Disturbance-Induced Changes in Population Size Structure Promote Coral Biodiversity.

AbstractReef-building coral assemblages are typically species rich, yet the processes maintaining high biodiversity remain poorly understood. Disturbance has long been thought to promote coral species coexistence by reducing the strength of competition (i.e., the intermediate disturbance hypothesis [IDH]). However, such disturbance-induced effects are insufficient to inhibit competitive exclusion. Nevertheless, there are other mechanisms by which disturbance and, more generally, environmental variation can favor coexistence. Here, we develop a size-structured, stochastic coral competition model calibrated with field data from two common colony morphologies to investigate the effects of hydrodynamic disturbance on community dynamics. We show that fluctuations in wave action can promote coral species coexistence but that this occurs via interspecific differences in size-dependent mortality rather than solely via stochastic fluctuations in competition (i.e., free space availability). While this mechanism differs from that originally envisioned in the IDH, it is nonetheless a mechanism by which intermediate levels of disturbance do promote coexistence. Given the sensitivity of coexistence to disturbance frequency and intensity, anthropogenic changes in disturbance regimes are likely to affect coral assemblages in ways that are not predictable from single-population models.

Widespread shifts in body size within populations and assemblages.

Biotic responses to global change include directional shifts in organismal traits. Body size, an integrative trait that determines demographic rates and ecosystem functions, is thought to be shrinking in the Anthropocene. Here, we assessed the prevalence of body size change in six taxon groups across 5025 assemblage time series spanning 1960 to 2020. Using the Price equation to partition this change into within-species body size versus compositional changes, we detected prevailing decreases in body size through time driven primarily by fish, with more variable patterns in other taxa. We found that change in assemblage composition contributes more to body size changes than within-species trends, but both components show substantial variation in magnitude and direction. The biomass of assemblages remains quite stable as decreases in body size trade off with increases in abundance.

Six years of demography data for 11 reef coral species.

Scleractinian corals are colonial animals with a range of life-history strategies, making up diverse species assemblages that define coral reefs. We tagged and tracked ~30 colonies from each of 11 species during seven trips spanning 6 years (2009-2015) to measure their vital rates and competitive interactions on the reef crest at Trimodal Reef, Lizard Island, Australia. Pairs of species were chosen from five growth forms in which one species of the pair was locally rare (R) and the other common (C). The sampled growth forms were massive (Goniastrea pectinata [R] and G. retiformis [C]), digitate (Acropora humilis [R] and A. cf. digitifera [C]), corymbose (A. millepora [R] and A. nasuta [C]), tabular (A. cytherea [R] and A. hyacinthus [C]) and arborescent (A. robusta [R] and A. intermedia [C]). An extra corymbose species with intermediate abundance, A. spathulata was included when it became apparent that A. millepora was too rare on the reef crest, making the 11 species in total. The tagged colonies were visited each year in the weeks prior to spawning. During visits, two or more observers each took two or three photographs of each tagged colony from directly above and on the horizontal plane with a scale plate to track planar area. Dead or missing colonies were recorded and new colonies tagged to maintain ~30 colonies per species throughout the 6 years of the study. In addition to tracking tagged corals, 30 fragments were collected from neighboring untagged colonies of each species for counting numbers of eggs per polyp (fecundity); and fragments of untagged colonies were brought into the laboratory where spawned eggs were collected for biomass and energy measurements. We also conducted surveys at the study site to generate size structure data for each species in several of the years. Each tagged colony photograph was digitized by at least two people. Therefore, we could examine sources of error in planar area for both photographers and outliners. Competitive interactions were recorded for a subset of species by measuring the margins of tagged colony outlines interacting with neighboring corals. The study was abruptly ended by Tropical Cyclone Nathan (Category 4) that killed all but nine of the more than 300 tagged colonies in early 2015. Nonetheless, these data will be of use to other researchers interested in coral demography and coexistence, functional ecology, and parametrizing population, community, and ecosystem models. The data set is not copyright restricted, and users should cite this paper when using the data.

A word on habitat complexity.

In their recent synopsis, Loke and Chisholm (Ecology Letters, 25, 2269-2288, 2022) present an overview of habitat complexity metrics for ecologists. They provide a review and some sound advice. However, we found several of their analyses and opinions misleading. This technical note provides a different perspective on the complexity metrics assessed.

Net effects of life-history traits explain persistent differences in abundance among similar species.

