Marine organisms are simultaneously exposed to anthropogenic stressors with likely interactive effects, including synergisms in which the combined effects of multiple stressors are greater than the sum of individual effects. Early life stages of marine organisms are potentially vulnerable to the stressors associated with global change, but identifying general patterns across studies, species and response variables is challenging. This review represents the first meta-analysis of multistressor studies to target early marine life stages (embryo to larvae), particularly between temperature, salinity and pH as these are the best studied. Knowledge gaps in research on multiple abiotic stressors and early life stages are also identified. The meta-analysis yielded several key results: (1) Synergistic interactions (65% of individual tests) are more common than additive (17%) or antagonistic (17%) interactions. (2) Larvae are generally more vulnerable than embryos to thermal and pH stress. (3) Survival is more likely than sublethal responses to be affected by thermal, salinity and pH stress. (4) Interaction types vary among stressors, ontogenetic stages and biological responses, but they are more consistent among phyla. (5) Ocean acidification is a greater stressor for calcifying than noncalcifying larvae. Despite being more ecologically realistic than single-factor studies, multifactorial studies may still oversimplify complex systems, and so meta-analyses of the data from them must be cautiously interpreted with regard to extrapolation to field conditions. Nonetheless, our results identify taxa with early life stages that may be particularly vulnerable (e.g. molluscs, echinoderms) or robust (e.g. arthropods, cnidarians) to abiotic stress. We provide a list of recommendations for future multiple stressor studies, particularly those focussed on early marine life stages.
Benthic marine invertebrates live in a multistressor world where stressor levels are, and will continue to be, exacerbated by global warming and increased atmospheric carbon dioxide. These changes are causing the oceans to warm, decrease in pH, become hypercapnic, and to become less saturated in carbonate minerals. These stressors have strong impacts on biological processes, but little is known about their combined effects on the development of marine invertebrates. Increasing temperature has a stimulatory effect on development, whereas hypercapnia can depress developmental processes. The pH, pCO2, and CaCO3 of seawater change simultaneously with temperature, challenging our ability to predict future outcomes for marine biota. The need to consider both warming and acidification is reflected in the recent increase in cross-factorial studies of the effects of these stressors on development of marine invertebrates. The outcomes and trends in these studies are synthesized here. Based on this compilation, significant additive or antagonistic effects of warming and acidification of the ocean are common (16 of 20 species studied), and synergistic negative effects also are reported. Fertilization can be robust to near-future warming and acidification, depending on the male-female mating pair. Although larvae and juveniles of some species tolerate near-future levels of warming and acidification (+2°C/pH 7.8), projected far-future conditions (ca. ≥4°C/ ≤pH 7.6) are widely deleterious, with a reduction in the size and survival of larvae. It appears that larvae that calcify are sensitive both to warming and acidification, whereas those that do not calcify are more sensitive to warming. Different sensitivities of life-history stages and species have implications for persistence and community function in a changing ocean. Some species are more resilient than others and may be potential "winners" in the climate-change stakes. As the ocean will change more gradually over coming decades than in "future shock" perturbation investigations, it is likely that some species, particularly those with short generation times, may be able to tolerate near-future oceanic change through acclimatization and/or adaption.
Climate change is threatening tropical reefs across the world, with most scientists agreeing that the current changes in climate conditions are occurring at a much faster rate than in the past and are potentially beyond the capacity of reefs to adapt and recover. Current research in tropical ecosystems focuses largely on corals and fishes, although other benthic marine invertebrates provide crucial services to reef systems, with roles in nutrient cycling, water quality regulation, and herbivory. We review available information on the effects of environmental conditions associated with climate change on noncoral tropical benthic invertebrates, including inferences from modern and fossil records. Increasing sea surface temperatures may decrease survivorship and increase the developmental rate, as well as alter the timing of gonad development, spawning, and food availability. The broad latitudinal distribution and associated temperature ranges of several pantropical taxa suggest that some reef communities may have an in-built adaptive capacity. Tropical benthic invertebrates will also show species-specific sublethal and lethal responses to sea-level rise, ocean acidification, physical disturbance, runoff, turbidity, sedimentation, and changes in ocean circulation. In order to accurately predict a species' response to these stressors, we must consider the magnitude and duration of exposure to each stressor, as well as the physiology, mobility, and habitat requirements of the species. Stressors will not act independently, and many organisms will be exposed to multiple stressors concurrently, including anthropogenic stressors. Environmental changes associated with climate change are linked to larger ecological processes, including changes in larval dispersal and recruitment success, shifts in community structure and range extensions, and the establishment and spread of invasive species. Loss of some species will trigger economic losses and negative effects on ecosystem function. Our review is intended to create a framework with which to predict the vulnerability of benthic invertebrates to the stressors associated with climate change, as well as their adaptive capacity. We anticipate that this review will assist scientists, managers, and policy-makers to better develop and implement regional research and management strategies, based on observed and predicted changes in environmental conditions.
