Ben Radford

Climate-driven regime shift of a temperate marine ecosystem

No turning back? Ecosystems over time have endured much disturbance, yet they tend to remain intact, a characteristic we call resilience. Though many systems have been lost and destroyed, for systems that remain physically intact, there is debate as to whether changing temperatures will result in shifts or collapses. Wernburg et al. show that extreme warming of a temperate kelp forest off Australia resulted not only in its collapse, but also in a shift in community composition that brought about an increase in herbivorous tropical fishes that prevent the reestablishment of kelp. Thus, many systems may not be resilient to the rapid climate change that we face. Science, this issue p. 169 Rapid warming tropicalizes a temperate kelp forest. 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.

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.

Environmental factors controlling the distribution of symbiodinium harboured by the coral acropora millepora on the great barrier reef

Background The Symbiodinium community associated with scleractinian corals is widely considered to be shaped by seawater temperature, as the corals upper temperature tolerance is largely contingent on the Symbiodinium types harboured. Few studies have challenged this paradigm as knowledge of other environmental drivers on the distribution of Symbiodinium is limited. Here, we examine the influence of a range of environmental variables on the distribution of Symbiodinium associated with Acropora millepora collected from 47 coral reefs spanning 1,400 km on the Great Barrier Reef (GBR), Australia. Methodology/Principal Findings The environmental data included Moderate Resolution Imaging Spectroradiometer (MODIS) satellite data at 1 km spatial resolution from which a number of sea surface temperature (SST) and water quality metrics were derived. In addition, the carbonate and mud composition of sediments were incorporated into the analysis along with in situ water quality samples for a subset of locations. Analyses were conducted at three spatio-temporal scales [GBR (regional-scale), Whitsunday Islands (local-scale) and Keppel Islands/Trunk Reef (temporal)] to examine the effects of scale on the distribution patterns. While SST metrics were important drivers of the distribution of Symbiodinium types at regional and temporal scales, our results demonstrate that spatial variability in water quality correlates significantly with Symbiodinium distribution at local scales. Background levels of Symbiodinium types were greatest at turbid inshore locations of the Whitsunday Islands where SST predictors were not as important. This was not the case at regional scales where combinations of mud and carbonate sediment content coupled with SST anomalies and mean summer SST explained 51.3% of the variation in dominant Symbiodinium communities. Conclusions/Significance Reef corals may respond to global-scale stressors such as climate change through changes in their resident symbiont communities, however, management of local-scale stressors such as altered water quality is also necessary for maintenance of coral-Symbiodinium associations.

The sponge gardens of Ningaloo Reef, Western Australia

Preliminary results from biodiversity surveys in the deeper waters of Ningaloo Marine Park, Western Australia revealed that while much of the area is composed of sediments and rhodolith fields with low densities of macro- epibenthos, locally dense and extensive filter feeding communities exist. They were distinctly dominated by demosponges, both in biomass and diversity. A subsample of dominant taxa determined by fresh weight yielded 155 different demosponge species from over 350 transects between 18-102 m depth. Data from three successive years of sampling indicated that only a few species were ubiquitous, suggesting that as minor species are identified the cumulative species list will significantly exceed the present species record. This implies greatly enhanced biodiversity values associated with Ningaloo Marine Park, complementing records attributed to the shallow coral reef environment. The richness of the observed filter feeding communities adds additional weight to the increasing perception of Australia as a global hotspot for Porifera biodiversity.

Behavioural mediation of the costs and benefits of fast growth in a marine fish

Trade-offs between the costs and benefits of growth are thought to be mediated by behaviour, whereby rapid growth is associated with greater predation mortality because of increased foraging effort. We tested this hypothesis by collecting young Pomacentrus amboinensis using light traps and settling them onto patch reefs where their behaviour and survivorship were monitored for 24 h. One month later, individuals of the same cohort were collected from shallow reefs and released onto patch reefs where their behaviour and survivorship were monitored for 6 days. At settlement young fish suffered high (60% in 24 h) mortality that preferentially removed larger, faster-growing individuals. However, we could find no evidence that foraging behaviour contributed to this selective mortality. In contrast, 1 month later the same cohort underwent negative size-selective mortality where the smallest, slower-growing fish were preferentially removed by predators. Larger fish spent more time foraging, were more aggressive, swam greater distances and chased more fish than smaller individuals. Thus, consistent individual differences in behaviour contributed to patterns of mortality, but in a way that involved no apparent trade-off with growth. For P. amboinensis, consistent variation in growth may be maintained by spatial and temporal differences in the selective regime within the reef environment.

A Rapid Method for Determining Lipid Fraction Ratios of Hard Corals under Varying Sediment and Light Regimes

Environmental Context.Monitoring the health of coral reef systems is vitally important to maintain and manage these threatened, complex and biodiverse natural ecosystems. Although total lipid content has been suggested as a potential index of coral condition, current methods of measurement are time consuming, technically challenging and expensive. These limitations have prohibited the application of coral lipid content as an impact-monitoring tool. The development of a practical and rapid method to determine lipid fraction ratios has the potential to lead towards an effective tool for coral reef monitoring. Abstract.Lipid content has been used as a measure of energetic status and condition in a number of fish and invertebrate species and can potentially be applied to hard corals. However, common methods for measuring lipid content are time consuming, technically challenging and expensive and these limitations have prohibited the application of lipid content as an impact-monitoring tool. To overcome these limitations, a rapid low-tech method for determining neutral to polar lipid ratios from hard coral tissue samples has been developed. This paper describes the development of the method together with a preliminary application of the technique carried out in a field study to determine whether the relative amounts of non-polar storage lipid to polar structural lipid may provide insight into the nutritional condition of individual coral colonies under differing environmental stresses. Variation in the lipid ratios of the hard coral Acropora nobilis, collected from the Montebello Islands off Western Australia, was correlated with local light and sediment regimes. This initial application of the method has demonstrated the viability of the technique, which subsequently has the potential to be applied in the analysis of a large number of samples as would be required in environmental monitoring.

