Katharina E. Fabricius

CLASSIFICATION AND REGRESSION TREES: A POWERFUL YET SIMPLE TECHNIQUE FOR ECOLOGICAL DATA ANALYSIS

Classification and regression trees are ideally suited for the analysis of com- plex ecological data. For such data, we require flexible and robust analytical methods, which can deal with nonlinear relationships, high-order interactions, and missing values. Despite such difficulties, the methods should be simple to understand and give easily interpretable results. Trees explain variation of a single response variable by repeatedly splitting the data into more homogeneous groups, using combinations of explanatory var- iables that may be categorical and/or numeric. Each group is characterized by a typical value of the response variable, the number of observations in the group, and the values of the explanatory variables that define it. The tree is represented graphically, and this aids exploration and understanding. Trees can be used for interactive exploration and for description and prediction of patterns and processes. Advantages of trees include: (1) the flexibility to handle a broad range of response types, including numeric, categorical, ratings, and survival data; (2) invariance to monotonic transformations of the explanatory variables; (3) ease and ro- bustness of construction; (4) ease of interpretation; and (5) the ability to handle missing values in both response and explanatory variables. Thus, trees complement or represent an alternative to many traditional statistical techniques, including multiple regression, analysis of variance, logistic regression, log-linear models, linear discriminant analysis, and survival models. We use classification and regression trees to analyze survey data from the Australian central Great Barrier Reef, comprising abundances of soft coral taxa (Cnidaria: Octocorallia) and physical and spatial environmental information. Regression tree analyses showed that dense aggregations, typically formed by three taxa, were restricted to distinct habitat types, each of which was defined by combinations of 3-4 environmental variables. The habitat definitions were consistent with known experimental findings on the nutrition of these taxa. When used separately, physical and spatial variables were similarly strong predictors of abundances and lost little in comparison with their joint use. The spatial variables are thus effective surrogates for the physical variables in this extensive reef complex, where infor- mation on the physical environment is often not available. Finally, we compare the use of regression trees and linear models for the analysis of these data and show how linear models fail to find patterns uncovered by the trees.

The 27–year decline of coral cover on the Great Barrier Reef and its causes

The world’s coral reefs are being degraded, and the need to reduce local pressures to offset the effects of increasing global pressures is now widely recognized. This study investigates the spatial and temporal dynamics of coral cover, identifies the main drivers of coral mortality, and quantifies the rates of potential recovery of the Great Barrier Reef. Based on the world’s most extensive time series data on reef condition (2,258 surveys of 214 reefs over 1985–2012), we show a major decline in coral cover from 28.0% to 13.8% (0.53% y−1), a loss of 50.7% of initial coral cover. Tropical cyclones, coral predation by crown-of-thorns starfish (COTS), and coral bleaching accounted for 48%, 42%, and 10% of the respective estimated losses, amounting to 3.38% y−1 mortality rate. Importantly, the relatively pristine northern region showed no overall decline. The estimated rate of increase in coral cover in the absence of cyclones, COTS, and bleaching was 2.85% y−1, demonstrating substantial capacity for recovery of reefs. In the absence of COTS, coral cover would increase at 0.89% y−1, despite ongoing losses due to cyclones and bleaching. Thus, reducing COTS populations, by improving water quality and developing alternative control measures, could prevent further coral decline and improve the outlook for the Great Barrier Reef. Such strategies can, however, only be successful if climatic conditions are stabilized, as losses due to bleaching and cyclones will otherwise increase.

Declining Coral Calcification on the Great Barrier Reef

Reef-building corals are under increasing physiological stress from a changing climate and ocean absorption of increasing atmospheric carbon dioxide. We investigated 328 colonies of massive Porites corals from 69 reefs of the Great Barrier Reef (GBR) in Australia. Their skeletal records show that throughout the GBR, calcification has declined by 14.2% since 1990, predominantly because extension (linear growth) has declined by 13.3%. The data suggest that such a severe and sudden decline in calcification is unprecedented in at least the past 400 years. Calcification increases linearly with increasing large-scale sea surface temperature but responds nonlinearly to annual temperature anomalies. The causes of the decline remain unknown; however, this study suggests that increasing temperature stress and a declining saturation state of seawater aragonite may be diminishing the ability of GBR corals to deposit calcium carbonate.

Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity

Suspended particulate matter (SPM) strongly alters the trophic environment of photosymbiotic aquatic organisms. At high particles loads, phototrophic energy gains can be diminished due to light absorption by suspended particles, and stress from particle abrasion or deposition on tissues. However, energy gains are enhanced if organisms are able to use SPM as a food source. For photosymbiotic benthic suspension feeders, increases in SPM concentrations may require both phototrophic and heterotrophic acclimation to sustain a positive energy balance. This study provides an experimental analysis of the effects of contrasting light and SPM regimes on the energy budget (scope for growth) of two zooxanthellate corals (Goniastrea retiformis and Porites cylindrica). Using a factorial design in a flow-through tank system, corals were exposed for 2 months to shaded and unshaded conditions (equivalent to 3-4 m depth at 4 and 16 mg dry weight SPM l(-1), respectively) and a range of controlled SPM loads with a natural organic content ( approximately 3% w/w). In G. retiformis, rates of particle ingestion were a linear function of SPM concentration within a broad range (1-30 mg dry weight l(-1)). After 2 months of shading, photosynthetic acclimation was significant in G. retiformis, but did not compensate for the reduced light level, as daily respiration exceeded daily photosynthesis. However, in response to the prolonged shading, G. retiformis more than doubled its rate of particle feeding. At high SPM treatments (16 mg dw l(-1)), sediment feeding by this species compensated fully for the 35-47% lower phototrophy in the shaded treatment. Due to both photo- and heterotrophic plasticity, G. retiformis gained tissue and skeletal mass at all experimental levels of light and SPM. In contrast, rates of particle intake by P. cylindrica contributed <10% to the energy budget in shaded and <3% in unshaded conditions. Feeding rates of P. cylindrica were half-saturated at approximately 3 mg dry weight l(-1), and four- to eight-fold lower than those of G. retiformis. Skeletal growth was sustained, but tissue mass and lipid contents declined in shaded and high-SPM treatments, and carbon loss due to shading by SPM was not compensated for by particle feeding. Thus, due to a lack of photo- and heterotrophic plasticity, periods of high turbidity resulted in energy deficiency in P. cylindrica, and high turbidity conditions appeared physiologically unsustainable for this species. This study is the first to show heterotrophic plasticity in a symbiotic coral, and to show that such plasticity can offset stress from high particle loads. It demonstrates that changes in the trophic mode of some coral species are a mechanism for sustaining a positive energy balance in turbid environments, thereby broadening their physiological niche.

Recognition and selection of settlement substrata determine post-settlement survival in corals

Habitat recognition and selective settlement by dispersive propagules greatly increases the post-settlement survival chances of sessile organisms. To better understand the key role some species can play in the structure of highly complex coral reef ecosystems, we compare the role of two independent, but sequential, processes: settlement choice and post-settlement survival. This study describes the chemical and physical recognition and ranking of specific settlement substrata by coral larvae. Several species of crustose coralline algae (CCA) are known to induce coral settlement; however they also employ physical and biological anti-settlement defense strategies that vary greatly in effectiveness. We examine the interactions between settling larvae of two common reef building coral species (Acropora tenuis and A. millepora) and five species of CCA (Neogoniolithon fosliei, Porolithon onkodes, Hydrolithon reinboldii, Titanoderma prototypum, and Lithoporella melobesioides) that co-occur on reef crests and slopes of the Great Barrier Reef, Australia. Distinct settlement patterns were observed when coral larvae were provided with a choice of settlement substrata. Settlement on the most preferred substratum, the CCA species T. prototypum, was 15 times higher than on N. fosliei, the least preferred substratum. The rates of post-settlement survival of the corals also varied between CCA species in response to their anti-settlement strategies (shedding of surface cell layers, overgrowth, and potential chemical deterrents). Rates of larval settlement, post-settlement survival, and the sensitivity of larvae to chemical extracts of CCA were all positively correlated across the five species of CCA. Nonliving settlement substrata on coral reefs is sparse; consequently the fact that only a few CCA species (notably T. prototypum) facilitate coral recruitment, has important implications for structuring the reef ecosystem.

