017). Who needs the hotspot? The effect of temperature on the fish host immune response to Tetracapsuloides bryosalmonae the causative agent of proliferative kidney disease. Fish & Shellfish Immunology 63, 424–437.Google Scholar
Baldwin, T. J., Vincent, E. R., Silflow, R. M. and Stanek, D. (2000). Myxobolus cerebralis infection in rainbow trout (Oncorhynchus mykiss) and brown trout (Salmo trutta) exposed under natural stream conditions. Journal of Veterinary Diagnostic Investigation 12, 312–321.Google Scholar
Bates, D., Machler, M., Bolker, B. M. and Walker, S. C. (2015). Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.Google Scholar
Bettge, K., Segner, H., Burki, R., Schmidt-Posthaus, H. and Wahli, T. (2009 a). Proliferative kidney disease (PKD) of rainbow trout: temperature- and time-related changes of Tetracapsuloides bryosalmonae DNA in the kidney. Parasitology 136, 615–625.Google Scholar
Bettge, K., Wahli, T., Segner, H. and Schmidt-Posthaus, H. (2009 b). Proliferative kidney disease in rainbow trout: time- and temperature-related renal pathology and parasite distribution. Diseases of Aquatic Organisms 83, 67–76.CrossRefGoogle ScholarPubMed
Bowden, T. J. (2008). Modulation of the immune system of fish by their environment. Fish & Shellfish Immunology 25, 373–383.Google Scholar
Bruneaux, M., Visse, M., Gross, R., Pukk, L., Saks, L. and Vasemägi, A. (2017). Parasite infection and decreased thermal tolerance: impact of proliferative kidney disease on a wild salmonid fish in the context of climate change. Functional Ecology 31, 216–226.Google Scholar
Cheng, A. C., Cheng, S. A., Chen, Y. Y. and Chen, J. C. (2009). Effects of temperature change on the innate cellular and humoral immune responses of orange-spotted grouper Epinephelus coioides and its susceptibility to Vibrio alginolyticus . Fish & Shellfish Immunology 26, 768–772.Google Scholar
Chilmonczyk, S., Monge, D. and de Kinkelin, P. (2002). Proliferative kidney disease: cellular aspects of the rainbow trout, Oncorhynchus mykiss (Walbaum), response to parasitic infection. Journal of Fish Diseases 25, 217–226.CrossRefGoogle Scholar
Dash, M. and Vasemagi, A. (2014). Proliferative kidney disease (PKD) agent Tetracapsuloides bryosalmonae in brown trout populations in Estonia. Diseases of Aquatic Organisms 109, 139–148.CrossRefGoogle ScholarPubMed
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2000). Emerging infectious diseases of wildlife – threats to biodiversity and human health. Science 287, 443–449.Google Scholar
de Kinkelin, P., Gay, M. and Forman, S. (2002). The persistence of infectivity of Tetracapsula bryosalmonae-infected water for rainbow trout, Oncorhynchus mykiss (Walbaum). Journal of Fish Diseases 25, 477–482.Google Scholar
de Micheaux, P., Drouilhet, R. and Liquet, B. (2013). Programming in R. In The R Software Vol. 40, pp. 193–282. Springer, New York.Google Scholar
El-Matbouli, M., McDowell, T. S., Antonio, D. B., Andree, K. B. and Hedrick, R. P. (1999). Effect of water temperature on the development, release and survival of the triactinomyxon stage of Myxobolus cerebralis in its oligochaete host. International Journal for Parasitology 29, 627–641.Google Scholar
Feist, S. W., Longshaw, M., Canning, E. U. and Okamura, B. (2001). Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae . Diseases of Aquatic Organisms 45, 61–68.CrossRefGoogle ScholarPubMed
Fey, S. B., Siepielski, A. M., Nussle, S., Cervantes-Yoshida, K., Hwan, J. L., Huber, E. R., Fey, M. J., Catenazzi, A. and Carlson, S. M. (2015). Recent shifts in the occurrence, cause, and magnitude of animal mass mortality events. Proceedings of the National Academy of Sciences of the United States of America 112, 1083–1088.Google Scholar
Fiala, I., Bartošová-Sojková, P., Okamura, B. and Hartikainen, H. (2015). Adaptive radiation and evolution within the myxozoa. In Myxozoan Evolution, Ecology and Development (ed. Okamura, B., Gruhl, A. and Bartholomew, J. L.), pp. 85–110. Springer International Publishing, Switzerland.Google Scholar
Fischer, U., Ototake, M. and Nakanishi, T. (1999). Effect of environmental temperature on in vitro cell-mediated cytotoxicity (CMC) and graft-versus-host reaction (GVHR) in ginbuna crucian carp (Carassius auratus langsdorfii). Fish & Shellfish Immunology 9, 233–236.Google Scholar