Symbiodinium Genotypic and Environmental Controls on Lipids in Reef Building Corals

Background Lipids in reef building corals can be divided into two classes; non-polar storage lipids, e.g. wax esters and triglycerides, and polar structural lipids, e.g. phospholipids and cholesterol. Differences among algal endosymbiont types are known to have important influences on processes including growth and the photobiology of scleractinian corals yet very little is known about the role of symbiont types on lipid energy reserves. Methodology/Principal Findings The ratio of storage lipid and structural lipid fractions of Scott Reef corals were determined by thin layer chromatography. The lipid fraction ratio varied with depth and depended on symbiont type harboured by two corals (Seriatopora hystrix and Pachyseris speciosa). S. hystrix colonies associated with Symbiodinium C1 or C1/C# at deep depths (>23 m) had lower lipid fraction ratios (i.e. approximately equal parts of storage and structural lipids) than those with Symbiodinium D1 in shallow depths (<23 m), which had higher lipid fraction ratios (i.e. approximately double amounts of storage relative to structural lipid). Further, there was a non-linear relationship between the lipid fraction ratio and depth for S. hystrix with a modal peak at ∼23 m coinciding with the same depth as the shift from clade D to C types. In contrast, the proportional relationship between the lipid fraction ratio and depth for P. speciosa, which exhibited high specificity for Symbiodinium C3 like across the depth gradient, was indicative of greater amounts of storage lipids contained in the deep colonies. Conclusions/Significance This study has demonstrated that Symbiodinium exert significant controls over the quality of coral energy reserves over a large-scale depth gradient. We conclude that the competitive advantages and metabolic costs that arise from flexible associations with divergent symbiont types are offset by energetic trade-offs for the coral host.

Classification and Regression Tree and Spatial Analyses Reveal Geographic Heterogeneity in Genome Wide Linkage Study of Indian Visceral Leishmaniasis

Background Genome wide linkage studies (GWLS) have provided evidence for loci controlling visceral leishmaniasis on Chromosomes 1p22, 6q27, 22q12 in Sudan and 6q27, 9p21, 17q11-q21 in Brazil. Genome wide studies from the major focus of disease in India have not previously been reported. Methods and Findings We undertook a GWLS in India in which a primary ∼10 cM (515 microsatellites) scan was carried out in 58 multicase pedigrees (74 nuclear families; 176 affected, 353 total individuals) and replication sought in 79 pedigrees (102 nuclear families; 218 affected, 473 total individuals). The primary scan provided evidence (≥2 adjacent markers allele-sharing LOD≥0.59; nominal P≤0.05) for linkage on Chromosomes 2, 5, 6, 7, 8, 10, 11, 20 and X, with peaks at 6p25.3-p24.3 and 8p23.1-p21.3 contributed to largely by 31 Hindu families and at Xq21.1-q26.1 by 27 Muslim families. Refined mapping confirmed linkage across all primary scan families at 2q12.2-q14.1 and 11q13.2-q23.3, but only 11q13.2-q23.3 replicated (combined LOD = 1.59; P = 0.0034). Linkage at 6p25.3-p24.3 and 8p23.1-p21.3, and at Xq21.1-q26.1, was confirmed by refined mapping for primary Hindu and Muslim families, respectively, but only Xq21.1-q26.1 replicated across all Muslim families (combined LOD 1.49; P = 0.0045). STRUCTURE and SMARTPCA did not identify population genetic substructure related to religious group. Classification and regression tree, and spatial interpolation, analyses confirm geographical heterogeneity for linkages at 6p25.3-p24.3, 8p23.1-p21.3 and Xq21.1-q26.1, with specific clusters of families contributing LOD scores of 2.13 (P = 0.0009), 1.75 (P = 0.002) and 1.84 (P = 0.001), respectively. Conclusions GWLS has identified novel loci that show geographical heterogeneity in their influence on susceptibility to VL in India.

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.

A robust operational model for predicting where tropical cyclone waves damage coral reefs.

Tropical cyclone (TC) waves can severely damage coral reefs. Models that predict where to find such damage (the ‘damage zone’) enable reef managers to: 1) target management responses after major TCs in near-real time to promote recovery at severely damaged sites; and 2) identify spatial patterns in historic TC exposure to explain habitat condition trajectories. For damage models to meet these needs, they must be valid for TCs of varying intensity, circulation size and duration. Here, we map damage zones for 46 TCs that crossed Australia’s Great Barrier Reef from 1985–2015 using three models – including one we develop which extends the capability of the others. We ground truth model performance with field data of wave damage from seven TCs of varying characteristics. The model we develop (4MW) out-performed the other models at capturing all incidences of known damage. The next best performing model (AHF) both under-predicted and over-predicted damage for TCs of various types. 4MW and AHF produce strikingly different spatial and temporal patterns of damage potential when used to reconstruct past TCs from 1985–2015. The 4MW model greatly enhances both of the main capabilities TC damage models provide to managers, and is useful wherever TCs and coral reefs co-occur.