Ocean acidification alters the otoliths of a pantropical fish species with implications for sensory function

Abstract

Ocean acidification affects a wide diversity of marine organisms and is of particular concern for vulnerable larval stages critical to population replenishment and connectivity. Whereas it is well known that ocean acidification will negatively affect a range of calcareous taxa, the study of fishes is more limited in both depth of understanding and diversity of study species. We used new 3D microcomputed tomography to conduct in situ analysis of the impact of ocean acidification on otolith (ear stone) size and density of larval cobia (Rachycentron canadum), a large, economically important, pantropical fish species that shares many life history traits with a diversity of high-value, tropical pelagic fishes. We show that 2,100 μatm partial pressure of carbon dioxide (pCO 2 ) significantly increased not only otolith size (up to 49% greater volume and 58% greater relative mass) but also otolith density (6% higher). Estimated relative mass in 800 μatm pCO 2 treatments was 14% greater, and there was a similar but nonsignificant trend for otolith size. Using a modeling approach, we demonstrate that these changes could affect auditory sensitivity including a ∼50% increase in hearing range at 2,100 μatm pCO 2 , which may alter the perception of auditory information by larval cobia in a high-CO 2 ocean. Our results indicate that ocean acidification has a graded effect on cobia otoliths, with the potential to substantially influence the dispersal, survival, and recruitment of a pelagic fish species. These results have important implications for population maintenance/replenishment, connectivity, and conservation efforts for other valuable fish stocks that are already being deleteriously impacted by overfishing. P resent day atmospheric CO 2 concentration is higher than at any point in the past 800,000 y (1), driving unprecedented anthropogenic ocean acidification in pelagic (2) and coastal environments (3). Future climate scenarios project further decline in ocean pH (4-6) at a rate of change faster than any experienced in the last 300 million years (7). Although ocean acidification is known to influence a diversity of marine organisms (8), it is a particular concern for vulnerable larval stages critical to population replenishment and connectivity (9). Recently, the impact of ocean acidification on the larval stages of invertebrate and vertebrate marine species has attracted increased attention; however, experiments on larval fishes raised under projected ocean acidification scenarios have produced mixed results (10, 11). The days-to month-long pelagic larval period is an ecologically vital ontogenetic phase in marine fishes because it constitutes the primary mode of dispersal in many species (9) and represents the life stage most susceptible to mortality (12). During this phase, the sensory abilities of larval fishes are important determinants of survival (13) and ultimately influence the persistence of viable populations. Therefore, the study of ocean acidification impacts on sensory function in fishes is of critical imp...

You Better Repeat It: Complex CO2 × Temperature Effects in Atlantic Silverside Offspring Revealed by Serial Experimentation

“…We conducted five factorial experiments to evaluate the sensitivity of M. menidia early life traits to high (2000-2800 µatm) and extreme CO 2 conditions (4000-6200 µatm) across four temperatures (17,20,24, and 28 • C) that encompassed contemporary and potential future conditions in nearshore silverside spawning habitats. The experiments showed few significant CO 2 effects on response traits.…”

“…The latter has been particularly well documented for marine fish, where adults are largely tolerant of acute high-CO 2 levels far exceeding predicted OA conditions [9,10]. By contrast, fish early life-stages (embryos and early larvae) that are still developing effective acid-base regulation have exhibited reduced survival [11,12], reduced growth [13,14], defective development [14,15], otolith over-calcification [16,17], and behavioral abnormalities in response to high-CO 2 conditions Table 1. Summary of five CO 2 × temperature experiments on M. menidia offspring.…”

“…Here, we summarize five CO 2 × temperature experiments on wild Atlantic silverside, Menidia menidia, offspring that were reared under factorial combinations of CO 2 (nominal: 400, 2200, 4000, and 6000 µatm) and temperature (17,20,24, and 28 • C) to quantify the temperature-dependence of CO 2 effects in early life growth and survival. Across experiments and temperature treatments, we found few significant CO 2 effects on response traits.…”

Organ damage in Atlantic herring larvae as a result of ocean acidification

“…An increase in otolith size in relation to increases in CO 2 was found in temperate fish such as sea bass larvae (Checkley et al 2009), newly hatched herring larvae (Franke and Clemmesen 2011), juvenile walleye pollock (Hurst et al 2012), and cod larvae (Maneja et al 2013b) as well as in tropical fish such as clownfish larvae (Munday et al 2011b) and cobia (Bignami et al 2013b). A change in otolith size and density may affect the auditory sensitivity and perception in the larvae (Bignami et al 2013a). Sensory and cognitive impairment in respect to homing behavior (Munday et al 2009b, Devine et al 2011, prey detection (Cripps et al 2011), predator avoidance , and risk assessment (Ferrari et al 2012) has been observed in coral reef fishes and has been linked to effects of CO 2 on neurotransmitter functions in the brain (Nilsson et al 2012).…”

“…But differences in the reaction to OA are not only found in the extent but also the mode of reaction to OA between species. Bignami et al (2013a) predict differences in the sound reception in cobia larvae based on an otolith hearing model, whereas behavioral studies performed on larval Atlantic cod using swimming kinematics have shown that Atlantic cod larvae seem rather resilient to increased pCO 2 , despite a significant difference in otolith growth (Maneja et al 2013a, b). Further studies should be performed using older fish and applying the behavioral approaches used for coral reef fish.…”