Life histories predict coral community disassembly under multiple stressors

Climate change is reshaping biological communities against a background of existing human pressure. Evaluating the impacts of multiple stressors on community dynamics can be particularly challenging in species‐rich ecosystems, such as coral reefs. Here, we investigate whether life‐history strategies and cotolerance to different stressors can predict community responses to fishing and temperature‐driven bleaching using a 20‐year time series of coral assemblages in Kenya. We found that the initial life‐history composition of coral taxa largely determined the impacts of bleaching and coral loss. Prior to the 1998 bleaching event, coral assemblages within no‐take marine reserves were composed of three distinct life histories – competitive, stress‐tolerant and weedy– and exhibited strong declines following bleaching with limited subsequent recovery. In contrast, fished reefs had lower coral cover, fewer genera and were composed of stress‐tolerant and weedy corals that were less affected by bleaching over the long term. Despite these general patterns, we found limited evidence for cotolerance as coral genera and life histories were variable in their sensitivities to fishing and bleaching. Overall, fishing and bleaching have reduced coral diversity and led to altered coral communities of ‘survivor’ species with stress‐tolerant and weedy life histories. Our findings are consistent with expectations that climate change interacting with existing human pressure will result in the loss of coral diversity and critical reef habitat.     

Mechanical vulnerability explains size‐dependent mortality of reef corals

Understanding life history and demographic variation among species within communities is a central ecological goal. Mortality schedules are especially important in ecosystems where disturbance plays a major role in structuring communities, such as coral reefs. Here, we test whether a trait‐based, mechanistic model of mechanical vulnerability in corals can explain mortality schedules. Specifically, we ask whether species that become increasingly vulnerable to hydrodynamic dislodgment as they grow have bathtub‐shaped mortality curves, whereas species that remain mechanically stable have decreasing mortality rates with size, as predicted by classical life history theory for reef corals. We find that size‐dependent mortality is highly consistent between species with the same growth form and that the shape of size‐dependent mortality for each growth form can be explained by mechanical vulnerability. Our findings highlight the feasibility of predicting assemblage‐scale mortality patterns on coral reefs with trait‐based approaches.     

The transformation of Caribbean coral communities since humans

The mass die‐off of Caribbean corals has transformed many of this region’s reefs to macroalgal‐dominated habitats since systematic monitoring began in the 1970s. Although attributed to a combination of local and global human stressors, the lack of long‐term data on Caribbean reef coral communities has prevented a clear understanding of the causes and consequences of coral declines. We integrated paleoecological, historical, and modern survey data to track the occurrence of major coral species and life‐history groups throughout the Caribbean from the prehuman period to the present. The regional loss of Acropora corals beginning by the 1960s from local human disturbances resulted in increases in the occurrence of formerly subdominant stress‐tolerant and weedy scleractinian corals and the competitive hydrozoan Millepora beginning in the 1970s and 1980s. These transformations have resulted in the homogenization of coral communities within individual countries. However, increases in stress‐tolerant and weedy corals have slowed or reversed since the 1980s and 1990s in tandem with intensified coral bleaching and disease. These patterns reveal the long history of increasingly stressful environmental conditions on Caribbean reefs that began with widespread local human disturbances and have recently culminated in the combined effects of local and global change.     

Ontogenetic shifts in the habitat associations of butterflyfishes (F. Chaetodontidae)

The habitat associations of species are vital in determining an organism’s vulnerability to environmental and anthropogenic stress. In the marine environment, post-settlement processes such as ontogenetic shifts in habitat use can affect this vulnerability by subjecting a species to differing biological and environmental conditions at various life stages. This study documents the habitat associations of adult and juvenile butterflyfishes on an inshore reef of the Great Barrier Reef (GBR) to investigate if ontogenetic shifts in habitat use occur, and if such shifts relate to the trophic ecologies of species. Coral-feeding species displayed highly concordant distributions among adults and juveniles. In contrast, adults and juveniles of species with wider dietary selectivities (generalists) displayed significantly different distributions across reef zones. Juvenile generalist feeders were limited to the shallow, patchy areas of the reef flat whilst adult conspecifics displayed comparatively wide distributions. Butterflyfishes with a heavy reliance on corals for food appear to settle preferentially in areas with high abundances of adult conspecifics, which may partially explain why coral specialists are more vulnerable to localized depletion events. In contrast, generalist species utilize distinct habitats as adults and juveniles, suggesting that generalist butterflyfishes expand their ranges and are therefore subjected to changing environmental conditions as they reach adulthood.     