Freyhof, J. (2013). Salmo trutta. The IUCN Red List of Threatened Species 2013: e.T19861A9050312.Google Scholar
Froese, R. and Pauly, D. (2016). FishBase. World Wide Web electronic publication. http://www.fishbase.org.Google Scholar
Gallana, M., Ryser-Degiorgis, M. P., Wahli, T. and Segner, H. (2013). Climate change and infectious diseases of wildlife: altered interactions between pathogens, vectors and hosts. Current Zoology 59, 427–437.Google Scholar
Gorgoglione, B., Wang, T., Secombes, C. J. and Holland, J. W. (2013). Immune gene expression profiling of Proliferative Kidney Disease in rainbow trout Oncorhynchus mykiss reveals a dominance of anti-inflammatory, antibody and T helper cell-like activities. Veterinary Research 44, 55.Google Scholar
Grabner, D. S. and El-Matbouli, M. (2010). Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Parasitology 137, 629–639.Google Scholar
Hartikainen, H. and Okamura, B. (2015). Ecology and evolution of Malacosporean-Bryozoan interactions. In Myxozoan Evolution, Ecology and Development (ed. Okamura, B., Gruhl, A. and Bartholomew, J. L.), pp. 201–216. Springer International Publishing, Switzerland.Google Scholar
Harvell, C. D., Mitchell, C. E., Ward, J. R., Altizer, S., Dobson, A. P., Ostfeld, R. S. and Samuel, M. D. (2002). Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.Google Scholar
Hellemans, J., Mortier, G., De Paepe, A., Speleman, F. and Vandesompele, J. (2007). Qbase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biology 8, R19.Google Scholar
Johnson, A. C., Acreman, M. C., Dunbar, M. J., Feist, S. W., Giacomello, A. M., Gozlan, R. E., Hinsley, S. A., Ibbotson, A. T., Jarvie, H. P., Jones, J. I., Longshaw, M., Maberly, S. C., Marsh, T. J., Neal, C., Newman, J. R., Nunn, M. A., Pickup, R. W., Reynard, N. S., Sullivan, C. A., Sumpter, J. P. and Williams, R. J. (2009). The British river of the future: how climate change and human activity might affect two contrasting river ecosystems in England. Science of the Total Environment 407, 4787–4798.Google Scholar
Jokinen, I. E., Salo, H. M., Markkula, E., Rikalainen, K., Arts, M. T. and Browman, H. I. (2011). Additive effects of enhanced ambient ultraviolet B radiation and increased temperature on immune function, growth and physiological condition of juvenile (parr) Atlantic Salmon, Salmo salar . Fish & Shellfish Immunology 30, 102–108.Google Scholar
Joly, P., Falconnet, P. A., Andre, J., Weill, N., Reyrolle, M., Vandenesch, F., Maurin, M., Etienne, J. and Jarraud, S. (2006). Quantitative real-time Legionella PCR for environmental water samples: data interpretation. Applied and Environmental Microbiology 72, 2801–2808.Google Scholar
Karvonen, A., Rintamaki, P., Jokela, J. and Valtonen, E. T. (2010). Increasing water temperature and disease risks in aquatic systems: climate change increases the risk of some, but not all, diseases. International Journal for Parasitology 40, 1483–1488.Google Scholar
Kollner, B. and Kotterba, G. (2002). Temperature dependent activation of leucocyte populations of rainbow trout, Oncorhynchus mykiss, after intraperitoneal immunisation with Aeromonas salmonicida . Fish & Shellfish Immunology 12, 35–48.Google Scholar
Kollner, B., Wasserrab, B., Kotterba, G. and Fischer, U. (2002). Evaluation of immune functions of rainbow trout (Oncorhynchus mykiss) – how can environmental influences be detected? Toxicology Letters 131, 83–95.Google Scholar
Lom, J. and Dykova, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica (Praha) 53, 1–36.CrossRefGoogle ScholarPubMed
Mackay, I. M. (2004). Real-time PCR in the microbiology laboratory. Clinical Microbiology and Infection 10, 190–212.Google Scholar
Marcos-Lopez, M., Gale, P., Oidtmann, B. C. and Peeler, E. J. (2010). Assessing the impact of climate change on disease emergence in freshwater fish in the United Kingdom. Transboundary and Emerging Diseases 57, 293–304.CrossRefGoogle ScholarPubMed
Maricondi-Massari, M., Kalinin, A. L., Glass, M. L. and Rantin, F. T. (1998). The effects of temperature on oxygen uptake, gill ventilation and ecg waveforms in the Nile tilapia, Oreochromis niloticus . Journal of Thermal Biology 23, 283–290.CrossRefGoogle Scholar
Morris, D. J. and Adams, A. (2006). Transmission of freshwater myxozoans during the asexual propagation of invertebrate hosts. International Journal for Parasitology 36, 371–377.Google Scholar
