Shark teeth can resist ocean acidification.

Ocean acidification can cause dissolution of calcium carbonate minerals in biological structures of many marine organisms, which can be exacerbated by warming. However, it is still unclear whether this also affects organisms that have body parts made of calcium phosphate minerals (e.g. shark teeth), which may also be impacted by the 'corrosive' effect of acidified seawater. Thus, we examined the effect of ocean acidification and warming on the mechanical properties of shark teeth (Port Jackson shark, Heterodontus portusjacksoni), and assessed whether their mineralogical properties can be modified in response to predicted near-future seawater pH (-0.3 units) and temperature (+3°C) changes. We found that warming resulted in the production of more brittle teeth (higher elastic modulus and lower mechanical resilience) that were more vulnerable to physical damage. Yet, when combined with ocean acidification, the durability of teeth increased (i.e. less prone to physical damage due to the production of more elastic teeth) so that they did not differ from those raised under ambient conditions. The teeth were chiefly made of fluorapatite (Ca5 (PO4 )3 F), with increased fluoride content under ocean acidification that was associated with increased crystallinity. The increased precipitation of this highly insoluble mineral under ocean acidification suggests that the sharks could modulate and enhance biomineralization to produce teeth which are more resistant to corrosion. This adaptive mineralogical adjustment could allow some shark species to maintain durability and functionality of their teeth, which underpins a fundamental component of predation and sustenance of the trophic dynamics of future oceans.

Near-future ocean warming and acidification alter foraging behaviour, locomotion, and metabolic rate in a keystone marine mollusc.

Environmentally-induced changes in fitness are mediated by direct effects on physiology and behaviour, which are tightly linked. We investigated how predicted ocean warming (OW) and acidification (OA) affect key ecological behaviours (locomotion speed and foraging success) and metabolic rate of a keystone marine mollusc, the sea hare Stylocheilus striatus, a specialist grazer of the toxic cyanobacterium Lyngbya majuscula. We acclimated sea hares to OW and/or OA across three developmental stages (metamorphic, juvenile, and adult) or as adults only, and compare these to sea hares maintained under current-day conditions. Generally, locomotion speed and time to locate food were reduced ~1.5- to 2-fold when the stressors (OW or OA) were experienced in isolation, but reduced ~3-fold when combined. Decision-making was also severely altered, with correct foraging choice nearly 40% lower under combined stressors. Metabolic rate appeared to acclimate to the stressors in isolation, but was significantly elevated under combined stressors. Overall, sea hares that developed under OW and/or OA exhibited a less severe impact, indicating beneficial phenotypic plasticity. Reduced foraging success coupled with increased metabolic demands may impact fitness in this species and highlight potentially large ecological consequences under unabated OW and OA, namely in regulating toxic cyanobacteria blooms on coral reefs.

Reproductive phenotype predicts adult bite-force performance in sex-reversed dragons (Pogona vitticeps).

Sex-related differences in morphology and behavior are well documented, but the relative contributions of genes and environment to these traits are less well understood. Species that undergo sex reversal, such as the central bearded dragon (Pogona vitticeps), offer an opportunity to better understand sexually dimorphic traits because sexual phenotypes can exist on different chromosomal backgrounds. Reproductively female dragons with a discordant sex chromosome complement (sex reversed), at least as juveniles, exhibit traits in common with males (e.g., longer tails and greater boldness). However, the impact of sex reversal on sexually dimorphic traits in adult dragons is unknown. Here, we investigate the effect of sex reversal on bite-force performance, which may be important in resource acquisition (e.g., mates and/or food). We measured body size, head size, and bite force of the three sexual phenotypes in a colony of captive animals. Among adults, we found that males (ZZm) bite more forcefully than either chromosomally concordant females (ZWf) or sex-reversed females (ZZf), and this difference is associated with having relatively larger head dimensions. Therefore, adult sex-reversed females, despite apparently exhibiting male traits as juveniles, do not develop the larger head and enhanced bite force of adult male bearded dragons. This pattern is further illustrated in the full sample by a lack of positive allometry of bite force in sex-reversed females that is observed in males. The results reveal a close association between reproductive phenotype and bite force performance, regardless of sex chromosome complement.

On the wrong track: ocean acidification attracts larval fish to irrelevant environmental cues.

Population replenishment of marine life largely depends on successful dispersal of larvae to suitable adult habitat. Ocean acidification alters behavioural responses to physical and chemical cues in marine animals, including the maladaptive deterrence of settlement-stage larval fish to odours of preferred habitat and attraction to odours of non-preferred habitat. However, sensory compensation may allow fish to use alternative settlement cues such as sound. We show that future ocean acidification reverses the attraction of larval fish (barramundi) to their preferred settlement sounds (tropical estuarine mangroves). Instead, acidification instigates an attraction to unfamiliar sounds (temperate rocky reefs) as well as artificially generated sounds (white noise), both of which were ignored by fish living in current day conditions. This finding suggests that by the end of the century, following a business as usual CO2 emission scenario, these animals might avoid functional environmental cues and become attracted to cues that provide no adaptive advantage or are potentially deleterious. This maladaptation could disrupt population replenishment of this and other economically important species if animals fail to adapt to elevated CO2 conditions.

Ocean acidification alters temperature and salinity preferences in larval fish.

Ocean acidification alters the way in which animals perceive and respond to their world by affecting a variety of senses such as audition, olfaction, vision and pH sensing. Marine species rely on other senses as well, but we know little of how these might be affected by ocean acidification. We tested whether ocean acidification can alter the preference for physicochemical cues used for dispersal between ocean and estuarine environments. We experimentally assessed the behavioural response of a larval fish (Lates calcarifer) to elevated temperature and reduced salinity, including estuarine water of multiple cues for detecting settlement habitat. Larval fish raised under elevated CO2 concentrations were attracted by warmer water, but temperature had no effect on fish raised in contemporary CO2 concentrations. In contrast, contemporary larvae were deterred by lower salinity water, where CO2-treated fish showed no such response. Natural estuarine water-of higher temperature, lower salinity, and containing estuarine olfactory cues-was only preferred by fish treated under forecasted high CO2 conditions. We show for the first time that attraction by larval fish towards physicochemical cues can be altered by ocean acidification. Such alterations to perception and evaluation of environmental cues during the critical process of dispersal can potentially have implications for ensuing recruitment and population replenishment. Our study not only shows that freshwater species that spend part of their life cycle in the ocean might also be affected by ocean acidification, but that behavioural responses towards key physicochemical cues can also be negated through elevated CO2 from human emissions.

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

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 CO2 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 CO2-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.

Ocean acidification boosts larval fish development but reduces the window of opportunity for successful settlement.

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 CO2, 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 CO2 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.

Ocean acidification and global warming impair shark hunting behaviour and growth.

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.