Life-history traits are promising tools to predict species commonness and rarity because they influence a population's fitness in a given environment. Yet, species with similar traits can have vastly different abundances, challenging the prospect of robust trait-based predictions. Using long-term demographic monitoring, we show that coral populations with similar morphological and life-history traits show persistent (decade-long) differences in abundance. Morphological groups predicted species positions along two, well known life-history axes (the fast-slow continuum and size-specific fecundity). However, integral projection models revealed that density-independent population growth (λ) was more variable within morphological groups, and was consistently higher in dominant species relative to rare species. Within-group λ differences projected large abundance differences among similar species in short timeframes, and were generated by small but compounding variation in growth, survival, and reproduction. Our study shows that easily measured morphological traits predict demographic strategies, yet small life-history differences can accumulate into large differences in λ and abundance among similar species. Quantifying the net effects of multiple traits on population dynamics is therefore essential to anticipate species commonness and rarity.

Intraspecific variation reshapes coral assemblages under elevated temperature and acidity.

Insights into assemblages that can persist in extreme environments are still emerging. Ocean warming and acidification select against species with low physiological tolerance (trait-based 'filtering'). However, intraspecific trait variation can promote species adaptation and persistence, with potentially large effects on assemblage structure. By sampling nine coral traits (four morphological, four tissue and one skeletal) along an offshore-inshore gradient in temperature and pH, we show that distantly related coral species undergo consistent intraspecific changes as they cross into warm, acidic environments. Intraspecific variation and species turnover each favoured colonies with greater tissue biomass, higher symbiont densities and reduced skeletal investments, indicating strong filtering on colony physiology within and across species. Physiological tissue traits were highly variable within species and were independent of morphology, enabling morphologically diverse species to cross into sites of elevated temperature and acidity. Widespread intraspecific change can therefore counter the loss of biodiversity and morphological structure across a steep environmental gradient.

AnimalTraits - a curated animal trait database for body mass, metabolic rate and brain size.

Trait databases have become important resources for large-scale comparative studies in ecology and evolution. Here we introduce the AnimalTraits database, a curated database of body mass, metabolic rate and brain size, in standardised units, for terrestrial animals. The database has broad taxonomic breadth, including tetrapods, arthropods, molluscs and annelids from almost 2000 species and 1000 genera. All data recorded in the database are sourced from their original empirical publication, and the original metrics and measurements are included with each record. This allows for subsequent data transformations as required. We have included rich metadata to allow users to filter the dataset. The additional R scripts we provide will assist researchers with aggregating standardised observations into species-level trait values. Our goals are to provide this resource without restrictions, to keep the AnimalTraits database current, and to grow the number of relevant traits in the future.

Coral-bleaching responses to climate change across biological scales.

The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral-bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral-reef processes, will not only rapidly advance coral-reef science but will also provide necessary information to guide decision-making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km2 ) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero.

Strategic traits of bacteria and archaea vary widely within substrate-use groups.

Quantitative traits such as maximum growth rate and cell radial diameter are one facet of ecological strategy variation across bacteria and archaea. Another facet is substrate-use pathways, such as iron reduction or methylotrophy. Here, we ask how these two facets intersect, using a large compilation of data for culturable species and examining seven quantitative traits (genome size, signal transduction protein count, histidine kinase count, growth temperature, temperature-adjusted maximum growth rate, cell radial diameter and 16S rRNA operon copy number). Overall, quantitative trait variation within groups of organisms possessing a particular substrate-use pathway was very broad, outweighing differences between substrate-use groups. Although some substrate-use groups had significantly different means for some quantitative traits, standard deviation of quantitative trait values within each substrate-use pathway mostly averaged between 1.6 and 1.8 times larger than standard deviation across group means. Most likely, this wide variation reflects ecological strategy: for example, fast maximum growth rate is likely to express an early successional or copiotrophic strategy, and maximum growth varies widely within most substrate-use pathways. In general, it appears that these quantitative traits express different and complementary information about ecological strategy, compared with substrate use.

Cell size, genome size, and maximum growth rate are near-independent dimensions of ecological variation across bacteria and archaea.

Among bacteria and archaea, maximum relative growth rate, cell diameter, and genome size are widely regarded as important influences on ecological strategy. Via the most extensive data compilation so far for these traits across all clades and habitats, we ask whether they are correlated and if so how. Overall, we found little correlation among them, indicating they should be considered as independent dimensions of ecological variation. Nor was correlation evident within particular habitat types. A weak nonlinearity (6% of variance) was found whereby high maximum growth rates (temperature-adjusted) tended to occur in the midrange of cell diameters. Species identified in the literature as oligotrophs or copiotrophs were clearly separated on the dimension of maximum growth rate, but not on the dimensions of genome size or cell diameter.

