Philip L. Munday

Ocean acidification impairs olfactory discrimination and homing ability of a marine fish

The persistence of most coastal marine species depends on larvae finding suitable adult habitat at the end of an offshore dispersive stage that can last weeks or months. We tested the effects that ocean acidification from elevated levels of atmospheric carbon dioxide (CO2) could have on the ability of larvae to detect olfactory cues from adult habitats. Larval clownfish reared in control seawater (pH 8.15) discriminated between a range of cues that could help them locate reef habitat and suitable settlement sites. This discriminatory ability was disrupted when larvae were reared in conditions simulating CO2-induced ocean acidification. Larvae became strongly attracted to olfactory stimuli they normally avoided when reared at levels of ocean pH that could occur ca. 2100 (pH 7.8) and they no longer responded to any olfactory cues when reared at pH levels (pH 7.6) that might be attained later next century on a business-as-usual carbon-dioxide emissions trajectory. If acidification continues unabated, the impairment of sensory ability will reduce population sustainability of many marine species, with potentially profound consequences for marine diversity.

Ocean acidification disrupts the innate ability of fish to detect predator olfactory cues

While ocean acidification is predicted to threaten marine biodiversity, the processes that directly impact species persistence are not well understood. For marine species, early life history stages are inherently vulnerable to predators and an innate ability to detect predators can be critical for survival. However, whether or not acidification inhibits predator detection is unknown. Here, we show that newly hatched larvae of the marine fish Amphiprion percula innately detect predators using olfactory cues and this ability is retained through to settlement. Aquarium-reared larvae, not previously exposed to predators, were able to distinguish between the olfactory cues of predatory and non-predatory species. However, when eggs and larvae were exposed to seawater simulating ocean acidification (pH 7.8 and 1000 p.p.m. CO2) settlement-stage larvae became strongly attracted to the smell of predators and the ability to discriminate between predators and non-predators was lost. Newly hatched larvae were unaffected by CO2 exposure and were still able to distinguish between predatory and non-predatory fish. If this impairment of olfactory preferences in settlement-stage larvae translates to higher mortality as a result of increased predation risk, there could be direct consequences for the replenishment and the sustainability of marine populations.

Replenishment of fish populations is threatened by ocean acidification

There is increasing concern that ocean acidification, caused by the uptake of additional CO2 at the ocean surface, could affect the functioning of marine ecosystems; however, the mechanisms by which population declines will occur have not been identified, especially for noncalcifying species such as fishes. Here, we use a combination of laboratory and field-based experiments to show that levels of dissolved CO2 predicted to occur in the ocean this century alter the behavior of larval fish and dramatically decrease their survival during recruitment to adult populations. Altered behavior of larvae was detected at 700 ppm CO2, with many individuals becoming attracted to the smell of predators. At 850 ppm CO2, the ability to sense predators was completely impaired. Larvae exposed to elevated CO2 were more active and exhibited riskier behavior in natural coral-reef habitat. As a result, they had 5–9 times higher mortality from predation than current-day controls, with mortality increasing with CO2 concentration. Our results show that additional CO2 absorbed into the ocean will reduce recruitment success and have far-reaching consequences for the sustainability of fish populations.

Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function

A study of two species of coral reef fish demonstrates that the anticipated increase in atmospheric carbon dioxide directly interferes with neurotransmitter function in their larvae, a hitherto unrecognized problem for marine fishes. Predicted future CO2 levels have been found to alter sensory responses and behaviour of marine fishes. Changes include increased boldness and activity, loss of behavioural lateralization, altered auditory preferences and impaired olfactory function1,2,3,4,5. Impaired olfactory function makes larval fish attracted to odours they normally avoid, including ones from predators and unfavourable habitats1,3. These behavioural alterations have significant effects on mortality that may have far-reaching implications for population replenishment, community structure and ecosystem function2,6. However, the underlying mechanism linking high CO2 to these diverse responses has been unknown. Here we show that abnormal olfactory preferences and loss of behavioural lateralization exhibited by two species of larval coral reef fish exposed to high CO2 can be rapidly and effectively reversed by treatment with an antagonist of the GABA-A receptor. GABA-A is a major neurotransmitter receptor in the vertebrate brain. Thus, our results indicate that high CO2 interferes with neurotransmitter function, a hitherto unrecognized threat to marine populations and ecosystems. Given the ubiquity and conserved function of GABA-A receptors, we predict that rising CO2 levels could cause sensory and behavioural impairment in a wide range of marine species, especially those that tightly control their acid–base balance through regulatory changes in HCO3− and Cl− levels.

