Skip to main content
SpringerLink
Log in

Spatial epidemiology model can explain the seasonal dynamics of infectious disease Cyprinid herpesvirus 3 (CyHV-3) by thermoregulation behavior of the host, common carp (Cyprinus carpio)

Theoretical Ecology Aims and scope Submit manuscript

Cite this article

Abstract

For ectotherms, habitat temperature is one of the most fundamental factors responsible for disease dynamics. Therefore, temperature-dependent habitat selection of hosts could alter their susceptibility to pathogens. Here, we examined the effect of host behavior in the fluctuating thermal regime on disease dynamics, by a dynamical modeling with field surveys. Cyprinid herpesvirus 3 (CyHV-3) was used as a model disease, which is a mass mortality agent of common carp (Cyprinus carpio). Telemetry analysis revealed that carp shifted their location according to the temporal fluctuations of the thermal regime in the habitat, suggesting a preference for specific temperatures. Numerical simulation using a disease transmission model reproduced the characteristic bimodal seasonal trends of infection rate to CyHV-3. The simulation demonstrated that the temperature preference of individual carp was central in determining whether the temperature-dependent behavior ameliorates or exacerbates disease severity. Moreover, it also demonstrated that increases in the fraction of warmer coastal areas can mitigate the impact of CyHV-3 on the carp population by promoting the acquisition of immunity. Our findings suggest that the prevalence of infectious disease in poikilothermic animals can be regulated by the combined effects of the thermal regime of their habitat and the host’s thermally induced behavior.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The main part of the programming code for this study is available at https://github.com/tksmiki/theor-ecol2023.

References

  • Arai M, Yanai T, Takashima Y (2006) A survey of koi herpesvirus (KHV) in the wild carp of Lake Kasumigaura and Kitaura. Bull Ibaraki Pref Freshw Fish Exp Stat 40:37–43 (in Japanese)

    Google Scholar 

  • Carey C, Cohen N, Rollins-Smith L (1999) Amphibian declines: an immunological perspective. Dev Comp Immunol 23:459–472

    Article  CAS  PubMed  Google Scholar 

  • Dong C, Li X, Weng S, Xe S, He J (2013) Emergence of fatal European genotype CyHV-3/KHV in mainland China. Vet Microbiol 162:239–244

    Article  PubMed  Google Scholar 

  • Durr PA, Davis S, Joehnk K, Graham K, Hopf J, McColl KA, Taylor S, Chen Y, Sengupta A, Merrin L, Stratford D, Aryal S, van Klinken RD, West P, Newton M, Brown P, Gilligan D (2019) Development of hydrological, ecological and epidemiological modelling to inform a CyHV3 release strategy for the biocontrol of carp in the murray darling basin: part a. Integrated Ecological and Epidemiological Modelling. FRDC, Canberra. http://www.frdc.com.au/project/2016–170

  • Froese R, Pauly D (2010) FishBase. World Wide Web electronic publication. version (04/2013). www.fishbase.org

  • Gilad O, Yun S, Adkison MA, Way K, Willits NH, Bercovier H, Hedrick RP (2003) Molecular comparison of isolates of an emerging fish pathogen koi herpesvirus and the effect of water temperature on mortality of experimentally infected koi. J Gen Virol 84:2661–2668

    Article  CAS  PubMed  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS et al (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    Article  CAS  PubMed  Google Scholar 

  • Hedrick RP, Gilad O, Yun S, Spangenberg JV, Marty GD, Nordhausen RW et al (2000) A herpesvirus associated with mass mortality of juvenile and adult koi, a strain of common carp. J Aquat Anim Health 12:44–57

    Article  CAS  PubMed  Google Scholar 

  • Hedrick RP, Gilad O, Yun SC, McDowell TS, Waltzek TB, Kelley GO et al (2005) Initial isolation and characterization of a herpes-like virus (KHV) from koi and common carp. Bull Fish Res Agency S2:1–7

    Google Scholar 

  • Huey RB (1974) Behavioral thermoregulation in lizards: importance of associated costs. Science 184:1001–1003

    Article  Google Scholar 

  • Hutchison VH, Maness JD (1979) The role of behavior in temperature acclimation and tolerance in ectotherms. Am Zool 19:367–384

    Article  Google Scholar 

  • Iida T, Sano M (2005) Koi Herpesvirus Disease Virus 55:145–152 (in Japanese)

    PubMed  Google Scholar 

  • Kelsch SW, Neill WH (1990) Temperature preference versus acclimation in fishes: selection for changing metabolic optima. Trans Am Fish Soc 119:601–610

    Article  Google Scholar 

  • Klein MS, Conn CA, Kluger MJ (1992) Behavioral thermoregulation in mice inoculated with influenza virus. Physiol Behav 52:1133–1139

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Ke H, Ma Y, Hao L, Ma J, Liang Z, Chen Z (2016) First report of occurrences of two cyprinid herpesvirus 3 variants, I++ II− and I++ II+Δ, in China. Fish Pathol 51:169–175

