Alterations in predation pressure can have large effects on trophically-structured systems. Modification of predator behaviour via ocean warming has been assessed by laboratory experimentation and metabolic theory. However, the influence of ocean acidification with ocean warming remains largely unexplored for mesopredators, including experimental assessments that incorporate key components of the assemblages in which animals naturally live. We employ a combination of long-term laboratory and mesocosm experiments containing natural prey and habitat to assess how warming and acidification affect the development, growth, and hunting behaviour in sharks. Although embryonic development was faster due to temperature, elevated temperature and CO2 had detrimental effects on sharks by not only increasing energetic demands, but also by decreasing metabolic efficiency and reducing their ability to locate food through olfaction. The combination of these effects led to considerable reductions in growth rates of sharks held in natural mesocosms with elevated CO2, either alone or in combination with higher temperature. Our results suggest a more complex reality for predators, where ocean acidification reduces their ability to effectively hunt and exert strong top-down control over food webs.

Locating appropriate settlement habitat is a crucial step in the life cycle of most benthic marine animals. In marine fish, this step involves the use of multiple senses, including audition, olfaction and vision. To date, most investigations of larval fish audition focus on the hearing thresholds to various frequencies of sounds without testing an ecological response to such sounds. Identifying responses to biologically relevant sounds at the development stage in which orientation is most relevant is fundamental. We tested for the existence of ontogenetic windows of reception to sounds that could act as orientation cues with a focus on vulnerability to alteration by human impacts. Here we show that larvae of a catadromous fish species (barramundi, Lates calcarifer) were attracted towards sounds from settlement habitat during a surprisingly short ontogenetic window of approximately 3 days. Yet, this auditory preference was reversed in larvae reared under end-of-century levels of elevated CO 2 , such that larvae are repelled from cues of settlement habitat. These future conditions also reduced the swimming speeds and heightened the anxiety levels of barramundi. Unexpectedly, an acceleration of development and onset of metamorphosis caused by elevated CO 2 were not accompanied by the earlier onset of attraction towards habitat sounds. This mismatch between ontogenetic development and the timing of orientation behaviour may reduce the ability of larvae to locate habitat or lead to settlement in unsuitable habitats. The misinterpretation of key orientation cues can have implications for population replenishment, which are only exacerbated when ontogenetic development decouples from the specific behaviours required for location of settlement habitats.

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.

Soundscapes are multidimensional spaces that carry meaningful information for many species about the location and quality of nearby and distant resources. Because soundscapes are the sum of the acoustic signals produced by individual organisms and their interactions, they can be used as a proxy for the condition of whole ecosystems and their occupants. Ocean acidification resulting from anthropogenic CO 2 emissions is known to have profound effects on marine life. However, despite the increasingly recognized ecological importance of soundscapes, there is no empirical test of whether ocean acidification can affect biological sound production. Using field recordings obtained from three geographically separated natural CO 2 vents, we show that forecasted end-of-century ocean acidification conditions can profoundly reduce the biological sound level and frequency of snapping shrimp snaps. Snapping shrimp were among the noisiest marine organisms and the suppression of their sound production at vents was responsible for the vast majority of the soundscape alteration observed. To assess mechanisms that could account for these observations, we tested whether long-term exposure (two to three months) to elevated CO 2 induced a similar reduction in the snapping behaviour (loudness and frequency) of snapping shrimp. The results indicated that the soniferous behaviour of these animals was substantially reduced in both frequency (snaps per minute) and sound level of snaps produced. As coastal marine soundscapes are dominated by biological sounds produced by snapping shrimp, the observed suppression of this component of soundscapes could have important and possibly pervasive ecological consequences for organisms that use soundscapes as a source of information. This trend towards silence could be of particular importance for those species whose larval stages use sound for orientation towards settlement habitats.

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