Climate change and coral reef connectivity

This review assesses and predicts the impacts that rapid climate change will have on population connectivity in coral reef ecosystems, using fishes as a model group. Increased ocean temperatures are expected to accelerate larval development, potentially leading to reduced pelagic durations and earlier reef-seeking behaviour. Depending on the spatial arrangement of reefs, the expectation would be a reduction in dispersal distances and the spatial scale of connectivity. Small increase in temperature might enhance the number of larvae surviving the pelagic phase, but larger increases are likely to reduce reproductive output and increase larval mortality. Changes to ocean currents could alter the dynamics of larval supply and changes to planktonic productivity could affect how many larvae survive the pelagic stage and their condition at settlement; however, these patterns are likely to vary greatly from place-to-place and projections of how oceanographic features will change in the future lack sufficient certainty and resolution to make robust predictions. Connectivity could also be compromised by the increased fragmentation of reef habitat due to the effects of coral bleaching and ocean acidification. Changes to the spatial and temporal scales of connectivity have implications for the management of coral reef ecosystems, especially the design and placement of marine-protected areas. The size and spacing of protected areas may need to be strategically adjusted if reserve networks are to retain their efficacy in the future.

Effects of climate change on fish reproduction and early life history stages

Seasonal change in temperature has a profound effect on reproduction in fish. Increasing temperatures cue reproductive development in spring-spawning species, and falling temperatures stimulate reproduction in autumn-spawners. Elevated temperatures truncate spring spawning, and delay autumn spawning. Temperature increases will affect reproduction, but the nature of these effects will depend on the period and amplitude of the increase and range from phase-shifting of spawning to complete inhibition of reproduction. This latter effect will be most marked in species that are constrained in their capacity to shift geographic range. Studies from a range of taxa, habitats and temperature ranges all show inhibitory effects of elevated temperature albeit about different environmental set points. The effects are generated through the endocrine system, particularly through the inhibition of ovarian oestrogen production. Larval fishes are usually more sensitive than adults to environmental fluctuations, and might be especially vulnerable to climate change. In addition to direct effects on embryonic duration and egg survival, temperature also influences size at hatching, developmental rate, pelagic larval duration and survival. A companion effect of marine climate change is ocean acidification, which may pose a significant threat through its capacity to alter larval behaviour and impair sensory capabilities. This in turn impacts on population replenishment and connectivity patterns of marine fishes.

Ocean acidification erodes crucial auditory behaviour in a marine fish

Ocean acidification is predicted to affect marine ecosystems in many ways, including modification of fish behaviour. Previous studies have identified effects of CO2-enriched conditions on the sensory behaviour of fishes, including the loss of natural responses to odours resulting in ecologically deleterious decisions. Many fishes also rely on hearing for orientation, habitat selection, predator avoidance and communication. We used an auditory choice chamber to study the influence of CO2-enriched conditions on directional responses of juvenile clownfish (Amphiprion percula) to daytime reef noise. Rearing and test conditions were based on Intergovernmental Panel on Climate Change predictions for the twenty-first century: current-day ambient, 600, 700 and 900 µatm pCO2. Juveniles from ambient CO2-conditions significantly avoided the reef noise, as expected, but this behaviour was absent in juveniles from CO2-enriched conditions. This study provides, to our knowledge, the first evidence that ocean acidification affects the auditory response of fishes, with potentially detrimental impacts on early survival.

Predicting evolutionary responses to climate change in the sea.

An increasing number of short-term experimental studies show significant effects of projected ocean warming and ocean acidification on the performance on marine organisms. Yet, it remains unclear if we can reliably predict the impact of climate change on marine populations and ecosystems, because we lack sufficient understanding of the capacity for marine organisms to adapt to rapid climate change. In this review, we emphasise why an evolutionary perspective is crucial to understanding climate change impacts in the sea and examine the approaches that may be useful for addressing this challenge. We first consider what the geological record and present-day analogues of future climate conditions can tell us about the potential for adaptation to climate change. We also examine evidence that phenotypic plasticity may assist marine species to persist in a rapidly changing climate. We then outline the various experimental approaches that can be used to estimate evolutionary potential, focusing on molecular tools, quantitative genetics, and experimental evolution, and we describe the benefits of combining different approaches to gain a deeper understanding of evolutionary potential. Our goal is to provide a platform for future research addressing the evolutionary potential for marine organisms to cope with climate change.

