Incorporating uncertainty in Indigenous sea Country monitoring with Bayesian statistics: Towards more informed decision-making.

Partnerships in marine monitoring combining Traditional Ecological Knowledge and western science are developing globally to improve our understanding of temporal changes in ecological communities that better inform coastal management practices. A fuller communication between scientists and Indigenous partners about the limitations of monitoring results to identify change is essential to the impact of monitoring datasets on decision-making. Here we present a 5-year co-developed case study from a fish monitoring partnership in northwest Australia showing how uncertainty estimated by Bayesian models can be incorporated into monitoring management indicators. Our simulation approach revealed there was high uncertainty in detecting immediate change over the following monitoring year when translated to health performance indicators. Incorporating credibility estimates into health assessments added substantial information to monitoring trends, provided a deeper understanding of monitoring limitations and highlighted the importance of carefully selecting the way we evaluate management performance indicators.

Macroalgae exhibit diverse responses to human disturbances on coral reefs.

Scientists and managers rely on indicator taxa such as coral and macroalgal cover to evaluate the effects of human disturbance on coral reefs, often assuming a universally positive relationship between local human disturbance and macroalgae. Despite evidence that macroalgae respond to local stressors in diverse ways, there have been few efforts to evaluate relationships between specific macroalgae taxa and local human-driven disturbance. Using genus-level monitoring data from 1205 sites in the Indian and Pacific Oceans, we assess whether macroalgae percent cover correlates with local human disturbance while accounting for factors that could obscure or confound relationships. Assessing macroalgae at genus level revealed that no genera were positively correlated with all human disturbance metrics. Instead, we found relationships between the division or genera of algae and specific human disturbances that were not detectable when pooling taxa into a single functional category, which is common to many analyses. The convention to use percent cover of macroalgae as an indication of local human disturbance therefore likely obscures signatures of local anthropogenic threats to reefs. Our limited understanding of relationships between human disturbance, macroalgae taxa, and their responses to human disturbances impedes the ability to diagnose and respond appropriately to these threats.

Comment on 'Lack of evidence for associative learning in pea plants'.

In 2016 we reported evidence for associative learning in plants (Gagliano et al., 2016). In view of the far-reaching implications of this finding we welcome the attempt made by Markel to replicate our study (Markel, 2020). However, as we discuss here, the protocol employed by Markel was unsuitable for testing for associative learning.

Towards modelling the future risk of cyclone wave damage to the world's coral reefs.

Tropical cyclones generate extreme waves that can damage coral reef communities. Recovery typically requires up to a decade, driving the trajectory of coral community structure. Coral reefs have evolved over millennia with cyclones. Increasingly, however, processes of recovery are interrupted and compromised by additional pressures (thermal stress, pollution, diseases, predators). Understanding how cyclones interact with other pressures to threaten coral reefs underpins spatial prioritization of conservation and management interventions. Models that simulate coral responses to cumulative pressures often assume that the worst cyclone wave damage occurs within ~100 km of the track. However, we show major coral loss at exposed sites up to 800 km from a cyclone that was both strong (high sustained wind speeds >=33 m/s) and big (widespread circulation >~300 km), using numerical wave models and field data from northwest Australia. We then calculate the return time of big and strong cyclones, big cyclones of any strength and strong cyclones of any size, for each of 150 coral reef ecoregions using a global data set of past cyclones from 1985 to 2015. For the coral ecoregions that regularly were exposed to cyclones during that time, we find that 75% of them were exposed to at least one cyclone that was both big and strong. Return intervals of big and strong cyclones are already less than 5 years for 13 ecoregions, primarily in the cyclone-prone NW Pacific, and less than 10 years for an additional 14 ecoregions. We identify ecoregions likely at higher risk in future given projected changes in cyclone activity. Robust quantification of the spatial distribution of likely cyclone wave damage is vital not only for understanding past coral response to pressures, but also for predicting how this may change as the climate continues to warm and the relative frequency of the strongest cyclones rises.

Tuned in: plant roots use sound to locate water.

