Lost at sea: ocean acidification undermines larval fish orientation via altered hearing and marine soundscape modification

Abstract

The dispersal of larvae and their settlement to suitable habitat is fundamental to the replenishment of marine populations and the communities in which they live. Sound plays an important role in this process because for larvae of various species, it acts as an orientational cue towards suitable settlement habitat. Because marine sounds are largely of biological origin, they not only carry information about the location of potential habitat, but also information about the quality of habitat. While ocean acidification is known to affect a wide range of marine organisms and processes, its effect on marine soundscapes and its reception by navigating oceanic larvae remains unknown. Here, we show that ocean acidification causes a switch in role of present-day soundscapes from attractor to repellent in the auditory preferences in a temperate larval fish. Using natural CO 2 vents as analogues of future ocean conditions, we further reveal that ocean acidification can impact marine soundscapes by profoundly diminishing their biological sound production. An altered soundscape poorer in biological cues indirectly penalizes oceanic larvae at settlement stage because both control and CO 2 -treated fish larvae showed lack of any response to such future soundscapes. These indirect and direct effects of ocean acidification put at risk the complex processes of larval dispersal and settlement.

Expression of genes involved in brain GABAergic neurotransmission in three-spined stickleback exposed to near-future CO2

“…The sensory systems affected include olfaction, hearing and vision (Munday et al ., 2009; Dixson et al ., 2010; Ferrari et al ., 2011; Simpson et al ., 2011; Forsgren et al ., 2013; Chung et al ., 2014; Rossi et al ., 2016). Other neural challenges detected involve brain lateralization (Domenici et al ., 2012; Nilsson et al ., 2012; Jutfelt et al ., 2013; Lai et al ., 2015), learning (Ferrari et al ., 2012), anxiety (Hamilton et al ., 2014), boldness and activity (Munday et al ., 2010; Jutfelt et al ., 2013).…”

Silent oceans: ocean acidification impoverishes natural soundscapes by altering sound production of the world's noisiest marine invertebrate

“…Future research could investigate the effect of CO 2 not only on sound-producing animals, but also on those species that are known to use sound as a settlement cue [20,51]. This aspect of research is of particular priority because CO 2 can reverse auditory preferences in fish [52][53][54]. The potential for adaptation to ocean acidification remains largely unknown, but recent findings show lack of trans-generational acclimation in fish [55].…”

Sensory System Responses to Human-Induced Environmental Change

“…Given their composition, otoliths are susceptible to either the reduced availability of carbonate ions in seawater at low pH, or to changes in the concentrations of bicarbonate and carbonate ions caused by acid-base regulation in fish exposed to high CO 2 levels (Munday et al, 2011b;Heuer and Grosell, 2014). An increase in otolith size was revealed in a range of species following exposure to as little as 64 µatm of additional CO 2 compared to control levels of CO 2 , in species such as sea bass larvae (Atractoscion nobilis) (Checkley et al, 2009), clownfish (A. percula) larvae (Munday et al, 2011b), juvenile walleye Pollock (Theragra chalcogramma) (Hurst et al, 2012), cobia (Rachycentron canadum) larvae (Bignami et al, 2013a,b), cod (Gadus morhua) larvae (Frommel et al, 2012;Maneja et al, 2013), juvenile sticklebacks (Gasterosteus aculeatus) (Schade et al, 2014), mahi-mahi (Coryphaena hippurus) larvae (Bignami et al, 2014), juvenile sea bream (Sparus aurata) (Réveillac et al, 2015), and mulloway (Argyrosomus japonicus) larvae (Rossi et al, 2016b). However, the otoliths of juvenile spiny damselfish (Acanthochromis polyacanthus) (Munday et al, 2011a), juvenile clownfish (A. percula) (Simpson et al, 2011), Atlantic herring (Clupea harengus) larvae (Franke and Clemmesen, 2011), and juvenile scup (Stenotomus chrysops, (Perry et al, 2015) showed no size differences at increased levels of CO 2 , whereas the size of the otoliths in marine medaka larvae, Oryzias melastigma, were even observed to be reduced (Mu et al, 2015).…”