Rachel Przeslawski

A review and meta‐analysis of the effects of multiple abiotic stressors on marine embryos and larvae

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.

Effectiveness of biological surrogates for predicting patterns of marine biodiversity: a global meta-analysis.

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.

A review of the effects of environmental stress on embryonic development within intertidal gastropod egg masses

Gastropod egg masses are often deposited in the intertidal zone, where they are exposed to variable and often stressful environmental conditions that may affect the encapsulated embryonic development and survival of offspring. The present paper reviews data on developmental variation in gastropod egg masses owing to temperature, salinity, ultraviolet radiation (UVR) and oxygen availability. In general, increases in temperature or oxygen availability accelerate development, whereas UVR or extremes of salinity and temperature slow development and/or increase embryonic mortality. The relationships among these factors are discussed, as are their interactions with biotic factors, such as fouling, embryonic position within the egg mass and predation. One purpose of the present review is to raise awareness of these interactions so they become a focus for future research. Protective mechanisms of egg masses against environmental stresses are also reviewed. M a astm R. P la Additional keywords: mollusc, oxygen availability, reproduction, salinity, temperature, ultraviolet radiation.

A Standardised Vocabulary for Identifying Benthic Biota and Substrata from Underwater Imagery: The CATAMI Classification Scheme

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.

Complex Responses of Intertidal Molluscan Embryos to a Warming and Acidifying Ocean in the Presence of UV Radiation

Climate change and ocean acidification will expose marine organisms to synchronous multiple stressors, with early life stages being potentially most vulnerable to changing environmental conditions. We simultaneously exposed encapsulated molluscan embryos to three abiotic stressors—acidified conditions, elevated temperate, and solar UV radiation in large outdoor water tables in a multifactorial design. Solar UV radiation was modified with plastic filters, while levels of the other factors reflected IPCC predictions for near-future change. We quantified mortality and the rate of embryonic development for a mid-shore littorinid, Bembicium nanum, and low-shore opisthobranch, Dolabrifera brazieri. Outcomes were consistent for these model species with embryos faring significantly better at 26°C than 22°C. Mortality sharply increased at the lowest temperature (22°C) and lowest pH (7.6) examined, producing a significant interaction. Under these conditions mortality approached 100% for each species, representing a 2- to 4-fold increase in mortality relative to warm (26°C) non-acidified conditions. Predictably, development was more rapid at the highest temperature but this again interacted with acidified conditions. Development was slowed under acidified conditions at the lowest temperature. The presence of UV radiation had minimal impact on the outcomes, only slowing development for the littorinid and not interacting with the other factors. Our findings suggest that a warming ocean, at least to a threshold, may compensate for the effects of decreasing pH for some species. It also appears that stressors will interact in complex and unpredictable ways in a changing climate.

A critical review of the potential impacts of marine seismic surveys on fish & invertebrates

Marine seismic surveys produce high intensity, low-frequency impulsive sounds at regular intervals, with most sound produced between 10 and 300Hz. Offshore seismic surveys have long been considered to be disruptive to fisheries, but there are few ecological studies that target commercially important species, particularly invertebrates. This review aims to summarise scientific studies investigating the impacts of low-frequency sound on marine fish and invertebrates, as well as to critically evaluate how such studies may apply to field populations exposed to seismic operations. We focus on marine seismic surveys due to their associated unique sound properties (i.e. acute, low-frequency, mobile source locations), as well as fish and invertebrates due to the commercial value of many species in these groups. The main challenges of seismic impact research are the translation of laboratory results to field populations over a range of sound exposure scenarios and the lack of sound exposure standardisation which hinders the identification of response thresholds. An integrated multidisciplinary approach to manipulative and in situ studies is the most effective way to establish impact thresholds in the context of realistic exposure levels, but if that is not practical the limitations of each approach must be carefully considered.

Sponge biodiversity and ecology of the Van Diemen Rise and eastern Joseph Bonaparte Gulf, northern Australia

Australia is increasingly recognised as a global hotspot for sponge biodiversity, but there is a knowledge gap about sponge communities in northern Australia, including those in Commonwealth Marine Reserves. We aim to quantify sponge biodiversity of the eastern Joseph Bonaparte Gulf and adjacent Van Diemen Rise (VDR) and to examine spatial and environmental patterns in community structure. Sponges were collected with a benthic sled from 65 sites encompassing five geomorphic features (bank, terrace, ridge, plain, and valley), study area (as a proxy for distance offshore) and three environmental variables (depth, substrate hardness, and slope). A total of 283 species were collected, representing four classes, 53 families and at least 117 genera. Sponge richness and biomass were related to those of other taxa. Sponge diversity was generally highest further offshore and on raised geomorphic features, particularly banks. Sponge assemblages on the same bank were more similar than those from different banks, although full interpretation of patterns is limited by the relatively low sampling effort. The current study will help facilitate integrated marine management by providing a baseline species inventory, supporting the VDR’s carbonate banks as a key ecological feature, and highlighting the importance of sponges as habitat providers and potential biological surrogates for monitoring.

