Synchronous biological feedbacks in parrotfishes associated with pantropical coral bleaching

Biological feedbacks generated through patterns of disturbance are vital for sustaining ecosystem states. Recent ocean warming and thermal anomalies have caused pantropical episodes of coral bleaching, which has led to widespread coral mortality and a range of subsequent effects on coral reef communities. Although the response of many reef‐associated fishes to major disturbance events on coral reefs is negative (e.g., reduced abundance and condition), parrotfishes show strong feedbacks after disturbance to living reef structure manifesting as increases in abundance. However, the mechanisms underlying this response are poorly understood. Using biochronological reconstructions of annual otolith (ear stone) growth from two ocean basins, we tested whether parrotfish growth was enhanced following bleaching‐related coral mortality, thus providing an organismal mechanism for demographic changes in populations. Both major feeding guilds of parrotfishes (scrapers and excavators) exhibited enhanced growth of individuals after bleaching that was decoupled from expected thermal performance, a pattern that was not evident in other reef fish taxa from the same environment. These results provide evidence for a more nuanced ecological feedback system—one where disturbance plays a key role in mediating parrotfish–benthos interactions. By influencing the biology of assemblages, disturbance can thereby stimulate change in parrotfish grazing intensity and ultimately reef geomorphology over time. This feedback cycle operated historically at within‐reef scales; however, our results demonstrate that the scale, magnitude, and severity of recent thermal events are entraining the biological responses of disparate communities to respond in synchrony. This may fundamentally alter feedbacks in the relationships between parrotfishes and reef systems.     

Protection from illegal fishing and shark recovery restructures mesopredatory fish communities on a coral reef

The recovery of communities of predatory fishes within a no‐take marine reserve after the eradication of illegal fishing provides an opportunity to examine the role of sharks and other large‐bodied mesopredatory fishes in structuring reef fish communities. We used baited remote underwater video stations to investigate whether an increase in sharks was associated with a change in structure of the mesopredatory fish community at Ashmore Reef, Western Australia. We found an almost fourfold increase in shark abundance in reef habitat from 0.64 hr^?1 ± 0.15 SE in 2004, when Ashmore Reef was being fished illegally, to 2.45 hr^?1 ± 0.37 in 2016, after eight years of full‐time enforcement of the reserve. Shark recovery in reef habitat was accompanied by a two and a half‐fold decline in the abundance of small mesopredatory fishes (≤50 cm TL) (14.00 hr^?1 ± 3.79 to 5.6 hr^?1 ± 1.20) and a concomitant increase in large mesopredatory fishes (≥100 cm TL) from 1.82 hr^?1 ± 0.48 to 4.27 hr^?1 ± 0.93. In contrast, near‐reef habitats showed an increase in abundance of large mesopredatory fishes between years (2.00 hr^?1 ± 0.65 to 4.56 hr^?1 ± 1.11), although only smaller increases in sharks (0.67 hr^?1 ± 0.25 to 1.22 hr^?1 ± 0.34) and smaller mesopredatory fishes. Although the abundance of most mesopredatory groups increased with recovery from fishing, we suggest that the large decline of small mesopredatory fish in reef habitat was mostly due to higher predation pressure following the increase in sharks and large mesopredatory fishes. At the regional scale, the structure of fished communities at Ashmore Reef in 2004 resembled those of present day Scott Reefs, where fishing still continues today. In 2016, Ashmore fish communities resembled those of the Rowley Shoals, which have been protected from fishing for decades.     

Survival against the odds: ontogenetic changes in selective pressure mediate growth-mortality trade-offs in a marine fish

For organisms with complex life cycles, variation among individuals in traits associated with survival in one life-history stage can strongly affect the performance in subsequent stages with important repercussions on population dynamics. To identify which individual attributes are the most influential in determining patterns of survival in a cohort of reef fish, we compared the characteristics of Pomacentrus amboinensis surviving early juvenile stages on the reef with those of the cohort from which they originated. Individuals were collected at hatching, the end of the planktonic phase, and two, three, four, six and eight weeks post-settlement. Information stored in the otoliths of individual fish revealed strong carry-over effects of larval condition at hatching on juvenile survival, weeks after settlement (i.e. smaller-is-better). Among the traits examined, planktonic growth history was, by far, the most influential and long-lasting trait associated with juvenile persistence in reef habitats. However, otolith increments suggested that larval growth rate may not be maintained during early juvenile life, when selective mortality swiftly reverses its direction. These changes in selective pressure may mediate growth-mortality trade-offs between predation and starvation risks during early juvenile life. Ontogenetic changes in the shape of selectivity may be a mechanism maintaining phenotypic variation in growth rate and size within a population.     

