Does the seasonal acidification of spawning habitat influence offspring CO2 reaction norms through transgenerational plasticity in the coastal fish species, Menidia menidia

Experimental assessments of species vulnerabilities to ocean acidification are rapidly expanding, yet the potential for short- and long-term adaptation to high CO2 by contemporary marine organisms remains poorly understood. We used a novel experimental approach that combined bi-weekly sampling of a wild, spawning fish population (Atlantic silverside, Menidia menidia) with standardized offspring CO2 exposure experiments and parallel pH monitoring of a coastal ecosystem. We assessed whether offspring produced at different times of the spawning season (April-July) would be similarly susceptible to elevated (∼1,100 uatm, pHNBS = 7.77) and high CO2 levels (∼2,300 uatm, pHNBS = 7.47). Early in the season (April), high CO2 levels significantly (P < 0.05) reduced fish survival by 54% (2012) and 33% (2013) and 1-10d post hatch growth by 17% relative to ambient conditions. However, offspring from parents collected later in the season became increasingly CO2-tolerant until, by mid-May, offspring survival was equally high at all CO2 levels. This interannually consistent plasticity coincided with the rapid annual pH decline in the species' spawning habitat (mean pH: 1 April/31 May = 8.05/7.67). It suggests that parents can condition their offspring to seasonally acidifying environments, either via changes in maternal provisioning and/or epigenetic transgenerational plasticity (TGP). TGP to increasing CO2 has been shown in the laboratory but never before in a wild population. Our novel findings of direct CO2-related survival reductions in wild fish offspring and seasonally plastic responses imply that realistic assessments of species CO2-sensitivities must control for parental environments that are seasonally variable in coastal habitats.