A Field Primer for Monitoring Benthic Ecosystems using Structure-from-Motion Photogrammetry.

Structure-from-motion (SfM) photogrammetry is a technique used to generate three-dimensional (3D) reconstructions from a sequence of two-dimensional (2D) images. SfM methods are becoming increasingly popular as a noninvasive way to monitor many systems, including anthropogenic and natural landscapes, geologic structures, and both terrestrial and aquatic ecosystems. Here, a detailed protocol is provided for collecting SfM imagery to generate 3D models of benthic habitats. Additionally, the cost, time efficiency, and output quality of employing a Digital Single Lens Reflex (DSLR) camera versus a less expensive action camera have been compared. A tradeoff between computational time and resolution was observed, with the DSLR camera producing models with more than twice the resolution, but taking approximately 1.4-times longer to produce than the action camera. This primer aims to provide a thorough description of the steps necessary to collect SfM data in benthic habitats for those who are unfamiliar with the technique as well as for those already using similar methods.

Trait dimensions in bacteria and archaea compared to vascular plants.

Bacteria and archaea have very different ecology compared to plants. One similarity, though, is that much discussion of their ecological strategies has invoked concepts such as oligotrophy or stress tolerance. For plants, so-called 'trait ecology'-strategy description reframed along measurable trait dimensions-has made global syntheses possible. Among widely measured trait dimensions for bacteria and archaea three main axes are evident. Maximum growth rate in association with rRNA operon copy number expresses a rate-yield trade-off that is analogous to the acquisitive-conservative spectrum in plants, though underpinned by different trade-offs. Genome size in association with signal transduction expresses versatility. Cell size has influence on diffusive uptake and on relative wall costs. These trait dimensions, and potentially others, offer promise for interpreting ecology. At the same time, there are very substantial differences from plant trait ecology. Traits and their underpinning trade-offs are different. Also, bacteria and archaea use a variety of different substrates. Bacterial strategies can be viewed both through the facet of substrate-use pathways, and also through the facet of quantitative traits such as maximum growth rate. Preliminary evidence shows the quantitative traits vary widely within substrate-use pathways. This indicates they convey information complementary to substrate use.

Climate change transforms the functional identity of Mediterranean coralligenous assemblages.

Quantifying changes in functional community structure driven by disturbance is critical to anticipate potential shifts in ecosystem functioning. However, how marine heatwaves (MHWs) affect the functional structure of temperate coral-dominated communities is poorly understood. Here, we used five long-term (> 10 years) records of Mediterranean coralligenous assemblages in a multi-taxa, trait-based analysis to investigate MHW-driven changes in functional structure. We show that, despite stability in functional richness (i.e. the range of species functional traits), MHW-impacted assemblages experienced long-term directional changes in functional identity (i.e. their dominant trait values). Declining traits included large sizes, long lifespans, arborescent morphologies, filter-feeding strategies or calcified skeletons. These traits, which were mostly supported by few sensitive and irreplaceable species from a single functional group (habitat-forming octocorals), disproportionally influence certain ecosystem functions (e.g. 3D-habitat provision). Hence, MHWs are leading to assemblages that are deficient in key functional traits, with likely consequences for the ecosystem functioning.

A geometric basis for surface habitat complexity and biodiversity.

Structurally complex habitats tend to contain more species and higher total abundances than simple habitats. This ecological paradigm is grounded in first principles: species richness scales with area, and surface area and niche density increase with three-dimensional complexity. Here we present a geometric basis for surface habitats that unifies ecosystems and spatial scales. The theory is framed by fundamental geometric constraints between three structure descriptors-surface height, rugosity and fractal dimension-and explains 98% of surface variation in a structurally complex test system: coral reefs. Then, we show how coral biodiversity metrics (species richness, total abundance and probability of interspecific encounter) vary over the theoretical structure descriptor plane, demonstrating the value of the theory for predicting the consequences of natural and human modifications of surface structure.

Latitude and protection affect decadal trends in reef trophic structure over a continental scale.

