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R Soc Open Sci
2024 Sep 11;119:240789. doi: 10.1098/rsos.240789.
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Dynamic effects of thermal acclimation on chytridiomycosis infection intensity and transmission potential in Xenopus laevis.
Noelker JE
,
Abreu Ruozzi V
,
Spengler KD
,
Craig HM
,
Raffel TR
.
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The pandemic amphibian pathogen Batrachochytrium dendrobatidis (Bd) can cause more severe infections with variable temperatures owing to delays in host thermal acclimation following temperature shifts. However, little is known about the timing of these acclimation effects or their consequences for Bd transmission. We measured how thermal acclimation affects Bd infection in Xenopus laevis, using a timing-of-exposure treatment to investigate acclimation effect persistence following a temperature shift. Consistent with a delay in host acclimation, warm-acclimated frogs exposed to Bd immediately following a temperature decrease (day 0) developed higher infection intensities than frogs already acclimated to the cool temperature. This acclimation effect was surprisingly persistent (five weeks). Acclimation did not affect infection intensity when Bd exposure occurred one week after the temperature shift, indicating that frogs fully acclimated to new temperatures within 7 days. This suggests that acclimation effect persistence beyond one week post-exposure was caused by carry-over from initially high infection loads, rather than an extended delay in host acclimation. In a second experiment, we replicated the persistent thermal acclimation effects on Bd infection but found no acclimation effects on zoospore production. This suggests that variable temperatures consistently exacerbate individual Bd infection but may not necessarily increase Bd transmission.
Figure 1. Experimental timelines for (a) Experiment 1A, (b) Experiment 1B, and (c) Experiment 2, summarizing the timing of Bd exposure (green→orange arrows) relative to a temperature shift (thermometer) for each exposure-day treatment. (d) Illustration of how frogs assigned to warm (red) or cold (blue) acclimation incubators were all transferred to randomly assigned performance incubators within the same spatial block. Each incubator also contained a ‘blank’ deli cup with a HOBO temperature logger (represented by the icon with ‘H’) and the same water volume as cups housing frogs, to verify temperatures achieved within each incubator.
Figure 2. Overall effects of performance temperature on Bd infection dynamics throughout the performance period for ‘day 0’ frogs (i.e. frogs exposed to Bd on the day of the temperature shift). (a) Experiment 1A dynamics based on skin swabs (LnSwabBd). (b) Experiment 2 dynamics based on skin swabs. (c) Zoospore production over 15 min from experiment 2 as measured by water filtration (LnFilterBd.rate). 10°C: blue solid squares and solid lines; 15°C: purple solid triangles and dashed lines; 20°C: solid magenta circles and dot-dashed lines; 25°C: solid red diamonds and dotted lines. Points have been jittered on the x-axis. Error bars indicate s.e.
Figure 3. Acclimation and performance temperature effects for: (a,c,e,g,i) experiment 1A, and (b,d,f,h,j) experiment 2. Acclimation temperatures were 10°C (open blue squares and solid lines), 15°C (open purple triangles and dashed lines) or 20°C (open magenta circles and dotted lines). Each row represents a different week during the performance period of the experiment, with ‘days’ indicating the time since the temperature shift and Bd exposure occurred. Points are jittered on the x-axis. Error bars indicate s.e.
Figure 4. Acclimation effects for timing of exposure treatments from experiment 1B. Panels (a,b,d,g,j,m) are frogs that were exposed one week prior to the temperature shift (day −7). Panels (c,e,h,k,n) are frogs exposed on the day of the temperature shift (day 0). Panels (f,i,l,o) are frogs exposed one week after the temperature shift (day +7). Acclimation temperatures were 10°C (blue squares and solid lines) or 20°C (magenta circles and dotted lines). Plots outlined in thick grey boxes indicate the time point 7 days after Bd exposure. Plots outlined with thick black boxes indicate time points 14 days after Bd exposure. Frogs in panel (a) had not yet experienced performance temperature treatments and are therefore shown at their acclimation temperatures. Error bars indicate s.e.
Figure 5. Bd zoospore production over 15 min (LnFilterBd.rate) as a function of performance temperature on day 7 of experiment 2. (a) Comparison of zoospore production (open squares and dashed line) to Bd load from skin swabs (LnSwabBd; open circles and solid line). (b) Comparison of zoospore production by frogs acclimated to 10°C (open blue squares), 15°C (open purple triangles) or 20°C (open magenta circles). Points are jittered on the x-axis. Error bars indicate s.e.