    Article  Google Scholar 

  • Matsui K, Honjo M, Kohmatsu Y, Uchii K, Yonekura R, Kawabata Z (2008) Detection and significance of koi herpesvirus (KHV) in freshwater environments. Fresh Biol 53:1262–1272

  • Magnuson JJ, DeStasio BT (1997) Thermal niche of fishes and global warming. In: Wood CM McDonald DG (eds) Global Warming: Implications for Freshwater and Marine Fish. Cambridge University Press, Cambridge, pp 377–408

  • Manning MJ, Nakanishi T (1996) The specific immune system: cellular defences. In: Iwama G, Nakanishi T (eds) The fish immune system. Howar WS, Randall DJ, Farrell AP (eds) Fish physiology, vol 15. Academic Press, San Diego, pp 159–205

  • Ouedraogo RM, Goettel MS, Brodeur J (2004) Behavioral thermoregulation in the migratory locust: a therapy to overcome fungal infection. Oecologia 138:312–319

    Article  CAS  PubMed  Google Scholar 

  • Perelberg A, Smirnov M, Hutoran M, Diamant A, Bejerano Y, Kotler M (2003) Epidemiological description of a new viral disease afflicting cultured Cyprinus carpio in Israel. Isr J Aquacult Bamidgeh 55:5–12

    Google Scholar 

  • Perelberg A, Ronen A, Hutoran M, Smith Y, Kotler M (2005) Protection of cultured Cyprinus carpio against a lethal viral disease by an attenuated virus vaccine. Vaccine 23:3396–3403

    Article  CAS  PubMed  Google Scholar 

  • Primack RB (2002) Essentials of conservation biology, 3rd edn. Sinauer Associates, Sunderland

    Google Scholar 

  • Rakus K, Ronsmans M, Vanderplasschen A (2017a) Behavioral fever in ectothermic vertebrates. Dev Comp Immunol 66:84–91

    Article  PubMed  Google Scholar 

  • Rakus K, Ronsmans M, Forlenza M, Boutier M, Piazzon MC, Jazowiecka-Rakus J, Gatherer D, Athanasiadis A, Farnir F, Davison AJ, Boudinot P, Michiels T, Wiegertjes GF, Vanderplasschen A (2017b) Conserved fever pathways across vertebrates: a herpesvirus expressed decoy TNF-alpha receptor delays behavioral fever in fish. Cell Host Microbe 21:244–253

    Article  PubMed  PubMed Central  Google Scholar 

  • Ronen A, Perelberg A, Abramowitz J, Hutoran M, Tinman S, Bejerano I et al (2003) Efficient vaccine against the virus causing a lethal disease in cultured Cyprinus carpio. Vaccine 21:4677–4684

    Article  CAS  PubMed  Google Scholar 

  • Samsing F, Hopf J, Dvis S, Wynne JW, Durr PA (2021) Will Australia’s common carp (Cyprinus carpio) populations develop resistance to Cyprinid herpesvirus 3 (CyHV-3) if released as a biocontrol agent? Identification of pathways and knowledge gap. Biol Control 157:104571

  • Sano M, Ito T, Kurita J, Yanai T, Watanabe N, Miwa S, Iida T (2004) First detection of koi herpesvirus in cultured common carp Cyprinus carpio in Japan. Fish Pathology 39:165–167

    Article  Google Scholar 

  • Suzuki K, Yamauchi Y, Yoshida T (2017) Interplay between microbial trait dynamics and population dynamics revealed by the combination of laboratory experiment and computational approaches. J Theor Biol 419:201–210

    Article  PubMed  Google Scholar 

  • Thieme HR (2003) SEIR (->S) type endemic models for “childhood diseases.” Mathematic in population biology. Princeton University Press, Princeton, pp 317–340

    Chapter  Google Scholar 

  • Uchii K, Matsui K, Iida T, Kawabata Z (2009) Distribution of the introduced cyprinid herpesvirus 3 in a wild population of common carp, Cyprinus carpio L. J Fish Dis 32:857–864

    Article  CAS  PubMed  Google Scholar 

  • Uchii K, Telschow A, Minamoto T, Yamanaka H, Honjo MN, Matsui K, Kawabata Z (2011) Transmission dynamics of an emerging infectious disease in wildlife through host reproductive cycles. ISME J 5:244–251

    Article  PubMed  Google Scholar 

  • Withers PC, Campbell JD (1985) Effects of environmental cost on thermoregulation in the desert iguana. Physiol Zool 58:329–339

    Article  Google Scholar 

  • Woolway RI, Merchant CJ (2018) Intralake heterogeneity of thermal responses to climate change: a study of large Northern Hemisphere lakes. J Geophy Res: Atmos 123:3087–3098. https://doi.org/10.1002/2017JD027661