Because water is essential to life, organisms have evolved a wide range of strategies to cope with water limitations, including actively searching for their preferred moisture levels to avoid dehydration. Plants use moisture gradients to direct their roots through the soil once a water source is detected, but how they first detect the source is unknown. We used the model plant Pisum sativum to investigate the mechanism by which roots sense and locate water. We found that roots were able to locate a water source by sensing the vibrations generated by water moving inside pipes, even in the absence of substrate moisture. When both moisture and acoustic cues were available, roots preferentially used moisture in the soil over acoustic vibrations, suggesting that acoustic gradients enable roots to broadly detect a water source at a distance, while moisture gradients help them to reach their target more accurately. Our results also showed that the presence of noise affected the abilities of roots to perceive and respond correctly to the surrounding soundscape. These findings highlight the urgent need to better understand the ecological role of sound and the consequences of acoustic pollution for plant as well as animal populations.

Learning by Association in Plants.

In complex and ever-changing environments, resources such as food are often scarce and unevenly distributed in space and time. Therefore, utilizing external cues to locate and remember high-quality sources allows more efficient foraging, thus increasing chances for survival. Associations between environmental cues and food are readily formed because of the tangible benefits they confer. While examples of the key role they play in shaping foraging behaviours are widespread in the animal world, the possibility that plants are also able to acquire learned associations to guide their foraging behaviour has never been demonstrated. Here we show that this type of learning occurs in the garden pea, Pisum sativum. By using a Y-maze task, we show that the position of a neutral cue, predicting the location of a light source, affected the direction of plant growth. This learned behaviour prevailed over innate phototropism. Notably, learning was successful only when it occurred during the subjective day, suggesting that behavioural performance is regulated by metabolic demands. Our results show that associative learning is an essential component of plant behaviour. We conclude that associative learning represents a universal adaptive mechanism shared by both animals and plants.

Influence of nursery microhabitats on the future abundance of a coral reef fish.

Species habitat associations are often complex, making it difficult to assess their influence on populations. Among coral reef fishes, habitat requirements vary among species and with ontogeny, but the relative importance of nursery and adult-preferred habitats on future abundances remain unclear. Moreover, adult populations may be influenced by recruitment of juveniles and assessments of habitat importance should consider relative effects of juvenile abundance. We conducted surveys across 16 sites and 200 km of reef to identify the microhabitat preferences of juveniles, sub-adults and adults of the damselfish Pomacentrus moluccensis Microhabitat preferences at different life-history stages were then combined with 6 years of juvenile abundance and microhabitat availability data to show that the availability of preferred juvenile microhabitat (corymbose corals) at the time of settlement was a strong predictor of future sub-adult and adult abundance. However, the influence of nursery microhabitats on future population size differed spatially and at some locations abundance of juveniles and adult microhabitat (branching corals) were better predictors of local populations. Our results demonstrate that while juvenile microhabitats are important nurseries, the abundance of coral-dependent fishes is not solely dependent on these microhabitats, especially when microhabitats are readily available or following large influxes of juveniles.

Climate-driven regime shift of a temperate marine ecosystem.

Ecosystem reconfigurations arising from climate-driven changes in species distributions are expected to have profound ecological, social, and economic implications. Here we reveal a rapid climate-driven regime shift of Australian temperate reef communities, which lost their defining kelp forests and became dominated by persistent seaweed turfs. After decades of ocean warming, extreme marine heat waves forced a 100-kilometer range contraction of extensive kelp forests and saw temperate species replaced by seaweeds, invertebrates, corals, and fishes characteristic of subtropical and tropical waters. This community-wide tropicalization fundamentally altered key ecological processes, suppressing the recovery of kelp forests.

Habitat Selectivity and Reliance on Live Corals for Indo-Pacific Hawkfishes (Family: Cirrhitidae).

