Multigenerational exposure to warming and fishing causes recruitment collapse, but size diversity and periodic cooling can aid recovery

Abstract

Global warming and fisheries harvest are significantly impacting wild fish stocks, yet their interactive influence on population resilience to stress remains unclear. We explored these interactive effects on early-life development and survival by experimentally manipulating the thermal and harvest regimes in 18 zebrafish (Danio rerio) populations over six consecutive generations. Warming advanced development rates across generations, but after three generations, it caused a sudden and large (30–50%) decline in recruitment. This warming impact was most severe in populations where size-selective harvesting reduced the average size of spawners. We then explored whether our observed recruitment decline could be explained by changes in egg size, early egg and larval survival, population sex ratio, and developmental costs. We found that it was most likely driven by temperature-induced shifts in embryonic development rate and fishing-induced male-biased sex ratios. Importantly, once harvest and warming were relaxed, recruitment rates rapidly recovered. Our study suggests that the effects of warming and fishing could have strong impacts on wild stock recruitment, but this may take several generations to manifest. However, resilience of wild populations may be higher if fishing preserves sufficient body size diversity, and windows of suitable temperature periodically occur.

Smaller adult fish size in warmer water is not explained by elevated metabolism

“…Despite earlier reproduction, warmed populations did not necessarily have higher reproductive output. In fact, after four generations of heating we observed a rapid decline in the recruitment (number of fish that reached 6 weeks of age) of our warmed experimental populations (see: Wootton et al, 2021). It is important to note that the observed decrease in recruitment was relative to the control populations and does not necessarily suggest that earlier maturation itself was disadvantageous.…”

“…This difference in adult body size persisted across all six generations. Observed adult body size differences could not be explained by a warming‐induced shift to a male biased sex‐ratio (males are smaller than females) as sex‐ratios remained constant through the experiment (data presented in Wootton et al (2021)). In contrast, juvenile body size patterns did not initially conform to TSR expectations as control and warmed juveniles grew at similar rates over the first two generations.…”

Genomic prediction of growth in a commercially, recreationally, and culturally important marine resource, the Australian snapper (Chrysophrys auratus)

“…There are several factors affecting growth in marine organisms, but one of the most important abiotic factors is temperature ( Besson et al 2016 ; Boltaña et al 2017 ; Wellenreuther et al 2019 ). In addition, many fish populations are under heavy exploitation, and there is strong evidence of selective harvesting gradually reducing the genetic potential for somatic growth in the population ( Enberg et al 2009 ; Denechaud et al 2020 ), and thus magnifying climatic change impacts ( Morrongiello et al 2021 ; Wootton et al 2021 ). Small changes in growth rates within a population can not only influence individual fitness but can also cause long-lasting shifts in population characteristics and demographic dynamics, including a reduction in fecundity, survival, and recruitment rates ( Lorenzen 2016 ; Denechaud et al 2020 ).…”

“…Because female fish retain their oocytes internally during their development, maximum reproductive output will be subject to body size constraints ( Lambert 2008 ; Ohlberger et al 2020 ). Alternatively, reduced body size can result in small eggs that maximize the number produced, but with a significant reduction of offspring survival ( Einum and Fleming 2000 ; Wootton et al 2021 ). Since large organisms have relatively high survival probabilities and reproductive success, it is expected that by predicting the size composition of a population, we can determine its average survival and recruitment dynamics ( Garrido et al 2015 ).…”

Evolutionary impact of size-selective harvesting on shoaling behavior: Individual-level mechanisms and possible consequences for natural and fishing mortality

“…Our study suggests that intensive harvesting directed at the larger individuals of a population could shift the fitness optimum of shoaling behavior in the opposite direction of what natural selection would favor. Evolution under anthropogenic selection has been demonstrated to occur within few generations (3–5, 67–69), and could impede recovery of exploited population even after harvesting halted (70, 71). Here, we provide the first functional integration of individual vigilance into mechanisms governing group dynamics with respect to fisheries and natural predation.…”