Imagery collected by still and video cameras is an increasingly important tool for minimal impact, repeatable observations in the marine environment. Data generated from imagery includes identification, annotation and quantification of biological subjects and environmental features within an image. To be long-lived and useful beyond their project-specific initial purpose, and to maximize their utility across studies and disciplines, marine imagery data should use a standardised vocabulary of defined terms. This would enable the compilation of regional, national and/or global data sets from multiple sources, contributing to broad-scale management studies and development of automated annotation algorithms. The classification scheme developed under the Collaborative and Automated Tools for Analysis of Marine Imagery (CATAMI) project provides such a vocabulary. The CATAMI classification scheme introduces Australian-wide acknowledged, standardised terminology for annotating benthic substrates and biota in marine imagery. It combines coarse-level taxonomy and morphology, and is a flexible, hierarchical classification that bridges the gap between habitat/biotope characterisation and taxonomy, acknowledging limitations when describing biological taxa through imagery. It is fully described, documented, and maintained through curated online databases, and can be applied across benthic image collection methods, annotation platforms and scoring methods. Following release in 2013, the CATAMI classification scheme was taken up by a wide variety of users, including government, academia and industry. This rapid acceptance highlights the scheme’s utility and the potential to facilitate broad-scale multidisciplinary studies of marine ecosystems when applied globally. Here we present the CATAMI classification scheme, describe its conception and features, and discuss its utility and the opportunities as well as challenges arising from its use.
The use of biological surrogates as proxies for biodiversity patterns is gaining popularity, particularly in marine systems where field surveys can be expensive and species richness high. Yet, uncertainty regarding their applicability remains because of inconsistency of definitions, a lack of standard methods for estimating effectiveness, and variable spatial scales considered. We present a Bayesian meta-analysis of the effectiveness of biological surrogates in marine ecosystems. Surrogate effectiveness was defined both as the proportion of surrogacy tests where predictions based on surrogates were better than random (i.e., low probability of making a Type I error; P) and as the predictability of targets using surrogates (R 2). A total of 264 published surrogacy tests combined with prior probabilities elicited from eight international experts demonstrated that the habitat, spatial scale, type of surrogate and statistical method used all influenced surrogate effectiveness, at least according to either P or R 2. The type of surrogate used (higher-taxa, cross-taxa or subset taxa) was the best predictor of P, with the higher-taxa surrogates outperforming all others. The marine habitat was the best predictor of R 2, with particularly low predictability in tropical reefs. Surrogate effectiveness was greatest for higher-taxa surrogates at a <10-km spatial scale, in low-complexity marine habitats such as soft bottoms, and using multivariate-based methods. Comparisons with terrestrial studies in terms of the methods used to study surrogates revealed that marine applications still ignore some problems with several widely used statistical approaches to surrogacy. Our study provides a benchmark for the reliable use of biological surrogates in marine ecosystems, and highlights directions for future development of biological surrogates in predicting biodiversity.
Global climate change and ozone layer thinning will simultaneously expose organisms to increasingly stressful conditions. Early life stages of marine organisms, particularly eggs and larvae, are considered most vulnerable to environmental extremes. Here, we exposed encapsulated embryos of three common rocky shore gastropods to simultaneous combinations of ecologically realistic levels of ultraviolet radiation (UVR), water temperature stress and salinity stress to identify potential interactions and associated impacts of climate change. We detected synergistic effects with increases in mortality and retardation in development associated with the most physiologically stressful conditions. The effects of UVR were particularly marked, with mortality increasing up to 12-fold under stressful conditions. Importantly, the complex outcomes observed on applying multiple stressors could not have been predicted from examining environmental variables in isolation. Hence, we are probably dramatically underestimating the ecological impacts of climate change by failing to consider the complex interplay of combinations of environmental variables with organisms.
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