Environmental,spatial and phylogenetic determinants of fish life‐history traits and functional composition of Australian rivers

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Correlated evolution of life history and host range in the nonphotosynthetic parasitic flowering plants Orobanche and Phelipanche (Orobanchaceae)

Most members of the nonphotosynthetic parasitic genera Orobanche and Phelipanche (Orobanchaceae) have narrow host ranges, and, as they grow on perennial hosts, are (at least potentially) perennial themselves. A few species, however, have wide host ranges and grow on annual hosts, and are thus (at least facultatively) annuals themselves. Among the latter are the weedy species, which include economically important pest taxa such as Orobanche crenata or Phelipanche aegyptiaca. Using a phylogenetically based maximum likelihood approach, which takes phylogenetic and branch length uncertainty into account, we can show that the life trait host range and life history evolve in a correlated fashion. This supports the hypothesis that parasite specialization is associated with predictable resources (i.e. long-lived hosts) and generalism with unpredictable ones (i.e. short-lived hosts), a pattern often found in animal parasites. The mechanisms and temporal sequence of the life trait changes and their interrelations remain speculative.     

Density‐dependent survival varies with species life‐history strategy in a tropical forest

Species coexistence in diverse communities likely results from multiple interacting factors. Mechanisms such as conspecific negative density dependence (CNDD) and varying life‐history strategies related to resource partitioning are known to influence plant fitness, and thereby community composition and diversity. However, we have little understanding of how these mechanisms interact and how they vary across life stages. Here, we document the interaction between CNDD and life‐history strategy, based on growth‐mortality trade‐offs, from seedling to adult tree for 47 species in a tropical forest. Species’ life‐history strategies remained consistent across stages: fast‐growing species had higher mortality than slow‐growing species at all stages. In contrast, mean CNDD was strongest at early life stages (i.e. seedling, sapling). Fast‐growing species tended to suffer greater CNDD than slow‐growing species at several, but not all life stages. Overall, our results demonstrate that coexistence mechanisms interact across multiple life stages to shape diverse tree communities.     

Does localized control of invasive eastern gambusia (Poeciliidae: Gambusia holbrooki) increase population growth of generalist wetland fishes?

While invasive fish management is heavily focussed on containment measures when introductions occur, examples from invasive species management in terrestrial systems suggest that there may also be considerable conservation benefits in implementing localized control programmes. We conducted a field‐based experiment to assess the effectiveness of removing a globally significant invasive fish, eastern gambusia Gambusia holbrooki, from natural wetland habitats of south‐eastern Australia. With recent work suggesting the impacts of eastern gambusia may be minimal for species with generalist life‐history strategies, we hypothesized that the removal of eastern gambusia will reduce localized population growth of the invasive species, but will have little influence on the population growth of more generalist sympatric wetland fish species. We used a predictive modelling approach to investigate changes in eastern gambusia populations following removal activities, and how sympatric fish species responded to such changes. Although eastern gambusia rapidly populated habitats, we demonstrated that control actions substantially reduced the rate of population increase over the four‐month study period. This suggests that control may be an effective localized strategy to suppress eastern gambusia densities. There was however, no evidence of any response to the removal actions by any of the three sympatric fish species investigated – carp gudgeon (Hypseleotris spp.), Australian smelt (Retropinna semoni) and the invasive common carp (Cyprinus carpio). These results support previous work which suggests that the flexible life‐history strategies and behavioural traits of all three species allow co‐existence with eastern gambusia. The study highlights the importance of understanding the potential outcomes of control options which is particularly pertinent for established aquatic invasive species where information on control effectiveness, population dynamics and/or ecosystem response is currently lacking.     

Using Agent-Based Models to Aid Reef Restoration: Enhancing Coral Cover and Topographic Complexity through the Spatial Arrangement of Coral Transplants

High coral cover and topographic complexity are favorable qualities of a healthy coral reef. Because coral reef restoration is expensive and coral growth is naturally slow, there is a need to strategically arrange coral transplants to maximize coral cover and topographic complexity. Similarly, it is important to understand how differences in the life history characteristics of coral transplants can influence changes in the structural attributes of coral reefs. This study utilizes agent‐based computer modeling to explore the different spatial scenarios of coral transplantation using corals with contrasting r‐ and K‐selected life histories. Spatial indexes are used to compare coral cover and topographic complexity at incremental time scales, within which disturbance events are of minor importance in spatial structuring. The outcomes of the model suggest that even‐spaced grided transplanting arrangements provide the fastest increase in coral cover and three‐dimensional habitat space (topographic complexity) across large temporal scales (<30 years) for corals with r‐selected life history strategies.     