Settlement strategies and distribution patterns of coral-reef fishes

Patterns of habitat use established at settlement may be a primary determinant of the distribution of coral-reef fishes within and among habitats. However, due to the difficulty of observing fish larvae in the wild, the behaviour of individuals at settlement has rarely been observed. Here, we examined the behaviour at settlement of five species of damselfishes (family Pomacentridae) by conducting multi-choice experiments in large outdoor aquaria at Lizard Island on the Great Barrier Reef, Australia. Late-stage larvae that were competent to settle were collected using light traps and placed in large circular aquaria at night where they could choose to settle among live coral, dead branching coral, coral rubble and bare sand habitats. We examined patterns of habitat choice at settlement by larvae with no prior experience of the reef (naive larvae). The effect of experience in the reef environment on habitat preferences was then determined by studying the behaviour of juveniles collected soon after settlement and exposed to the same experimental protocol. We also examined the importance of interspecific interactions among late-stage larvae and interactions between newly settled juveniles and adults in determining patterns of habitat choice exhibited by larvae and newly settled juveniles. Late-stage larvae and newly settled juveniles made distinct habitat choices but the choices made varied widely among species. Chromis viridis (Cuvier) late-stage larvae selected live coral and always settled as a group. Post-settlement C. viridis also selected live coral but exhibited stronger schooling behaviour and moved around the aquaria more frequently than late-stage larvae. Pomacentrus moluccensis (Bleeker) consistently selected live coral and also preferentially selected habitats where conspecifics, either settlers or adults, were present. P. amboinensis (Bleeker) late-stage larvae preferentially selected both live and dead standing coral habitats but avoided coral rubble. Post-settlement P. amboinensis selected live coral more frequently than late-stage larvae. P. coelestis (Jordan and Starks) late-stage larvae initially settled with equal frequency among the habitats presented but exhibited an increasing use of coral rubble and dead coral throughout the day. In contrast, early post-settlers always selected the coral rubble habitat with significantly greater frequency than other habitats. Therefore, experience on the reef may be associated with habitat preferences in P. coelestis. P. chrysurus settlers were distributed evenly among habitats due to agonistic interactions among individuals observed within hours of settling. Also, early post-settlement P. chrysurus avoided habitats containing adults. For the pomacentrids we tested, the patterns of habitat selection observed in our experiments were similar to the distribution of adults among habitats on the reef at Lizard Island. Also, interactions among individuals at settlement could explain the spacing of individuals within habitats. Therefore, precise selection of habitats at settlement and behaviour among conspecifics within hours of settling may have a major influence on the distribution of coral-reef fishes within and among habitats.

INTERSPECIFIC COMPETITION AND COEXISTENCE IN A GUILD OF CORAL-DWELLING FISHES

We investigated the effects of interspecific competition on abundance, habitat partitioning, and coexistence of six closely related species of gobies (genus Gobiodon) that inhabit a range of acroporid coral species at Lizard Island, Great Barrier Reef. After documenting the extent of overlap in habitat use among pairs of species in the field, we used a combination of field and laboratory experiments to investigate the relationship between these patterns and the occurrence of interspecific competition. Experiments in aquaria tested the ability of five of the species to compete against G. histrio, the apparent competitive dominant, including the effects of body size and prior residency. A manipulative field experiment, in which abundance of G. histrio was reduced, tested whether competition with this species limits the abundance of the other five species. Two species competed for space with G. histrio in the field, yet overlap in habitat use with G. histrio was high for one of these species (G. axillaris) and low for the other (G. brochus). In aquaria, G. axillaris and G. histrio preferred the same species of coral and had equivalent, size-based, competitive abilities. The coexistence of G. axillaris and G. histrio at the scale of 10’s metres on the reef can thus be explained by a competitive lottery model. However, differential distributions of these two species across the reef flat and reef crest suggests that resource partitioning or habitat selection at larger spatial scales are also important to their coexistence. In aquaria, G. brochus was an inferior competitor to G. histrio and could only gain access to the preferred species of coral through an advantage in body size or prior residency. Low overlap in habitat use between G. brochus and G. histrio in the field appears to result from niche shifts by the subordinate competitor only, indicating coexistence via an included niche model. The field experiment indicated that the other three other species did not compete for space with G. histrio, and these species exhibited either low (G. rivulatus) or high (G. quinquestrigatus and G. unicolor) overlap in habitat use with G. histrio. Experiments in aquaria demonstrated that G. rivulatus and G. histrio did not compete because they preferred different species of coral. In contrast, G. unicolor and G. histrio exhibited high overlap in habitat use but did not compete because they were able to co-habit the same coral colonies without affecting each other. In aquaria, G. quinquestrigatus and G. histrio preferred the same coral species and G. quinquestrigatus was an inferior competitor, so these species were expected to compete for space in the field. In a field recolonization experiment, coral colonies previously occupied by G. quinquestrigatus were rarely recolonized by G. histrio, indicating that these species coexist because they use different types of coral colonies in the field. The study demonstrates that there is no single relationship between overlap in resource use and the occurrence of interspecific competition, even among closely related species, and that species within a guild can coexist by a diversity of mechanisms.