Adaptive avoidance of reef noise

Auditory information is widely used throughout the animal kingdom in both terrestrial and aquatic environments. Some marine species are dependent on reefs for adult survival and reproduction, and are known to use reef noise to guide orientation towards suitable habitat. Many others that forage in food-rich inshore waters would, however, benefit from avoiding the high density of predators resident on reefs, but nothing is known about whether acoustic cues are used in this context. By analysing a sample of nearly 700,000 crustaceans, caught during experimental playbacks in light traps in the Great Barrier Reef lagoon, we demonstrate an auditory capability in a broad suite of previously neglected taxa, and provide the first evidence in any marine organisms that reef noise can act as a deterrent. In contrast to the larvae of species that require reef habitat for future success, which showed an attraction to broadcasted reef noise, taxa with a pelagic or nocturnally emergent lifestyle actively avoided it. Our results suggest that a far greater range of invertebrate taxa than previously thought can respond to acoustic cues, emphasising yet further the potential negative impact of globally increasing levels of underwater anthropogenic noise.     

Effects of ocean acidification on learning in coral reef fishes

Ocean acidification has the potential to cause dramatic changes in marine ecosystems. Larval damselfish exposed to concentrations of CO(2) predicted to occur in the mid- to late-century show maladaptive responses to predator cues. However, there is considerable variation both within and between species in CO(2) effects, whereby some individuals are unaffected at particular CO(2) concentrations while others show maladaptive responses to predator odour. Our goal was to test whether learning via chemical or visual information would be impaired by ocean acidification and ultimately, whether learning can mitigate the effects of ocean acidification by restoring the appropriate responses of prey to predators. Using two highly efficient and widespread mechanisms for predator learning, we compared the behaviour of pre-settlement damselfish Pomacentrus amboinensis that were exposed to 440 μatm CO(2) (current day levels) or 850 μatm CO(2), a concentration predicted to occur in the ocean before the end of this century. We found that, regardless of the method of learning, damselfish exposed to elevated CO(2) failed to learn to respond appropriately to a common predator, the dottyback, Pseudochromis fuscus. To determine whether the lack of response was due to a failure in learning or rather a short-term shift in trade-offs preventing the fish from displaying overt antipredator responses, we conditioned 440 or 700 μatm-CO(2) fish to learn to recognize a dottyback as a predator using injured conspecific cues, as in Experiment 1. When tested one day post-conditioning, CO(2) exposed fish failed to respond to predator odour. When tested 5 days post-conditioning, CO(2) exposed fish still failed to show an antipredator response to the dottyback odour, despite the fact that both control and CO(2)-treated fish responded to a general risk cue (injured conspecific cues). These results indicate that exposure to CO(2) may alter the cognitive ability of juvenile fish and render learning ineffective.     

Cleaner wrasse influence habitat selection of young damselfish

The presence of bluestreak cleaner wrasse, Labroides dimidiatus, on coral reefs increases total abundance and biodiversity of reef fishes. The mechanism(s) that cause such shifts in population structure are unclear, but it is possible that young fish preferentially settle into microhabitats where cleaner wrasse are present. As a first step to investigate this possibility, we conducted aquarium experiments to examine whether settlement-stage and young juveniles of ambon damselfish, Pomacentrus amboinensis, selected a microhabitat near a cleaner wrasse (adult or juvenile). Both settlement-stage (0 d post-settlement) and juvenile (~5 weeks post-settlement) fish spent a greater proportion of time in a microhabitat adjacent to L. dimidiatus than in one next to a control fish (a non-cleaner wrasse, Halichoeres melanurus) or one where no fish was present. This suggests that cleaner wrasse may serve as a positive cue during microhabitat selection. We also conducted focal observations of cleaner wrasse and counts of nearby damselfishes (1 m radius) to examine whether newly settled fish obtained direct benefits, in the form of cleaning services, from being near a cleaner wrasse. Although abundant, newly settled recruits (<20 mm total length) were rarely (2 %) observed being cleaned in 20 min observations compared with larger damselfishes (58 %). Individual damselfish that were cleaned were significantly larger than the median size of the surrounding nearby non-cleaned conspecifics; this was consistent across four species. The selection by settlement-stage fish of a microhabitat adjacent to cleaner wrasse in the laboratory, despite only being rarely cleaned in the natural environment, suggests that even rare cleaning events and/or indirect benefits may drive their settlement choices. This behaviour may also explain the decreased abundance of young fishes on reefs from which cleaner wrasse had been experimentally removed. This study reinforces the potentially important role of mutualism during the processes of settlement and recruitment of young reef fishes.     

