Alternate patterns of temperature variation bring about very different disease outcomes at different mean temperatures
Curation statements for this article:-
Curated by eLife
Evaluation Summary:
Kunze et al. provide a fine experiment to show that both increases in mean temperature and (extreme) variability in temperature regimes have important consequences in host-pathogen interactions. The results presented in this manuscript shed a light on why disease spread models fed by experimental data (commonly obtained in stable environmental conditions) are frequently inaccurate. These results lead us to more realistic understanding of the impacts of climate change in biological species but also identify the need of mechanisms behind species interaction in fluctuating environments/temperatures. This manuscript thus comes timely as the planet is warming, and disease ecologists, limnologists, epidemiologists and physiologists are interested in the consequences.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors).
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- Ecology (eLife)
Abstract
The dynamics of host-parasite interactions are highly temperature-dependent and may be modified by increasing frequency and intensity of climate-driven heat events. Here, we show that altered patterns of temperature variance lead to an almost order-of-magnitude shift in thermal performance of host and pathogen life-history traits over and above the effects of mean temperature and, moreover, that different temperature regimes affect these traits differently. We found that diurnal fluctuations of ±3°C lowered infection rates and reduced spore burden compared to constant temperatures in our focal host Daphnia magna exposed to the microsporidium parasite Ordospora colligata . In contrast, a 3-day heatwave (+6°C) did not affect infection rates, but increased spore burden (relative to constant temperatures with the same mean) at 16°C, while reducing burden at higher temperatures. We conclude that changing patterns of climate variation, superimposed on shifts in mean temperatures due to global warming, may have profound and unanticipated effects on disease dynamics.
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Author Response:
Reviewer #1 (Public Review):
Kunze et al. provide an interesting experiment aimed to understand the effects of variable temperature regimes in host-pathogen interactions. This is one of the most complete experiments to date, that goes beyond exploring increasing but constant temperature regimes. The experimental setup is strong, exposing Daphnia magna to the natural range of temperature variability and realistic fluctuating (+-3C) and extreme (6C pulse) regimes. Daphnia exposure to Odospora colligata pathogens was also rightly tested against a placebo control. Aided by their experimental approach Kunze et al. explore their results with clear figures and fine text, getting deep into our understanding of the thermal performance of important host and pathogen life history traits (such as reproductive output) and setting …
Author Response:
Reviewer #1 (Public Review):
Kunze et al. provide an interesting experiment aimed to understand the effects of variable temperature regimes in host-pathogen interactions. This is one of the most complete experiments to date, that goes beyond exploring increasing but constant temperature regimes. The experimental setup is strong, exposing Daphnia magna to the natural range of temperature variability and realistic fluctuating (+-3C) and extreme (6C pulse) regimes. Daphnia exposure to Odospora colligata pathogens was also rightly tested against a placebo control. Aided by their experimental approach Kunze et al. explore their results with clear figures and fine text, getting deep into our understanding of the thermal performance of important host and pathogen life history traits (such as reproductive output) and setting them in the larger picture of global warming. In short, I am impressed by the quality of the new information provided by this ms.
Thank you for these positive comments on our manuscript.
Reviewer #2 (Public Review):
The manuscript of Kunze et al. aimed at finding how different kinds of fluctuations in temperature affect the disease outcome. The authors used Daphnia magna - Ordospora colligate host - parasite system exposed to a range of temperatures which were either stable, regularly fluctuating, or included a single heat wave, and measured fitness of the host (as reproductive output) and the parasite (infection rate and spore burden). The experiment is very well designed, and the methods of data analysis are sound and well suited to address the questions stated by the authors. The authors found that the unstable thermal conditions change the fitness of the host and the parasite. Temperature fluctuations narrowed thermal breadth for infection and spore burden of the parasite, whereas the heat wave caused shift in thermal optimum and a strong increase of maximal spore burden of the parasite. Both thermal variation treatments resulted in shifts in thermal optimum and maximal performance of the host. The most interesting (and surprising) result was the spectacular increase in spore burden of the parasite exposed to heat wave in comparison to fluctuating temperature treatment and stable temperature treatment, obtained in 16{degree sign}C. Authors rightfully conclude that the outcome of infection could be strongly altered by variations in thermal regime. This context dependency might to some extent explain the limited accuracy of disease spread models. This is critical especially in the face of climate change, which is expected to result in more frequent and more rapid thermal variation events. Moreover, the narrowed thermal performance curve of the parasite (especially in the high temperatures range) under fluctuating temperature regime indicates, that the thermal tolerance of some organisms to warming might be overestimated, when tested under (less realistic) stable thermal conditions. I think the paper of Kunze et al. is a very strong contribution to the field of disease ecology, and I find no major weaknesses. The Introduction and Discussion sections are well written and provide some extensive overview of the relevant literature. The study design and results are described clearly and the conclusions are well supported. I have no major criticism to this manuscript.
We thank the reviewer for these positive comments on our manuscript.
