Sperm in hot water: Direct and indirect thermal challenges interact to impact on brown trout sperm quality

Abstract

Climate change alters the thermal habitat of aquatic species on a global scale, generating novel environmental challenges during all life stages, including reproduction. Changes in water temperature profoundly influence the performance of ectothermic aquatic organisms. This is an especially crucial issue for migratory fish, because they traverse multiple environments in order to reproduce. In externally fertilizing migratory fish, gametes are affected by water temperature indirectly, within the reproductive organ in which they are produced during migration, as well as directly, upon release into the surrounding medium at the spawning grounds. Both direct (after release) and indirect (during production) thermal impacts on gamete quality have been investigated, but never in conjunction. Here, we assessed the cumulative influence of temperature on brown trout, Salmo trutta, sperm quality during sperm production (male acclimation temperature) as well as upon release (sperm activation water temperature) on two consecutive dates during the brown trout spawning season. Early in the season, warm acclimation of males reduced their fertilization probability (lower sperm velocity) when compared with cold-acclimated males, especially when the activation water temperature was also increased beyond the thermal optimum (resulting in a lower proportion of motile sperm with lower velocity). Later in the season, sperm quality was unaffected by acclimation temperature and thermal sensitivity of sperm was reduced. These results give novel insights into the complex impacts of climate change on fish sperm, with implications for the reproduction and management of hatchery and wild trout populations in future climate scenarios.

From gametogenesis to spawning: How climate‐driven warming affects teleost reproductive biology

“…In addition to spermatogenesis, the spermiation initiation and duration can be influenced by temperature (Table 1 and Figure 4). In S. trutta , timing and duration of spawning was delayed and shortened, respectively (Fenkes et al ., 2017; Lahnsteiner & Leitner, 2013), following a 5°C temperature increase. On the contrary, in L. fluviatilis and T. thymallus , both spring spawners, no change in spawning timing was reported after a thermal treatment (Cejko et al ., 2016; Lahnsteiner & Kletzl, 2012).…”

“…Male exposure to warm temperatures during the meiotic and spermiogenic phase affects male reproductive potential and, depending on the species, sperm motility can be impaired (Cejko et al ., 2016; Lahnsteiner & Kletzl, 2012; Targońska et al ., 2014) or remain unchanged (Lahnsteiner & Leitner, 2013) (Table 4 and Figure 4). In a recent study on S. trutta , cumulative effects of high temperature during spermatogenesis (4 weeks at 13°C relative to 8°C) and sperm activation caused a decrease in sperm velocity, without impacting the proportion of motile cells at the beginning of spawning (Fenkes et al ., 2017). However, later in the spawning season, the temperature‐driven difference in sperm quality was no longer present (Fenkes et al ., 2017).…”

“…In a recent study on S. trutta , cumulative effects of high temperature during spermatogenesis (4 weeks at 13°C relative to 8°C) and sperm activation caused a decrease in sperm velocity, without impacting the proportion of motile cells at the beginning of spawning (Fenkes et al ., 2017). However, later in the spawning season, the temperature‐driven difference in sperm quality was no longer present (Fenkes et al ., 2017). In another study on S. trutta , no change in sperm velocity was observed when males were exposed for a longer time (4 months, 12.4°C relative to 7.4°C) (Lahnsteiner & Leitner, 2013).…”

The effectiveness of spawning habitat creation or enhancement for substrate-spawning temperate fish: a systematic review

“…For instance, physical spawning habitat may be created for salmonids by depositing rocky material, but the quality of such habitat depends on many other factors aside from the composition of the material itself. These include thermal conditions, flow, sedimentation, and dissolved oxygen levels [69][70][71]. Fish may not use created habitats unless all attributes are suitable, and only partly suitable artificial habitats could inadvertently serve as ecological sinks, especially if they fill with sediment after redds are constructed.…”

Sperm pre-fertilization thermal environment shapes offspring phenotype and performance

“…Cingi et al, 2010). Accordingly, relatively minor changes in the sperm thermal environment can have many fundamental effects on the sperm physiology and function in these species (Lahnsteiner and Mansour, 2012;Dadras et al, 2017a;Fenkes et al, 2017). Water temperature can, for example, affect the physiological state of lipids, properties of the plasma membrane and enzyme activity of sperm cells, as well as alter the composition of the seminal plasma (Dadras et al, 2017a).…”