The back-calculation of size and growth from otoliths: Validation and comparison of models at an individual level

Multiple internal and external tagging experiments tested the applicability of five back-calculation models (Biological Intercept, Modified-Fry, Body Proportional Hypothesis, Time-Varying Growth, and an Age-Effects model) as predictors of individual growth trajectories of two marine cleaning gobies, Elacatinus evelynae and E. prochilos, that were raised in aquaria under conditions that resulted in variable growth. Mixed-effect model analyses of longitudinal records of otoliths and somatic growth collected at the individual level revealed that E. evelynae and E. prochilos produced daily increments on their otoliths for up to two months post-settlement and that the Modified-Fry model provided the most accurate size-at-age estimates despite the presence of age, growth and time-varying growth effects in the dataset. Very large errors in predicted size were produced by the Age-Effects model. The four other back-calculation models all provided slightly biased estimates of back-calculated size-at-age, with the Modified-Fry model providing the least biased estimates. Regardless of bias, both experimental and theoretical evidence indicated that back-calculated size was a better proxy of fish length than otoliths radius. Relationships between fish length and otoliths radius were allometric at the level of individuals, which explained why the Modified-Fry model performed better. However, this allometry was undetectable at the population level. This study represents the first attempt to validate modern back-calculation models using longitudinal data collected and analysed at the individual level. Our results suggest the use of the Modified-Fry model as a conservative approach in routine back-calculations of fish size at age from otoliths.     

Restoring depleted coral‐reef fish populations through recruitment enhancement: a proof of concept

To determine whether enhancing the survival of new recruits is a sensible target for the restorative management of depleted coral‐reef fish populations, settlement‐stage ambon damsel fish Pomacentrus amboinensis were captured, tagged and then either released immediately onto small artificial reefs or held in aquaria for 1 week prior to release. Holding conditions were varied to determine whether they affected survival of fish: half the fish were held in bare tanks (non‐enriched) and the other half in tanks containing coral and sand (enriched). Holding fish for this short period had a significantly positive effect on survivorship relative to the settlement‐stage treatment group that were released immediately. The enrichment of holding conditions made no appreciable difference on the survival of fish once released onto the reef. It did, however, have a positive effect on the survival of fish while in captivity, thus supporting the case for the provision of simple environmental enrichment in fish husbandry. Collecting and holding settlement‐stage fish for at least a week before release appear to increase the short‐term survival of released fish; whether it is an effective method for longer‐term enhancement of locally depleted coral‐reef fish populations will require further study.     

Does a snapshot show the whole picture? Intrinsic limitations to growth inference of the short lived and fast growing

Individual growth patterns in ecology are often determined from population field data through the use of regression and model selection inference analyses. However, such approaches are typically unable to provide insight into dynamic processes when based upon collections of ‘snapshot’ data that consist of only a single observation for each individual. We caution how model selection inference from size-at-age data may lead to growth models that are mis-specified in the case of species such as squid and fishes that display fast and variable growth and for which, field data of the early part of the lifespan are typically sparse and difficult to obtain.     

Water temperature and fish growth: otoliths predict growth patterns of a marine fish in a changing climate

Ecological modeling shows that even small, gradual changes in body size in a fish population can have large effects on natural mortality, biomass, and catch. However, efforts to model the impact of climate change on fish growth have been hampered by a lack of long‐term (multidecadal) data needed to understand the effects of temperature on growth rates in natural environments. We used a combination of dendrochronology techniques and additive mixed‐effects modeling to examine the sensitivity of growth in a long‐lived (up to 70 years), endemic marine fish, the western blue groper (Achoerodus gouldii), to changes in water temperature. A multi‐decadal biochronology (1952–2003) of growth was constructed from the otoliths of 56 fish collected off the southwestern coast of Western Australia, and we tested for correlations between the mean index chronology and a range of potential environmental drivers. The chronology was significantly correlated with sea surface temperature in the region, but common variance among individuals was low. This suggests that this species has been relatively insensitive to past variations in climate. Growth increment and age data were also used in an additive mixed model to predict otolith growth and body size later this century. Although growth was relatively insensitive to changes in temperature, the model results suggested that a fish aged 20 in 2099 would have an otolith about 10% larger and a body size about 5% larger than a fish aged 20 in 1977. Our study shows that species or populations regarded as relatively insensitive to climate change could still undergo significant changes in growth rate and body size that are likely to have important effects on the productivity and yield of fisheries.