    Article  Google Scholar 

  • Yamanaka H, Kohmatsu Y, Minamoto T, Kawabata Z (2010) Spatial variation and temporal stability of littoral water temperature relative to lakeshore morphometry: environmental analysis from the view of fish thermal ecology. Limnol 11:71–76

    Article  Google Scholar 

Download references

Acknowledgements

We express our sincere gratitude to Notogawa Fisheries Union, Higashi-Omi, Shiga, Japan, for their support in field activities. We also thank Drs. Yasushi Mitsunaga, Kazuhoshi Komeyama, Takeshi Yamane, Yoshio Kunimune (Kindai University), and Yuya Makiguchi (Hokkaido University) for their instructions related to the telemetry survey. We are grateful to Dr. Thomas Ting Lei (Ryukoku University) for helpful comments on the manuscript. Our radio telemetry study was conducted with the permission of the Ministry of Internal Affairs and Communications. We declare that all experiments in this study comply with the current laws of Japan.

Funding

This research was supported by the Research Institute for Humanity and Nature (project number C-06) and by a research fellowship of the Japan Society for the Promotion of Science (JSPS) for Young Scientists to K.U. and JSPS KAKENHI Grant Numbers 20K03750 to Y.S.

Author information

Authors and Affiliations

  1. Faculty of Advanced Science & Technology, Ryukoku University, 1-5 Seta-Oe, Otsu, 520-2194, Japan

    Takeshi Miki & Hiroki Yamanaka

  2. Research Institute for Humanity and Nature, 457-4 Motoyama, Kami-Gamo, Kita-Ku, Kyoto, 603-8047, Japan

    Hiroki Yamanaka, Toshifumi Minamoto, Kimiko Uchii, Mie N. Honjo, Alata A. Suzuki & Zen’ichiro Kawabata

  3. Department of Biology, Hirosaki University, 3 Bunkyo-Cho, Hirosaki, 036-8561, Japan

    Atsushi Sogabe

  4. Center for Marine Environmental Studies, Ehime University, 2-5 Bunkyo-Cho, Matsuyama, 790-8577, Japan

    Koji Omori

  5. Institute of Oceanography, National Taiwan University, No. 1 Sec. 4, Roosevelt Road, Taipei, 10617, Taiwan

    Takeshi Miki

  6. Department of Mathematics, Shimane University, 1060 Nishi-Kawatsu, Matsue, 690-8504, Japan

    Yasuhisa Saito

  7. Graduate School of Human Development and Environment, Kobe University, 3-11 Tsurukabuto, Nada-Ku, Kobe, 657-8501, Japan

    Toshifumi Minamoto

  8. Faculty of Pharmacy, Osaka Ohtani University, 3-11-1 Nishikiori-Kita, Tondabayashi, 584-8540, Japan

    Kimiko Uchii

  9. Center for Ecological Research, Kyoto University, 509-3, 2-chome, Hirano, Otsu, 520-2113, Japan

    Mie N. Honjo

  10. Ritsumeikan Global Innovation Research Organization, Ritsumeikan University, 56-1 Toji-in Kitamachi, Kita-Ku, Kyoto, 603-8577, Japan

    Yukihiro Kohmatsu

  11. Center for Biodiversity Science, Ryukoku University, 1-5 Seta-Oe, Otsu, 520-2194, Japan

    Takeshi Miki, Hiroki Yamanaka, Toshifumi Minamoto & Kimiko Uchii

Authors
  1. Takeshi Miki
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hiroki Yamanaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Atsushi Sogabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Koji Omori
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yasuhisa Saito
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Toshifumi Minamoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kimiko Uchii
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mie N. Honjo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Alata A. Suzuki
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yukihiro Kohmatsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Zen’ichiro Kawabata
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Zen’ichiro Kawabata, Hiroki Yamanaka, Toshifumi Minamoto, Atsushi Sogabe, and Koji Omori designed the empirical part of this study. Researchers above conducted the field survey with the help of Kimiko Uchii, Mie N. Honjo, Alata A. Suzuki, and Yukihiro Kohmatsu. Hiroki Yamanaka and Toshifumi Minamoto conducted the DNA analysis. Takeshi Miki and Yasuhisa Saito developed and analyzed the model. Takeshi Miki, Kimiko Uchii, Hiroki Yamanaka, and Toshifumi Minamoto wrote the main manuscript text and prepared the figures. All authors reviewed the manuscript.

Corresponding authors

Correspondence to Takeshi Miki or Hiroki Yamanaka.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

The results/data/figures in this manuscript have not been published elsewhere nor are they under consideration by another publisher.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 205 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miki, T., Yamanaka, H., Sogabe, A. et al. Spatial epidemiology model can explain the seasonal dynamics of infectious disease Cyprinid herpesvirus 3 (CyHV-3) by thermoregulation behavior of the host, common carp (Cyprinus carpio). Theor Ecol 16, 195–208 (2023). https://doi.org/10.1007/s12080-023-00563-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12080-023-00563-3

Keywords

search

Navigation