Hawkfishes (family: Cirrhitidae) are small conspicuous reef predators that commonly perch on, or shelter within, the branches of coral colonies. This study examined habitat associations of hawkfishes, and explicitly tested whether hawkfishes associate with specific types of live coral. Live coral use and habitat selectivity of hawkfishes was explored at six locations from Chagos in the central Indian Ocean extending east to Fiji in the Pacific Ocean. A total of 529 hawkfishes from seven species were recorded across all locations with 63% of individuals observed perching on, or sheltering within, live coral colonies. Five species (all except Cirrhitus pinnulatus and Cirrhitichthys oxycephalus) associated with live coral habitats. Cirrhitichthys falco selected for species of Pocillopora while Paracirrhites arcatus and P. forsteri selected for both Pocillopora and Acropora, revealing that these habitats are used disproportionately more than expected based on the local cover of these coral genera. Habitat selection was consistent across geographic locations, and species of Pocillopora were the most frequently used and most consistently selected even though this coral genus never comprised more than 6% of the total coral cover at any of the locations. Across locations, Paracirrhites arcatus and P. forsteri were the most abundant species and variation in their abundance corresponded with local patterns of live coral cover and abundance of Pocilloporid corals, respectively. These findings demonstrate the link between small predatory fishes and live coral habitats adding to the growing body of literature highlighting that live corals (especially erect branching corals) are critically important for sustaining high abundance and diversity of fishes on coral reefs.

Facing the environment: onset and development of UV markings in young fish.

Most colour patterns in animals represent an elegant compromise between conspicuousness to ensure effective communication with preferred receivers and camouflage to avoid attracting the attention of unwanted predators. Many species, including several coral reef fishes, overcome this conflict by using ultraviolet (UV) colouration and signalling, as these colours are visible only over short distances and are often invisible to their predators. Despite a great interest in their behavioural significance and ecological influence on survival, little is known about when these colours first develop on the bodies of free-living animals. Here we show for the first time that the UV facial patterns of a coral reef fish do not develop in captivity but only when juveniles experience the socio-behavioural conditions of their natural environment. Using field and laboratory experiments, we determined that the onset and early development of these UV facial markings did not occur at metamorphosis. Instead, juveniles developed the UV markings during their first two weeks on the reef. Exposure to different reef environments revealed significant plasticity in the development of these markings. The direct or indirect (through intraspecific interactions) exposure to predators is a likely candidate trigger for the plastic development of these UV markings in the wild.

Experience teaches plants to learn faster and forget slower in environments where it matters.

The nervous system of animals serves the acquisition, memorization and recollection of information. Like animals, plants also acquire a huge amount of information from their environment, yet their capacity to memorize and organize learned behavioral responses has not been demonstrated. In Mimosa pudica-the sensitive plant-the defensive leaf-folding behaviour in response to repeated physical disturbance exhibits clear habituation, suggesting some elementary form of learning. Applying the theory and the analytical methods usually employed in animal learning research, we show that leaf-folding habituation is more pronounced and persistent for plants growing in energetically costly environments. Astonishingly, Mimosa can display the learned response even when left undisturbed in a more favourable environment for a month. This relatively long-lasting learned behavioural change as a result of previous experience matches the persistence of habituation effects observed in many animals.

Dynamic stability of coral reefs on the west Australian coast.

Monitoring changes in coral cover and composition through space and time can provide insights to reef health and assist the focus of management and conservation efforts. We used a meta-analytical approach to assess coral cover data across latitudes 10-35°S along the west Australian coast, including 25 years of data from the Ningaloo region. Current estimates of coral cover ranged between 3 and 44% in coral habitats. Coral communities in the northern regions were dominated by corals from the families Acroporidae and Poritidae, which became less common at higher latitudes. At Ningaloo Reef coral cover has remained relatively stable through time (∼28%), although north-eastern and southern areas have experienced significant declines in overall cover. These declines are likely related to periodic disturbances such as cyclones and thermal anomalies, which were particularly noticeable around 1998/1999 and 2010/2011. Linear mixed effects models (LME) suggest latitude explains 10% of the deviance in coral cover through time at Ningaloo. Acroporidae has decreased in abundance relative to other common families at Ningaloo in the south, which might be related to persistence of more thermally and mechanically tolerant families. We identify regions where quantitative time-series data on coral cover and composition are lacking, particularly in north-western Australia. Standardising routine monitoring methods used by management and research agencies at these, and other locations, would allow a more robust assessment of coral condition and a better basis for conservation of coral reefs.

Natural-born con artists and counterfeiters: Who is being deceived here?