Water quality as a regional driver of coral biodiversity and macroalgae on the Great Barrier Reef

Degradation of inshore coral reefs due to poor water quality is a major issue, yet it has proved difficult to demonstrate this linkage at other than local scales. This study modeled the relationships between large-scale data on water clarity and chlorophyll and four measures of reef status along the whole Great Barrier Reef, Australia (GBR; 12-24 degrees S). Four biotic groups with different trophic requirements, namely, the cover of macroalgae and the taxonomic richness of hard corals and phototrophic and heterotrophic octocorals, were predicted from water quality and spatial location. Water clarity and chlorophyll showed strong spatial patterns, with water clarity increasing more than threefold from inshore to offshore waters and chlorophyll decreasing approximately twofold from inshore to offshore and approximately twofold from south to north. Richness of hard corals and phototrophic octocorals declined with increasing turbidity and chlorophyll, whereas macroalgae and the richness of heterotrophic octocorals increased. Macroalgal cover experienced the largest water quality effects, increasing fivefold with decreasing water clarity and 1.4-fold with increasing chlorophyll. For each of the four biota, -45% of variation was predictable, with water quality effects accounting for 18-46% of that variation and spatial effects accounting for the remainder. Effects were consistent with the trophic requirements of the biota, suggesting that both macroalgal cover and coral biodiversity are partially controlled by energy supply limitation. Throughout the GBR, mean annual values of >10 m Secchi disk depth (a measure of water clarity) and < 0.45 g/L chlorophyll were associated with low macroalgal cover and high coral richness, indicating these values to be potentially useful water quality guidelines. The models predict that on the 22.8% of GBR reefs where guideline values are currently exceeded, water quality improvement, e.g., by minimizing agricultural runoff, should reduce macroalgal cover on average by 39% and increase the richness of hard corals and phototrophic octocorals on average by 16% and 33%, respectively (all else being equal). Such guidelines may help focus efforts to implement effective pollution reduction and integrated coastal management policies for the GBR and other Indo-Pacific coral reefs.

Photophysiological stress in scleractinian corals in response to short-term sedimentation

Effects of short-term sedimentation on common coastal coral species were investigated in laboratory and field experiments on the Great Barrier Reef (GBR) using pulse-amplitude modulated (PAM) chlorophyll fluorometry. In the laboratory, changes in maximal quantum yields of photosystem II (Fv/Fm) in Montipora peltiformis were examined in response to the amount of sedimentation (79–234 mg cm−2) and duration of exposure (0–36 h). In control colonies, Fv/Fm ranged from 0.67 to 0.71, and did not show any temporal trend, while maximum yields of sediment-covered fragments declined steadily and reached levels below 0.1 in most colonies after 36 h coverage. Maximal quantum yield in M. peltiformis declined linearly in relation to both the amount of sediment deposited per unit surface area and the duration of exposure. Zooxanthellae densities and chlorophyll concentrations per unit area of sediment-treated corals decreased in the same manner, however, their responses were not quite as strong as the changes in Fv/Fm. Within the ranges measured, sedimentation stress of colonies exposed to large amounts of sediment for short periods of time was similar to that exposed to low amounts of sediments for prolonged periods of time. Colonies were recovered from short-term, or low-level, sedimentation within <36 h, whereas long-term exposure, or high levels of sedimentation, killed exposed colony parts. Field experiments comparing susceptibilities of common coastal coral species towards sedimentation showed significant reductions in effective quantum yields (ΔF/Fm′) in 9 out of 12 common coastal species after 22 h of exposure. Three out of twelve investigated species were not affected by the experimental application of sediments (Galaxea fascicularis, Fungia crassa, and Pectinia lactuca). Our results suggest that anthropogenic sediment deposition can negatively affect the photosynthetic activity of zooxanthellae and thus the viability of corals. However, the results also showed the ability of corals to compartmentalise sedimentation stress, as the photosynthetic activity only from tissues directly underneath the sediment declined, whereas that of adjacent clean tissues did not change measurably.