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Evaluation Summary:
Kunze et al. provide a fine experiment to show that both increases in mean temperature and (extreme) variability in temperature regimes have important consequences in host-pathogen interactions. The results presented in this manuscript shed a light on why disease spread models fed by experimental data (commonly obtained in stable environmental conditions) are frequently inaccurate. These results lead us to more realistic understanding of the impacts of climate change in biological species but also identify the need of mechanisms behind species interaction in fluctuating environments/temperatures. This manuscript thus comes timely as the planet is warming, and disease ecologists, limnologists, epidemiologists and physiologists are interested in the consequences.
(This preprint has been reviewed by eLife. We include …
Evaluation Summary:
Kunze et al. provide a fine experiment to show that both increases in mean temperature and (extreme) variability in temperature regimes have important consequences in host-pathogen interactions. The results presented in this manuscript shed a light on why disease spread models fed by experimental data (commonly obtained in stable environmental conditions) are frequently inaccurate. These results lead us to more realistic understanding of the impacts of climate change in biological species but also identify the need of mechanisms behind species interaction in fluctuating environments/temperatures. This manuscript thus comes timely as the planet is warming, and disease ecologists, limnologists, epidemiologists and physiologists are interested in the consequences.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors).
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Reviewer #1 (Public Review):
Kunze et al. provide an interesting experiment aimed to understand the effects of variable temperature regimes in host-pathogen interactions. This is one of the most complete experiments to date, that goes beyond exploring increasing but constant temperature regimes. The experimental setup is strong, exposing Daphnia magna to the natural range of temperature variability and realistic fluctuating (+-3C) and extreme (6C pulse) regimes. Daphnia exposure to Odospora colligata pathogens was also rightly tested against a placebo control. Aided by their experimental approach Kunze et al. explore their results with clear figures and fine text, getting deep into our understanding of the thermal performance of important host and pathogen life history traits (such as reproductive output) and setting them in the larger …
Reviewer #1 (Public Review):
Kunze et al. provide an interesting experiment aimed to understand the effects of variable temperature regimes in host-pathogen interactions. This is one of the most complete experiments to date, that goes beyond exploring increasing but constant temperature regimes. The experimental setup is strong, exposing Daphnia magna to the natural range of temperature variability and realistic fluctuating (+-3C) and extreme (6C pulse) regimes. Daphnia exposure to Odospora colligata pathogens was also rightly tested against a placebo control. Aided by their experimental approach Kunze et al. explore their results with clear figures and fine text, getting deep into our understanding of the thermal performance of important host and pathogen life history traits (such as reproductive output) and setting them in the larger picture of global warming. In short, I am impressed by the quality of the new information provided by this ms.
-
Reviewer #2 (Public Review):
The manuscript of Kunze et al. aimed at finding how different kinds of fluctuations in temperature affect the disease outcome. The authors used Daphnia magna - Ordospora colligate host - parasite system exposed to a range of temperatures which were either stable, regularly fluctuating, or included a single heat wave, and measured fitness of the host (as reproductive output) and the parasite (infection rate and spore burden). The experiment is very well designed, and the methods of data analysis are sound and well suited to address the questions stated by the authors.
The authors found that the unstable thermal conditions change the fitness of the host and the parasite. Temperature fluctuations narrowed thermal breadth for infection and spore burden of the parasite, whereas the heat wave caused shift in …
Reviewer #2 (Public Review):
The manuscript of Kunze et al. aimed at finding how different kinds of fluctuations in temperature affect the disease outcome. The authors used Daphnia magna - Ordospora colligate host - parasite system exposed to a range of temperatures which were either stable, regularly fluctuating, or included a single heat wave, and measured fitness of the host (as reproductive output) and the parasite (infection rate and spore burden). The experiment is very well designed, and the methods of data analysis are sound and well suited to address the questions stated by the authors.
The authors found that the unstable thermal conditions change the fitness of the host and the parasite. Temperature fluctuations narrowed thermal breadth for infection and spore burden of the parasite, whereas the heat wave caused shift in thermal optimum and a strong increase of maximal spore burden of the parasite. Both thermal variation treatments resulted in shifts in thermal optimum and maximal performance of the host. The most interesting (and surprising) result was the spectacular increase in spore burden of the parasite exposed to heat wave in comparison to fluctuating temperature treatment and stable temperature treatment, obtained in 16°C.
Authors rightfully conclude that the outcome of infection could be strongly altered by variations in thermal regime. This context dependency might to some extent explain the limited accuracy of disease spread models. This is critical especially in the face of climate change, which is expected to result in more frequent and more rapid thermal variation events. Moreover, the narrowed thermal performance curve of the parasite (especially in the high temperatures range) under fluctuating temperature regime indicates, that the thermal tolerance of some organisms to warming might be overestimated, when tested under (less realistic) stable thermal conditions.
I think the paper of Kunze et al. is a very strong contribution to the field of disease ecology, and I find no major weaknesses. The Introduction and Discussion sections are well written and provide some extensive overview of the relevant literature. The study design and results are described clearly and the conclusions are well supported. I have no major criticism to this manuscript.
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