Deception is ubiquitous in plant and animal kingdoms and is widely thought to provide selective advantages to the individual and evolutionary success to the species. Mimicry, a form of deception whereby an individual imitates their model to advantage by closely resembling their behavior or appearance, is particularly well documented and represented by the peripheral eyespots seen on the wings of many butterfly species. The significance of butterfly eyespots has been convincingly demonstrated to serve as an anti-predatory function either by imitation of a predator's own dangerous enemies (intimidation hypothesis) or by deflecting predator strikes toward less-vital parts of the body (deflection hypothesis). A convincing and compelling explanation in butterflies, the functional role of eyespots as anti-predatory devices has become a widely held and firmly entrenched belief that has been freely adopted into other systems. Here we comment on a recent paper that demonstrates a vastly different role for eyespots, that of intra-specific male-male competition, and make the point that even long-held beliefs need to be tested and challenged under different contexts if we are not to be deceived ourselves.

Spot the difference: mimicry in a coral reef fish.

Eyespots on the body of many animals have long been assumed to confer protection against predators, but empirical evidence has recently demonstrated that this may not always be the case and suggested that such markings may also serve other purposes. Clearly, this raises the unresolved question of what functions do these markings have and do they contribute to an individual's evolutionary fitness in the wild. Here, we examined the occurrence of eyespots on the dorsal fin of a coral reef damselfish (Pomacentrus amboinensis), where these markings are typical of the juvenile stage and fade away as the fish approaches sexual maturation to then disappear completely in the vast majority of, but not all, adult individuals. By exploring differences in body shape among age and gender groups, we found that individuals retaining the eyespot into adulthood are all sexually mature males, suggesting that these eyespots may be an adult deceptive signal. Interestingly, the body shape of these individuals resembled more closely that of immature females than mature dominant males. These results suggest that eyespots have multiple roles and their functional significance changes within the lifetime of an animal from being a juvenile advertisement to a deceptive adult signal. Male removal experiments or colour manipulations may be necessary to establish specific functions.

Using age-based life history data to investigate the life cycle and vulnerability of Octopus cyanea.

Octopus cyanea is taken as an unregulated, recreationally fished species from the intertidal reefs of Ningaloo, Western Australia. Yet despite its exploitation and importance in many artisanal fisheries throughout the world, little is known about its life history, ecology and vulnerability. We used stylet increment analysis to age a wild O. cyanea population for the first time and gonad histology to examine their reproductive characteristics. O. cyanea conforms to many cephalopod life history generalisations having rapid, non-asymptotic growth, a short life-span and high levels of mortality. Males were found to mature at much younger ages and sizes than females with reproductive activity concentrated in the spring and summer months. The female dominated sex-ratios in association with female brooding behaviours also suggest that larger conspicuous females may be more prone to capture and suggests that this intertidal octopus population has the potential to be negatively impacted in an unregulated fishery. Size at age and maturity comparisons between our temperate bordering population and lower latitude Tanzanian and Hawaiian populations indicated stark differences in growth rates that correlate with water temperatures. The variability in life history traits between global populations suggests that management of O. cyanea populations should be tailored to each unique set of life history characteristics and that stylet increment analysis may provide the integrity needed to accurately assess this.

Coral recovery may not herald the return of fishes on damaged coral reefs.

The dynamic nature of coral reefs offers a rare opportunity to examine the response of ecosystems to disruption due to climate change. In 1998, the Great Barrier Reef experienced widespread coral bleaching and mortality. As a result, cryptobenthic fish assemblages underwent a dramatic phase-shift. Thirteen years, and up to 96 fish generations later, the cryptobenthic fish assemblage has not returned to its pre-bleach configuration. This is despite coral abundances returning to, or exceeding, pre-bleach values. The post-bleach fish assemblage exhibits no evidence of recovery. If these short-lived fish species are a model for their longer-lived counterparts, they suggest that (1) the full effects of the 1998 bleaching event on long-lived fish populations have yet to be seen, (2) it may take decades, or more, before recovery or regeneration of these long-lived species will begin, and (3) fish assemblages may not recover to their previous composition despite the return of corals.

Unprecedented mass bleaching and loss of coral across 12° of latitude in Western Australia in 2010-11.