IDENTIFYING ECOLOGICAL CHANGE AND ITS CAUSES: A CASE STUDY ON CORAL REEFS

The successful management of ecosystems depends on early detection of change and identification of factors causing such change. Determination of change and causality in ecosystems is difficult, both philosophically and practically, and these difficulties increase with the scale and complexity of ecosystems. Management also depends on the communication of scientific results to the broader public, and this can fail if the evidence of change and causality is not synthesized in a transparent manner. We developed a framework to address these problems when assessing the effects of agricultural runoff on coral reefs of the Australian Great Barrier Reef (GBR). The framework is based on improved methods of statistical estimation (rejecting the use of statistical tests to detect change), and the use of epidemiological causal criteria that are both scientifically rigorous and understood by nonspecialists. Many inshore reefs of the GBR are exposed to terrestrial runoff from agriculture. However, detecting change and ...

The other ocean acidification problem: CO2 as a resource among competitors for ecosystem dominance

Predictions concerning the consequences of the oceanic uptake of increasing atmospheric carbon dioxide (CO2) have been primarily occupied with the effects of ocean acidification on calcifying organisms, particularly those critical to the formation of habitats (e.g. coral reefs) or their maintenance (e.g. grazing echinoderms). This focus overlooks direct and indirect effects of CO2 on non-calcareous taxa that play critical roles in ecosystem shifts (e.g. competitors). We present the model that future atmospheric [CO2] may act as a resource for mat-forming algae, a diverse and widespread group known to reduce the resilience of kelp forests and coral reefs. We test this hypothesis by combining laboratory and field CO2 experiments and data from ‘natural’ volcanic CO2 vents. We show that mats have enhanced productivity in experiments and more expansive covers in situ under projected near-future CO2 conditions both in temperate and tropical conditions. The benefits of CO2 are likely to vary among species of producers, potentially leading to shifts in species dominance in a high CO2 world. We explore how ocean acidification combines with other environmental changes across a number of scales, and raise awareness of CO2 as a resource whose change in availability could have wide-ranging community consequences beyond its direct effects.

Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities

The ecological effects of ocean acidification (OA) from rising atmospheric carbon dioxide (CO2) on benthic marine communities are largely unknown. We investigated in situ the consequences of long-term exposure to high CO2 on coral-reef-associated macroinvertebrate communities around three shallow volcanic CO2 seeps in Papua New Guinea. The densities of many groups and the number of taxa (classes and phyla) of macroinvertebrates were significantly reduced at elevated CO2 (425–1100 µatm) compared with control sites. However, sensitivities of some groups, including decapod crustaceans, ascidians and several echinoderms, contrasted with predictions of their physiological CO2 tolerances derived from laboratory experiments. High CO2 reduced the availability of structurally complex corals that are essential refugia for many reef-associated macroinvertebrates. This loss of habitat complexity was also associated with losses in many macroinvertebrate groups, especially predation-prone mobile taxa, including crustaceans and crinoids. The transition from living to dead coral as substratum and habitat further altered macroinvertebrate communities, with far more taxa losing than gaining in numbers. Our study shows that indirect ecological effects of OA (reduced habitat complexity) will complement its direct physiological effects and together with the loss of coral cover through climate change will severely affect macroinvertebrate communities in coral reefs.