Phylogenetic effects on functional traits and life history strategies of Australian freshwater fish

Understanding the biogeographic and phylogenetic basis to interspecific differences in species’ functional traits is a central goal of evolutionary biology and community ecology. We quantify the extent of phylogenetic influence on functional traits and life‐history strategies of Australian freshwater fish to highlight intercontinental differences as a result of Australia's unique biogeographic and evolutionary history. We assembled data on life history, morphological and ecological traits from published sources for 194 Australian freshwater species. Interspecific variation among species could be described by a specialist–generalist gradient of variation in life‐history strategies associated with spawning frequency, fecundity and spawning migration. In general, Australian fish showed an affinity for life‐history strategies that maximise fitness in hydrologically unpredictable environments. We also observed differences in trait lability between and within life history, morphological and ecological traits where in general morphological and ecological traits were more labile. Our results showed that life‐history strategies are relatively evolutionarily labile and species have potentially evolved or colonised in freshwaters frequently and independently allowing them to maximise population performance in a range of environments. In addition, reproductive guild membership showed strong phylogenetic constraint indicating that evolutionary history is an important component influencing the range and distribution of reproductive strategies in extant species assemblages. For Australian freshwater fish, biogeographic and phylogenetic history contribute to broad taxonomic differences in species functional traits, while finer scale ecological processes contribute to interspecific differences in smaller taxonomic units. These results suggest that the lability or phylogenetic relatedness of different functional traits affects their suitability for testing hypothesis surrounding community level responses to environmental change.     

A unified framework for diversity gradients: the adaptive trait continuum

Aim Adaptive trait continua are axes of covariation observed in multivariate trait data for a given taxonomic group. These continua quantify and summarize life‐history variation at the inter‐specific level in multi‐specific assemblages. Here we examine whether trait continua can provide a useful framework to link life‐history variation with demographic and evolutionary processes in species richness gradients. Taking an altitudinal species richness gradient for Mediterranean butterflies as a study case, we examined a suite of traits (larval diet breadth, adult phenology, dispersal capacity and wing length) and species‐specific habitat measures (temperature and aridity breadth). We tested whether traits and species‐specific habitat measures tend to co‐vary, whether they are phylogenetically conserved, and whether they are able to explain species distributions and spatial genetic variation in a large number of butterfly assemblages. Location Catalonia, Spain. Methods We formulated predictions associated with species richness gradients and adaptive trait continua. We applied principal components analyses (PCAs), structural equation modelling and phylogenetic generalized least squares models. Results We found that traits and species‐specific habitat measures covaried along a main PCA axis, ranging from multivoltine trophic generalists with high dispersal capacity to univoltine (i.e. one generation per year), trophic specialist species with low dispersal capacity. This trait continuum was closely associated with the observed distributions along the altitudinal gradient and predicted inter‐specific differences in patterns of spatial genetic variability (F_ST and genetic distances), population responses to the impacts of global change and local turnover dynamics. Main conclusions The adaptive trait continuum of Mediterranean butterflies provides an integrative and mechanistic framework to: (1) analyse geographical gradients in species richness, (2) explain inter‐specific differences in population abundances, spatial distributions and demographic trends, (3) explain inter‐specific differences in patterns of genetic variation (F_ST and genetic distances), and (4) study specialist–generalist life‐history transitions frequently involved in butterfly diversification processes.     

Life-history strategies in freshwater macroinvertebrates

• 1 Explaining spatial and temporal differences in species assemblages is a central aim of ecology. It requires a sound understanding of the causal mechanisms underlying the relationship of species with their environment. A species trait is widely acknowledged to be the key that links pattern and process, although the enormous variety of traits hampers generalization about which combination of traits are adaptive in a particular environment.
• 2 In three steps, we used species traits to match species and environment, and chose lentic freshwater ecosystems to illustrate our approach. We first identified key environmental factors and selected the species traits that enable the organism to deal with them. Secondly, we investigated how investments in these traits are related (e.g. through trade‐offs). Thirdly, we outlined 13 life‐history strategies, based on biological species traits, their interrelations known from life‐history theory and their functional implications.
• 3 Species traits and environmental conditions are connected through life‐history strategies, with different strategies representing different solutions to particular ecological problems. In addition, strategies may present an integrated response to the environment as they are based on many different traits and their interrelationships. The presence and abundance of (species exhibiting) different life‐history strategies in a location may therefore give direct information about how a particular environment is experienced by the species present.
• 4 Life‐history strategies can be used to (i) explain differences in species assemblages either between locations or in different periods; (ii) compare waterbodies separated by large geographical distances, which may comprise different regional species pools or span species distribution areas and (iii) reduce often very complex, biodiverse assemblages into a few meaningful, easily interpretable relationships.