BACKGROUND: Globally, coral bleaching has been responsible for a significant decline in both coral cover and diversity over the past two decades. During the summer of 2010-11, anomalous large-scale ocean warming induced unprecedented levels of coral bleaching accompanied by substantial storminess across more than 12° of latitude and 1200 kilometers of coastline in Western Australia (WA). METHODOLOGY/PRINCIPAL FINDINGS: Extreme La-Niña conditions caused extensive warming of waters and drove considerable storminess and cyclonic activity across WA from October 2010 to May 2011. Satellite-derived sea surface temperature measurements recorded anomalies of up to 5°C above long-term averages. Benthic surveys quantified the extent of bleaching at 10 locations across four regions from tropical to temperate waters. Bleaching was recorded in all locations across regions and ranged between 17% (±5.5) in the temperate Perth region, to 95% (±3.5) in the Exmouth Gulf of the tropical Ningaloo region. Coincident with high levels of bleaching, three cyclones passed in close proximity to study locations around the time of peak temperatures. Follow-up surveys revealed spatial heterogeneity in coral cover change with four of ten locations recording significant loss of coral cover. Relative decreases ranged between 22%-83.9% of total coral cover, with the greatest losses in the Exmouth Gulf. CONCLUSIONS/SIGNIFICANCE: The anomalous thermal stress of 2010-11 induced mass bleaching of corals along central and southern WA coral reefs. Significant coral bleaching was observed at multiple locations across the tropical-temperate divide spanning more than 1200 km of coastline. Resultant spatially patchy loss of coral cover under widespread and high levels of bleaching and cyclonic activity, suggests a degree of resilience for WA coral communities. However, the spatial extent of bleaching casts some doubt over hypotheses suggesting that future impacts to coral reefs under forecast warming regimes may in part be mitigated by southern thermal refugia.

Habitat associations of juvenile fish at Ningaloo Reef, Western Australia: the importance of coral and algae.

Habitat specificity plays a pivotal role in forming community patterns in coral reef fishes, yet considerable uncertainty remains as to the extent of this selectivity, particularly among newly settled recruits. Here we quantified habitat specificity of juvenile coral reef fish at three ecological levels; algal meadows vs. coral reefs, live vs. dead coral and among different coral morphologies. In total, 6979 individuals from 11 families and 56 species were censused along Ningaloo Reef, Western Australia. Juvenile fishes exhibited divergence in habitat use and specialization among species and at all study scales. Despite the close proximity of coral reef and algal meadows (10's of metres) 25 species were unique to coral reef habitats, and seven to algal meadows. Of the seven unique to algal meadows, several species are known to occupy coral reef habitat as adults, suggesting possible ontogenetic shifts in habitat use. Selectivity between live and dead coral was found to be species-specific. In particular, juvenile scarids were found predominantly on the skeletons of dead coral whereas many damsel and butterfly fishes were closely associated with live coral habitat. Among the coral dependent species, coral morphology played a key role in juvenile distribution. Corymbose corals supported a disproportionate number of coral species and individuals relative to their availability, whereas less complex shapes (i.e. massive & encrusting) were rarely used by juvenile fish. Habitat specialisation by juvenile species of ecological and fisheries importance, for a variety of habitat types, argues strongly for the careful conservation and management of multiple habitat types within marine parks, and indicates that the current emphasis on planning conservation using representative habitat areas is warranted. Furthermore, the close association of many juvenile fish with corals susceptible to climate change related disturbances suggests that identifying and protecting reefs resilient to this should be a conservation priority.

Ockham's razor gone blunt: coenzyme Q adaptation and redox balance in tropical reef fishes.

The ubiquitous coenzyme Q (CoQ) is a powerful antioxidant defence against cellular oxidative damage. In fishes, differences in the isoprenoid length of CoQ and its associated antioxidant efficacy have been proposed as an adaptation to different thermal environments. Here, we examine this broad contention by a comparison of the CoQ composition and its redox status in a range of coral reef fishes. Contrary to expectations, most species possessed CoQ(8) and their hepatic redox balance was mostly found in the reduced form. These elevated concentrations of the ubiquinol antioxidant are indicative of a high level of protection required against oxidative stress. We propose that, in contrast to the current paradigm, CoQ variation in coral reef fishes is not a generalized adaptation to thermal conditions, but reflects species-specific ecological habits and physiological constraints associated with oxygen demand.