The relative roles of top-down (consumer-driven) and bottom-up (resource-driven) forcing in exploited marine ecosystems have been much debated. Examples from a variety of marine systems of exploitation-induced, top-down trophic forcing have led to a general view that human-induced predator perturbations can disrupt entire marine food webs, yet other studies that have found no such evidence provide a counterpoint. Though evidence continues to emerge, an unresolved debate exists regarding both the relative roles of top-down versus bottom-up forcing and the capacity of human exploitation to instigate top-down, community-level effects. Using time-series data for 104 reef communities spanning tropical to temperate Australia from 1992 to 2013, we aimed to quantify relationships among long-term trophic group population density trends, latitude, and exploitation status over a continental-scale biogeographic range. Specifically, we amalgamated two long-term monitoring databases of marine community dynamics to test for significant positive or negative trends in density of each of three key trophic levels (predators, herbivores, and algae) across the entire time series at each of the 104 locations. We found that trophic control tended toward bottom-up driven in tropical systems and top-down driven in temperate systems. Further, alternating long-term population trends across multiple trophic levels (a method of identifying trophic cascades), presumably due to top-down trophic forcing, occurred in roughly fifteen percent of locations where the prerequisite significant predator trends occurred. Such alternating trophic trends were significantly more likely to occur at locations with increasing predator densities over time. Within these locations, we found a marked latitudinal gradient in the prevalence of long-term, alternating trophic group trends, from rare in the tropics (<5% of cases) to relatively common in temperate areas (~45%). Lastly, the strongest trends in predator and algal density occurred in older no-take marine reserves; however, exploitation status did not affect the likelihood of alternating long-term trophic group trends occurring. Our data suggest that the type and degree of trophic forcing in this system are likely related to one or more covariates of latitude, and that ecosystem resiliency to top-down control does not universally vary in this system based on exploitation level.

A synthesis of bacterial and archaeal phenotypic trait data.

A synthesis of phenotypic and quantitative genomic traits is provided for bacteria and archaea, in the form of a scripted, reproducible workflow that standardizes and merges 26 sources. The resulting unified dataset covers 14 phenotypic traits, 5 quantitative genomic traits, and 4 environmental characteristics for approximately 170,000 strain-level and 15,000 species-aggregated records. It spans all habitats including soils, marine and fresh waters and sediments, host-associated and thermal. Trait data can find use in clarifying major dimensions of ecological strategy variation across species. They can also be used in conjunction with species and abundance sampling to characterize trait mixtures in communities and responses of traits along environmental gradients.

Publisher Correction: Open Science principles for accelerating trait-based science across the Tree of Life.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Open Science principles for accelerating trait-based science across the Tree of Life.

Synthesizing trait observations and knowledge across the Tree of Life remains a grand challenge for biodiversity science. Species traits are widely used in ecological and evolutionary science, and new data and methods have proliferated rapidly. Yet accessing and integrating disparate data sources remains a considerable challenge, slowing progress toward a global synthesis to integrate trait data across organisms. Trait science needs a vision for achieving global integration across all organisms. Here, we outline how the adoption of key Open Science principles-open data, open source and open methods-is transforming trait science, increasing transparency, democratizing access and accelerating global synthesis. To enhance widespread adoption of these principles, we introduce the Open Traits Network (OTN), a global, decentralized community welcoming all researchers and institutions pursuing the collaborative goal of standardizing and integrating trait data across organisms. We demonstrate how adherence to Open Science principles is key to the OTN community and outline five activities that can accelerate the synthesis of trait data across the Tree of Life, thereby facilitating rapid advances to address scientific inquiries and environmental issues. Lessons learned along the path to a global synthesis of trait data will provide a framework for addressing similarly complex data science and informatics challenges.

Partitioning colony size variation into growth and partial mortality.

Body size is a trait that broadly influences the demography and ecology of organisms. In unitary organisms, body size tends to increase with age. In modular organisms, body size can either increase or decrease with age, with size changes being the net difference between modules added through growth and modules lost through partial mortality. Rates of colony extension are independent of body size, but net growth is allometric, suggesting a significant role of size-dependent mortality. In this study, we develop a generalizable model of partitioned growth and partial mortality and apply it to data from 11 species of reef-building coral. We show that corals generally grow at constant radial increments that are size independent, and that partial mortality acts more strongly on small colonies. We also show a clear life-history trade-off between growth and partial mortality that is governed by growth form. This decomposition of net growth can provide mechanistic insights into the relative demographic effects of the intrinsic factors (e.g. acquisition of food and life-history strategy), which tend to affect growth, and extrinsic factors (e.g. physical damage, and predation), which tend to affect mortality.