Experimental heatwaves negatively impact sperm quality in the zebra finch

Abstract

For sexually reproducing species, functionally competent sperm are critical to reproduction. While high atmospheric temperatures are known to influence the timing of breeding, incubation and reproductive success in birds, the effect of temperature on sperm quality remains largely unexplored. Here, we experimentally investigated the impact of ecologically relevant extreme temperatures on cloacal temperature and sperm morphology and motility in zebra finches We periodically sampled males exposed to 30°C or 40°C temperatures daily for 14 consecutive days. Following a 12-day (23°C) recovery period, birds were again exposed to heat, but under the alternate treatment (e.g. birds initially exposed to 40°C were exposed to 30°C). Elevated temperatures led to an increase in cloacal temperature and a reduction in the proportion of sperm with normal morphology; these effects were most notable under 40°C conditions, and were influenced by the duration of heat exposure and prior exposure to high temperature. Our findings highlight the potential role of temperature in determining male fertility in birds, and perhaps also in constraining the timing of avian breeding. Given the increased frequency of heatwaves in a warming world, our results suggest the need for further work on climatic influences on sperm quality and male fertility.

Heat dissipation rate constrains reproductive investment in a wild bird

“…This could be achieved at lower T b than in control birds (Figure 2a), suggesting that featherclipped parents were probably also able to increasingly escape any costs pertaining to hyperthermia. At the physiological level, such costs include, for example, changes to energy metabolism within cells (Jimenez & Williams, 2014), oxidative stress and subsequent lipid peroxidation (Farag & Alagawany, 2018;Lin, Decuypere, & Buyse, 2006), reduced gamete quality (Hansen, 2009;Hurley, McDiarmid, Friesen, Griffith, & Rowe, 2018), and potentially lifethreatening disturbances to the immune defence system (Farag & Alagawany, 2018;Lim & Mackinnon, 2006). At the ecological level, costs of prohibitively high T b are less well understood, but it is easy to speculate that reduced (Marino, 2004), or temporarily arrested (Guillemette et al, 2016), work rate in anticipation of hyperthermia could make birds more vulnerable to predation during subsequent recovery.…”

Temperatures that sterilise males better predict global species distributions than lethal temperatures

“…There is evidence that sub-lethal temperatures cause losses in fertility in plants( 9 ), insects( 10-12 ), fish( 13 ), aquatic invertebrates( 14 ), birds( 15 ) and mammals, including humans( 16 ). These effects include direct impacts on physiological processes ( 10, 15, 17 ) and indirect influences via changes in behavior and phenology( 18 ). Previously, we proposed that temperatures at which fertility is lost, the thermal fertility limits (TFLs) ( 18 ), may be a critical but understudied part of species’ true upper thermal limits.…”

Variation in the timing of avian egg‐laying in relation to climate

“…2). Furthermore, reproduction in extreme heat could also be compromised by the effect of high ambient conditions on fertility, with a recent experimental study indicating a decline in the quality and motility of sperm in the desertliving zebra finch (Hurley et al 2018). Results from biome-level paired t-tests comparing breeding behaviour in reponse to lagged and average precipitation across 76 Australian bird species in the desert biome and 180 species in the grassland biome.…”

“…In desert regions, eggs can reach their thermal limits rapidly when exposed to direct sunlight (Carey 2002) and when eggs are exposed to very warm temperatures, 'ambient' incubation can occur, reducing incubation time and decreasing hatch synchrony (Griffith et al 2016). Furthermore, reproduction in extreme heat could also be compromised by the effect of high ambient conditions on fertility, with a recent experimental study indicating a decline in the quality and motility of sperm in the desertliving zebra finch (Hurley et al 2018). It is worth noting that even in some areas of the temperate biome daily maximum temperatures in the summer can be well over 40°C (Bureau of Meteorology 2009, Jones et al 2009).…”