Intergenerational effects of CO₂‐induced stream acidification in the Trinidadian guppy (Poecilia reticulata)

Abstract

Rising atmospheric carbon dioxide levels are driving decreases in aquatic pH. As a result, there has been a surge in the number of studies examining the impact of acidification on aquatic fauna over the past decade. Thus far, both positive and negative impacts on the growth of fish have been reported, creating a disparity in results. Food availability and single‐generation exposure have been proposed as some of the reasons for these variable results, where unrealistically high food treatments lead to fish overcoming the energetic costs associated with acclimating to decreased pH. Likewise, exposure of fish to lower pH for only one generation may not capture the likely ecological response to acidification that wild populations might experience over two or more generations. Here we compare somatic growth rates of laboratory populations of the Trinidadian guppy (Poecilia reticulata) exposed to pH levels that represent the average and lowest levels observed in streams in its native range. Specifically, we test the role of maternal acclimation and resource availability on the response of freshwater fishes to acidification. Acidification had a negative impact on growth at more natural, low food treatments. With high food availability, fish whose mothers were acclimated to the acidified treatment showed no reduction in growth, compared to controls. Compensatory growth was observed in both control–acidified (maternal–natal environment) and acidified–control groups, where fish that did not experience intergenerational effects achieved the same size in response to acidification as those that did, after an initial period of stunted growth. These results suggest that future studies on the effects of shifting mean of aquatic pH on fishes should take account of intergenerational effects and compensatory growth, as otherwise effects of acidification may be overestimated.

Effects of multigenerational exposure and phenotypic variation on a freshwater fish species exposed to elevated carbon dioxide (CO2)

“…For example, one study found an increase of reproductive output and an increase weight of juveniles in adult anemonefish (Miller et al, 2013) while in other studies, elevated CO2 has been linked with reduced reproductive success and effort in fishes (Miller et al, 2012). In one study on intergenerational effects of CO2 acidification on a guppy species (Poecilia reticulata), two of six pregnant females exposed to CO2 aborted dead underdeveloped or morphologically compromised fry, while no such observations were found under control pH (George et al, 2019). While many studies focus on maternal investments, other studies have found evidence for paternal effects such as reduced sperm motility (Ingermann et al, 2002).…”

“…Globally these ecosystems are experiencing major reductions in biodiversity and population sizes, with major threats including over-exploitation, water pollution, habitat degradation, flow modification, and species invasion (Dudgeon et al, 2006;Reid et al, 2019). Despite these present threats and that freshwater ecosystems are particularly vulnerable to climate change, currently, relatively little is known about how these ecosystems will respond to near-future CO2 conditions particularly across transgenerational timescales (Hasler et al, 2016;Brauner et al, 2019;George et al, 2019).…”

“…Several studies have found evidence for non-genetic inheritance in fishes (Salinas et al, 2013;Miller et al, 2012). For example, in some studies, maternal environments had significant impacts on the effects of acidification on fish growth (George et al, 2019). In a study on a marine fish, parental exposure to elevated CO2 mediated metabolic and growth impacts from elevated CO2, as offspring of fish exposed to elevated CO2 did not demonstrate higher metabolic rates, lower growth rates, or lower survival, which were observed when only juveniles (and not their parents) were exposed to elevated CO2 (Miller et al, 2012).…”

“…Previous studies have found similar multigenerational acclimatization effects after parental exposure to elevated CO2. For example, in a study on Trinidadian guppies (Poecilia reticulata), offspring growth was not affected in fish maternally exposed and acclimatized to elevated CO2 but was affected in fish who did not have parental exposure to elevated CO2 (George et al, 2019). Additionally, reduced growth and weight of cinnamon anemonefish (Amphiprion melanopus) was observed after exposure to elevated CO2 but was not observed when parents had also experienced elevated CO2 exposure (Miller et al, 2012).…”