Morris, D. J., Ferguson, H. W. and Adams, A. (2005). Severe, chronic proliferative kidney disease (PKD) induced in rainbow trout Oncorhynchus mykiss held at a constant 18 degrees C. Diseases of Aquatic Organisms 66, 221–226.CrossRefGoogle Scholar
Noe, J. G. and Dickerson, H. W. (1995). Sustained growth of Ichthyophthirius multifiliis at low temperature in the laboratory. Journal of Parasitology 81, 1022–1024.Google Scholar
Okamura, B., Hartikainen, H., Schmidt-Posthaus, H. and Wahli, T. (2011). Life cycle complexity, environmental change and the emerging status of salmonid proliferative kidney disease. Freshwater Biology 56, 735–753.Google Scholar
Paull, S. H. and Johnson, P. T. J. (2011). High temperature enhances host pathology in a snail–trematode system: possible consequences of climate change for the emergence of disease. Freshwater Biology 56, 767–778.Google Scholar
Perry, A. L., Low, P. J., Ellis, J. R. and Reynolds, J. D. (2005). Climate change and distribution shifts in marine fishes. Science 308, 1912–1915.CrossRefGoogle ScholarPubMed
Ray, R. A. and Bartholomew, J. L. (2013). Estimation of transmission dynamics of the Ceratomyxa shasta actinospore to the salmonid host. Parasitology 140, 907–916.Google Scholar
Ray, R. A., Holt, R. A. and Bartholomew, J. L. (2012). Relationship between temperature and Ceratomyxa shasta-induced mortality in Klamath River salmonids. Journal of Parasitology 98, 520–526.Google Scholar
R Core Team (2014). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Schmidt-Posthaus, H., Bettge, K., Forster, U., Segner, H. and Wahli, T. (2012). Kidney pathology and parasite intensity in rainbow trout Oncorhynchus mykiss surviving proliferative kidney disease: time course and influence of temperature. Diseases of Aquatic Organisms 97, 207–218.Google Scholar
Segner, H., Wahli, T. and Burkhardt-Holm, P. (2012). Combined effects of parasites, climate and pollution on brown trout, Salmo trutta, in Swiss rivers. Comparative Biochemistry and Physiology a – Molecular & Integrative Physiology 163, S40–S40.Google Scholar
Studer, A., Thieltges, D. W. and Poulin, R. (2010). Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Marine Ecology Progress Series 415, 11–22.Google Scholar
Thieltges, D. W. and Rick, J. (2006). Effect of temperature on emergence, survival and infectivity of cercariae of the marine trematode Renicola roscovita (Digenea: Renicolidae). Diseases of Aquatic Organisms 73, 63–68.Google Scholar
Tops, S., Baxa, D. V., McDowell, T. S., Hedrick, R. P. and Okamura, B. (2004). Evaluation of malacosporean life cycles through transmission studies. Diseases of Aquatic Organisms 60, 109–121.Google Scholar
Tops, S., Lockwood, W. and Okamura, B. (2006). Temperature-driven proliferation of Tetracapsuloides bryosalmonae in bryozoan hosts portends salmonid declines. Diseases of Aquatic Organisms 70, 227–236.Google Scholar
Tops, S., Hartikainen, H. L. and Okamura, B. (2009). The effects of infection by Tetracapsuloides bryosalmonae (Myxozoa) and temperature on Fredericella sultana (Bryozoa). International Journal for Parasitology 39, 1003–1010.CrossRefGoogle ScholarPubMed
Vassella, E., Reuner, B., Yutzy, B. and Boshart, M. (1997). Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. Journal of Cell Science 110, 2661–2671.Google Scholar
Vornanen, M., Haverinen, J. and Egginton, S. (2014). Acute heat tolerance of cardiac excitation in the brown trout (Salmo trutta fario). Journal of Experimental Biology 217, 299–309.Google Scholar
Williams, P., Winzer, K., Chan, W. C. and Camara, M. (2007). Look who's talking: communication and quorum sensing in the bacterial world. Philosophical Transactions of the Royal Society of London B Biological Sciences 362, 1119–1134.Google Scholar
Yun, J. J., Heisler, L. E., Hwang, I. I., Wilkins, O., Lau, S. K., Hyrcza, M., Jayabalasingham, B., Jin, J., McLaurin, J., Tsao, M. S. and Der, S. D. (2006). Genomic DNA functions as a universal external standard in quantitative real-time PCR. Nucleic Acids Research 34, e85.Google Scholar
Supplementary material: File

Strepparava et al. supplementary material

Strepparava et al. supplementary material 1

Download Strepparava et al. supplementary material(File)
File 417.7 KB