Heat and immunity: an experimental heat wave alters immune functions in three‐spined sticklebacks (Gasterosteus aculeatus)

Abstract

Summary 1.Global climate change is predicted to lead to increased temperatures and more extreme climatic events. This may influence host-parasite interactions, immunity and therefore the impact of infectious diseases on ecosystems. However, little is known about the effects of rising temperatures on immune defence, in particular in ectothermic animals, where the immune system is directly exposed to external temperature change. 2. Fish are ideal models for studying the effect of temperature on immunity, because they are poikilothermic, but possess a complete vertebrate immune system with both innate and adaptive immunity. We used three-spined sticklebacks (Gasterosteus aculeatus) originating from a stream and a pond, whereby the latter supposedly were adapted to higher temperature variation. We studied the effect of increasing and decreasing temperatures and a simulated heat wave with subsequent recovery on body condition and immune parameters. 3. We hypothesized that the immune system might be less active at low temperatures, but will be even more suppressed at temperatures towards the upper tolerable temperature range. 4. Contrary to our expectation, we found innate and adaptive immune activity to be highest at a temperature as low as 13°C. Exposure to a simulated heat wave induced long-lasting immune disorders, in particular in a stickleback population that might be less adapted to temperature variation in its natural environment. 5. The results show that the activity of the immune system of an ectothermic animal species is temperature dependent and suggest that heat waves associated with global warming may immunocompromise host species, thereby potentially facilitating the spread of infectious diseases.

Potential for adaptation to climate change: family-level variation in fitness-related traits and their responses to heat waves in a snail population

“…These effects are most likely due to high metabolic activity, which can increase the amount of resources allocated to reproduction and growth [25]. The observed decrease in immune activity at the high temperature is also in line with the results from other taxa (e.g., [28–32]) and may be due to altered resource allocation towards growth and reproduction rather than immune defence (see [33]). Variation in the responses of different immune parameters to high temperatures (see also [24, 34]) could be a result of the other functions of some immune traits beside defence (e.g.…”

Environmental temperature variation influences fitness trade-offs and tolerance in a fish-tapeworm association

“…Subsequently, all tanks were adjusted from 16 °C to 18 °C (∆ T 0.3 °C per day). This resulted in a starting temperature that was approximately mid-way between the two experimental temperatures (13 and 24 °C) and it was also the same temperature as previous studies testing stickleback immune activity [30]. The sticklebacks were starved 72 h prior to copepod exposure and 24 h before exposure they were measured to the nearest mm (infection length) and transferred to individual glass jars with 300 ml tank water.…”

“…Adaptation of sticklebacks to local temperatures was suggested by Dittmar et al [30], who observed stronger immunological disorders and higher mortality in F1 sticklebacks from a brook compared to F1 sticklebacks from a pond during experimental exposure to a heat wave of up to 28 °C. Furthermore, studies with three-spined sticklebacks from a marine origin, which were adapted to cold and warm conditions in the laboratory for one generation, illustrated that cold adapted sticklebacks had offspring with faster growth compared to warm adapted sticklebacks, which suggests considerable transgenerational plasticity in stickleback temperature adaptation [31–33].…”

“…it might alter host food consumption and thereby change the risk of becoming exposed to trophically transmitted parasites [35]. Furthermore, temperature plays a key role in determining the efficacy of the immune system - the host’s most important physiological barrier against parasitation [30, 36, 37]. In this respect it has been shown that increasing temperature coincided with a higher output of trematode cercariae [38–40] and increased infectivity of metacercariae, while the survival of amphipod hosts decreased [41].…”

Invasive slug pests and their parasites—temperature responses and potential implications of climate change

“…It is generally accepted that climate change can induce adaptations in one or both of the species disrupting the normal host-parasite relationship (Dittmar et al 2014;Easterling et al 2000;Hance et al 2007). While there have been numerous studies done on how climate change may influence crop pests in relation to insect predator or parasitoid natural enemies (Gerard et al 2013; Thomson et al 2010) and pathogenic microorganisms (Elderd and Reilly 2014;Thomas and Blanford 2003), little attention has been paid to how climate change may influence the helminth parasites of crop pests.…”