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.

Highlights

  • Densities were skewed towards males at vents, both females and males of the most common species showed a higher investment in reproduction at vents

  • Our study suggests that boosted reproduction is mediated by indirect effects rather than direct effects of elevated CO2 on fish reproductive tissues

  • Mature males of the fish species studied here provide parental care up to 3 weeks by aggressively defending their small territories in which eggs are deposited by the females [16]

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Summary

Introduction

They constrain the capacity of an environment to meet the energetic demands of organisms, thereby shaping the evolution of life history strategies that underpin their fitness and their population persistence [1,2]. Organisms have many competing demands of high-energy-consuming processes (e.g., maintenance, growth, and reproduction) and need to continually trade off their allocation of energy between them [3,4]. Future climate represents a major change to organisms as they adjust their behaviour [5] and physiology [6] to accommodate changes in resource availability [7]. We have little understanding of how these adjustments combine so that life history trade-offs alter an individual’s fitness and sustainability of their populations in a future world.

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