Loss of evolutionary resistance by the oligochaete Limnodrilus hoffmeisteri to a toxic substance - cost or gene flow?

The oligochaete Limnodrilus hoffmeisteri at Foundry Cove (FC), New York evolved genetic resistance to cadmium (Cd) and lost resistance after contaminated sediments were removed by dredging. Selection (on survival time in dissolved Cd) was used to generate tolerance to evaluate fitness cost, the commonplace expectation for evolutionary reversal. The hypothesis that gene flow from neighboring populations could “swamp” resistance was addressed by 16S rDNA sequences. In disagreement with the cost hypothesis, selected‐Cd tolerant worms and controls showed no difference in total fecundity or growth rate in environments. Highly‐Cd‐tolerant worms of the FC‐selected population grew rapidly at different temperatures and showed no growth impairment in the presence of Cd, indicating metabolically efficient resistance. Genetic structure at FC was consistent with invasion of genotypes from an adjacent population in the time since dredging. Applying selection to lines from FC and a reference site, demonstrated a more rapid increase in Cd tolerance in FC‐origin lines, indicating standing allelic variation for resistance at FC (despite phenotypic erosion). The selection experiment supports the view that resistance is simply controlled—probably by one allele of large effect. Whether such rapid “readaptation” could occur naturally is an important question for understanding broad effects of pollutants.

Predictive mapping of soft-bottom benthic biodiversity using a surrogacy approach

A key requirement for informed marine-zone management is an understanding of the spatial patterns of marine biodiversity, often measured as species richness, total abundance or presence of key taxa. In the present study, we focussed on the diversity of benthic infauna and applied a predictive modelling approach to map biodiversity patterns for three study sites on the tropical Carnarvon shelf of Western Australia. A random forest decision tree model was used to generate spatial predictions of two measures of infaunal diversity, namely, species richness and total abundance. Results explained between 20% and 37% of the variance of each measure. The modelling process also identified potential physical surrogates for species richness and abundance, with sediment physical properties ranked as most important across the study region. Specifically, coarse-grained heterogeneous sediments were associated with higher infaunal species richness and total abundance. Seabed topographic properties were also important at the local scale. The study demonstrated the value of a surrogacy approach to the prediction of biodiversity patterns, particularly when the number of biological samples was limited. Such an approach may facilitate an understanding of ecosystem processes in the region and contribute to integrated marine management.

Multiple measures are necessary to assess rarity in macro-molluscs: a case study from southeastern Australia

Our knowledge of suitable criteria to determine rarity in most marine invertebrates is lacking, thus hindering targeted impact studies, long-term monitoring programs, and associated conservation strategies. Standardized definitions of rarity are required to enable comparisons of different assemblages and taxa. Gaston (Rarity, Chapman and Hall, Melbourne, 1994) has recommended that rare species are defined as the lowest quartile of species in the assemblage. In this study, the 25% ‘cut-off’ was applied to intertidal macro-molluscs along the Illawarra Coast, Australia from 200 surveys of 13 reefs, using three measures of population structure; (1) local abundance (numerical rarity); (2) number of locations (spatial rarity) and; (3) percent of surveys (temporal rarity). Rare species were consequently defined as those species with no more than; (1) a local abundance of two individuals; (2) a regional occurrence at two reefs and/or; (3) a temporal occurrence in 2% of all surveys. These cut-off values increased when only intertidal specialists were analysed. Using a combination of all three measures, 62 species (42%) were classified as regionally rare, but only four of these were true intertidal specialists. Most species were rare by only one or two definitions of rarity; illustrating the importance of considering multiple measures of rarity and the need to design specifically targeted survey methods for future monitoring. Many species that are rare by all three definitions are likely to be temporary immigrants, as subtidal species were significantly more likely to be classified as rare. Clearly many factors can influence the rarity of marine invertebrates on intertidal reefs, and these must all be considered to set appropriate conservation priorities.