Ocean acidification boosts reproduction in fish via indirect effects

Abstract

Ocean acidification affects species populations and biodiversity through direct negative effects on physiology and behaviour. The indirect effects of elevated CO2 are less well known and can sometimes be counterintuitive. Reproduction lies at the crux of species population replenishment, but we do not know how ocean acidification affects reproduction in the wild. Here, we use natural CO2 vents at a temperate rocky reef and show that even though ocean acidification acts as a direct stressor, it can indirectly increase energy budgets of fish to stimulate reproduction at no cost to physiological homeostasis. Female fish maintained energy levels by compensation: They reduced activity (foraging and aggression) to increase reproduction. In male fish, increased reproductive investment was linked to increased energy intake as mediated by intensified foraging on more abundant prey. Greater biomass of prey at the vents was linked to greater biomass of algae, as mediated by a fertilisation effect of elevated CO2 on primary production. Additionally, the abundance and aggression of paternal carers were elevated at the CO2 vents, which may further boost reproductive success. These positive indirect effects of elevated CO2 were only observed for the species of fish that was generalistic and competitively dominant, but not for 3 species of subordinate and more specialised fishes. Hence, species that capitalise on future resource enrichment can accelerate their reproduction and increase their populations, thereby altering species communities in a future ocean.

Natural CO2 seeps reveal adaptive potential to ocean acidification in fish

“…Fish from natural CO 2 seeps showed increased gene expression levels across the gonad transcriptomes, suggesting an effect of ocean acidification on the overall regulation of gene expression. The elevated gene expression was more pronounced in males than in females from CO 2 seeps, which could have reproductive consequences and is possibly linked to the higher reproductive investment in males (Nagelkerken et al, 2021 ) as Common triplefin males provide parental care of the nests (Wellenreuther & Clements, 2007 ). Among the genes that presented significant elevated expression in individuals from CO 2 seeps compared with those from control areas, we found seven genes that are regulators of gene expression.…”

“…However, Common triplefins from these CO 2 seeps experience higher food availability due to bottom‐up CO 2 enrichment (Doubleday et al, 2019 ), and with their behavioral dominance over other fish species, they gain better access to food resources (Nagelkerken et al, 2017 ). Thus, individuals living at CO 2 seeps can maintain physiological homeostasis and compensate for the increasing energetic demand by increasing their food intake or reducing their activity levels (Nagelkerken et al, 2021 ). This energetic compensation might not involve long‐term adaptation directly but involve mechanisms of physiological acclimatization and behavioral adjustments.…”

“…Two CO 2 seeps at White Island (New Zealand) are located within temperate rocky reef habitats at 6 to 8 m of depth and have an average pH reduction of about −0.17 and −0.24 units, respectively, across years compared with ambient pH seawater (Nagelkerken et al, 2021 ), reflective of representative concentration pathway emission scenarios 4.5–6.0 (Bopp et al, 2013 ). Twenty individuals of the Common triplefin Forsterygion lapillum were collected on SCUBA with hand nets from rocky reefs habitats at the volcanic vents and adjacent control sites of White Island (New Zealand) in January 2019.…”

Positive species interactions strengthen in a high-CO2ocean

“…The average pH levels of the vents at White Island were relatively stable during 2016 and 2017 (electronic supplementary material, table S4). Multiple measurements during the years 2013-2017 (see Nagelkerken et al [46]) show that the average difference in pH levels between the two individual vents and their respective control sites ranges from −0.17 to −0.25 units, which approximates that forecast for the year 2100 according to an approximate RCP 4.5-6.0 emission scenario [19]. The control sites were located in an area approximately 25 m away from the edge of the vent plume.…”

Climate Change Effects on North American Fish and Fisheries to Inform Adaptation Strategies

“…Increased acidification coupled with increased nitrogen can promote growth of boring sponges that erode coral reefs (Zhao et al 2021). Acidification can increase the food availability for some fishes, but at the same time it also increases their reproductive investment (Nagelkerken et al 2021). These responses show the complex interactions among climate change and other stressors.…”