     

Towards an interactive,process‐based approach to understanding range shifts: developmental and environmental dependencies matter

Many species are undergoing distributional shifts in response to climate change. However, wide variability in range shifting rates has been observed across taxa, and even among closely‐related species. Attempts to link climate‐mediated range shifts to traits has often produced weak or conflicting results. Here we investigate interactive effects of developmental processes and environmental stress on the expression of traits relevant to range shifts. We use an individual‐based modelling approach to assess how different developmental strategies affect range shift rates under a range of environmental conditions. We find that under stressful conditions, such as at the margins of the species’ fundamental niche, investment in prolonged development leads to the greatest rates of range shifting, especially when longer time in development leads to improved fecundity and dispersal‐related traits. However, under benign conditions, and when traits are less developmentally plastic, shorter development times are preferred for rapid range shifts, because higher generational frequency increases the number of individual dispersal events occurring over time. Our results suggest that the ability of a species to range shift depends not only on their dispersal and colonisation characteristics but also how these characteristics interact with developmental strategies. Benefits of any trait always depended on the environmental and developmental sensitivity of life history trait combinations, and the environmental conditions under which the range shift takes place. Without considering environmental and developmental sources of variation in the expression of traits relevant to range shifts, there is little hope of developing a general understanding of intrinsic drivers of range shift potential.     

Dietary generalism accelerates arrival and persistence of coral‐reef fishes in their novel ranges under climate change

Climate change is redistributing marine and terrestrial species globally. Life‐history traits mediate the ability of species to cope with novel environmental conditions, and can be used to gauge the potential redistribution of taxa facing the challenges of a changing climate. However, it is unclear whether the same traits are important across different stages of range shifts (arrival, population increase, persistence). To test which life‐history traits most mediate the process of range extension, we used a 16‐year dataset of 35 range‐extending coral‐reef fish species and quantified the importance of various traits on the arrival time (earliness) and degree of persistence (prevalence and patchiness) at higher latitudes. We show that traits predisposing species to shift their range more rapidly (large body size, broad latitudinal range, long dispersal duration) did not drive the early stages of redistribution. Instead, we found that as diet breadth increased, the initial arrival and establishment (prevalence and patchiness) of climate migrant species in temperate locations occurred earlier. While the initial incursion of range‐shifting species depends on traits associated with dispersal potential, subsequent establishment hinges more on a species’ ability to exploit novel food resources locally. These results highlight that generalist species that can best adapt to novel food sources might be most successful in a future ocean.     

SYMBIODINIUM (DINOPHYTA) DIVERSITY AND STABILITY IN AQUARIUM CORALS1

Indo‐Pacific reef corals growing for years in closed‐system aquaria provide an alternate means to investigate host–symbiont specificity and stability. The diversity of dinoflagellate endosymbionts (Symbiodinium spp.) from coral communities in private and public aquaria was investigated using molecular‐genetic analyses. Of the 29 symbiont types (i.e., species) identified, 90% belonged to the most prevalent group of Symbiodinium harbored by Indo‐Pacific reef corals, Clade C, while the rest belonged to Clade D. Sixty‐five percent of all types were known from field surveys conducted throughout the Pacific and Indian oceans. Because specific coral–dinoflagellate partnerships appear to have defined geographic distributions, correspondence of the same symbionts in aquarium and field‐collected specimens identifies regions where particular colonies must have been collected in the wild. Symbiodinium spp. in clade D, believed to be “stress‐tolerant” and/or “opportunistic,” occurred in a limited number of individual colonies. The absence of a prevalent, or “weedy,” symbiont suggests that conditions under which aquarium corals are grown do not favor competitive replacements of their native symbiont populations. The finding of typical and diverse assemblages of Symbiodinium spp. among aquarium corals living many years under variable chemical/physical conditions, artificial and natural light, while undergoing fragmentation periodically, indicates that individual colonies maintain stable, long‐term symbiotic associations.     

An invasive species imposes selection on life‐history traits of a native frog

As well as their direct ecological impacts on native taxa, invasive species can impose selection on phenotypic attributes (morphology, physiology, behaviour, etc.) of the native fauna. In anurans, body size at metamorphosis is a critical life‐history trait: for most challenges faced by post‐metamorphic anurans, larger size at metamorphosis probably enhances survival. However, our studies on Australian frogs (Limnodynastes convexiusculus) show that this pattern can be reversed by the arrival of an invasive species. When metamorph frogs first encounter invasive cane toads (Bufo marinus), they try to eat the toxic invader and, if they are able to do so, are likely to die from poisoning. Because frogs are gape‐limited predators, small metamorphs cannot ingest a toad and thus survive long enough to disperse away from the natal pond (and thus from potentially deadly toads). These data show that larger size at metamorphosis can reduce rather than increase anuran survival rates, because larger metamorphs are more easily able to ingest (and thus be poisoned by) metamorph cane toads. Our results suggest that patterns of selection on life‐history traits of native taxa (such as size and age at metamorphosis, seasonal timing of breeding and duration of pondside aggregation prior to dispersal) can be modified by the arrival of an invasive species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 329–336.     

Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana

Intraspecific trait variation is caused by genetic and plastic responses to environment. This intraspecific diversity is captured in immense natural history collections, giving us a window into trait variation across continents and through centuries of environmental shifts. Here we tested if hypotheses based on life history and the leaf economics spectrum explain intraspecific trait changes across global spatiotemporal environmental gradients. We measured phenotypes on a 216‐year time series of Arabidopsis thaliana accessions from across its native range and applied spatially varying coefficient models to quantify region‐specific trends in trait coordination and trait responses to climate gradients. All traits exhibited significant change across space or through time. For example, δ¹⁵N decreased over time across much of the range and leaf C:N increased, consistent with predictions based on anthropogenic changes in land use and atmosphere. Plants were collected later in the growing season in more recent years in many regions, possibly because populations shifted toward more spring germination and summer flowering as opposed to fall germination and spring flowering. When climate variables were considered, collection dates were earlier in warmer years, while summer rainfall had opposing associations with collection date depending on regions. There was only a modest correlation among traits, indicating a lack of a single life history/physiology axis. Nevertheless, leaf C:N was low for summer‐ versus spring‐collected plants, consistent with a life history–physiology axis from slow‐growing winter annuals to fast‐growing spring/summer annuals. Regional heterogeneity in phenotype trends indicates complex responses to spatiotemporal environmental gradients potentially due to geographic genetic variation and climate interactions with other aspects of environment. Our study demonstrates how natural history collections can be used to broadly characterize trait responses to environment, revealing heterogeneity in response to anthropogenic change.     

Symbiodinium population genetics: testing for species boundaries and analysing samples with mixed genotypes

Population genetic markers are increasingly being used to study the diversity, ecology and evolution of Symbiodinium, a group of eukaryotic microbes that are often mutualistic with reef‐building corals. Population genetic markers can resolve individual clones, or strains, from samples of host tissue; however, samples may comprise different species that may confound interpretations of gene flow and genetic structure. Here, we propose a method for resolving species from population genetic data using tests for genetic recombination. Assigning individuals to genetically recombining populations prior to further analyses avoids critical errors in the interpretation of gene flow and dispersal. To demonstrate the effectiveness of the approach, we first apply this method to a simulated data set. We then use the method to resolve two species of host generalist Symbiodinium that commonly co‐occur in reef‐building corals collected from Indo‐West Pacific reefs. We demonstrate that the method is robust even when some hosts contain genotypes from two distinct species. Finally, we examine population genetic data sets from two recently published papers in Molecular Ecology. We show that each strongly supports a two species interpretation, which significantly changes the original conclusions presented in these studies. When combined with available phylogenetic and ecological evidence, the use of population genetic data offers a robust method for unambiguously delimiting morphologically cryptic species.     

Generalists are the most urban‐tolerant of birds: a phylogenetically controlled analysis of ecological and life history traits using a novel continuous measure of bird responses to urbanization

Identifying which ecological and life history traits influence a species’ tolerance to urbanization is critical to understanding the trajectory of biodiversity in an increasingly urbanizing world. There is evidence for a wide array of contrasting patterns for single trait associations with urbanization. In a continental‐scale analysis, incorporating 477 species and >5 000 000 bird observations, we developed a novel and scalable methodology that evaluated the ecological and life history traits which most influence a species’ adaptability to persist in urban environments. Specifically, we assigned species‐specific scores based on continuous measures of response to urbanization, using VIIRS night‐time light values (i.e. radiance) as a proxy for urbanization. We identified generalized, phylogenetically controlled patterns: bird species which are generalists (i.e. large niche breadth), with large clutch size, and large residual brain size are among the most urban‐tolerant bird species. Conversely, specialized feeding strategies (i.e. insectivores and granivores) were negatively associated with urbanization. Enhancement and persistence of avian biodiversity in urban environments probably relies on protecting, maintaining and restoring diverse habitats serving a range of life history strategies.     

Developing environmental flow recommendations for freshwater mussels using the biological traits of species guilds

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