Chapter 11: Vulnerability of benthic invertebrates of the Great Barrier Reef to climate change

This chapter deals with benthic invertebrates inhabiting the extensive inter-reef soft bottom habitats and those occurring on the reef, excluding corals. For the remainder of the chapter, the term ‘benthic invertebrate’ refers to all invertebrates excluding corals. An assessment of the impacts of climate change on non-coral benthic invertebrates poses particular challenges: i) benthic invertebrates include an extraordinary diversity of marine organisms, including many microscopic, infaunal, boring or ephemeral species that can be difficult to sample and are poorly known taxonomically; ii) benthic invertebrates employ a diversity of reproductive strategies, broadly including planktotrophy (development through feeding larvae), lecithotrophy (development through non-feeding larvae) and direct development (release of post-metamorphic juveniles), as well as asexual reproduction, making broad generalisations of dispersal capabilities difficult; iii) factors determining species distributions are poorly known for most species; iv) benthic invertebrates exhibit a tremendous variety of lifestyles and forms, including colonial, sedentary and errant species; v) many species include either a pelagic larval or adult stage, so effects of climate change may vary during their lives (see McKinnon et al. chapter 6 for comments on planktonic forms); and, vi) research on the biogeography of benthic invertebrates on the Great Barrier Reef (GBR) is strongly biased towards commercial or destructive species.This is Chapter 11 of Climate change and the Great Barrier Reef: a vulnerability assessment. The entire book can be found at http://hdl.handle.net/11017/13

The Role of the Proteinase Inhibitor Ovorubin in Apple Snail Eggs Resembles Plant Embryo Defense against Predation

BACKGROUND: Fieldwork has thoroughly established that most eggs are intensely predated. Among the few exceptions are the aerial egg clutches from the aquatic snail Pomacea canaliculata which have virtually no predators. Its defenses are advertised by the pigmented ovorubin perivitellin providing a conspicuous reddish coloration. The nature of the defense however, was not clear, except for a screening for defenses that identified a neurotoxic perivitellin with lethal effect on rodents. Ovorubin is a proteinase inhibitor (PI) whose role to protect against pathogens was taken for granted, according to the prevailing assumption. Through biochemical, biophysical and feeding experiments we studied the proteinase inhibitor function of ovorubin in egg defenses. METHODOLOGY/PRINCIPAL FINDINGS: Mass spectrometry sequencing indicated ovorubin belongs to the Kunitz-type serine proteinase inhibitor family. It specifically binds trypsin as determined by small angle X-ray scattering (SAXS) and cross-linking studies but, in contrast to the classical assumption, it does not prevent bacterial growth. Ovorubin was found extremely resistant to in vitro gastrointestinal proteolysis. Moreover feeding studies showed that ovorubin ingestion diminishes growth rate in rats indicating that this highly stable PI is capable of surviving passage through the gastrointestinal tract in a biologically active form. CONCLUSIONS: To our knowledge, this is the first direct evidence of the interaction of an egg PI with a digestive protease of potential predators, limiting predator's ability to digest egg nutrients. This role has not been reported in the animal kingdom but it is similar to plant defenses against herbivory. Further, this would be the only defense model with no trade-offs between conspicuousness and noxiousness by encoding into the same molecule both the aposematic warning signal and an antinutritive/antidigestive defense. These defenses, combined with a neurotoxin and probably unpalatable factors would explain the near absence of predators, opening new perspectives in the study of the evolution and ecology of egg defensive strategies

Transgenerational plasticity and selection shape the adaptive potential of sticklebacks to salinity change

In marine climate change research, salinity shifts have been widely overlooked. While widespread desalination effects are expected in higher latitudes, salinity is predicted to increase closer to the equator. Here, we use the steep salinity gradient of the Baltic Sea as a space‐for time design to address effects of salinity change on populations. Additionally, genetic diversity, a prerequisite for adaptive responses, is reduced in Baltic compared to Atlantic populations. On the one hand, adaptive transgenerational plasticity (TGP) might buffer the effects of environmental change, which may be of particular importance under reduced genetic variation. On the other hand, physiological trade‐offs due to environmental stress may hamper parental provisioning to offspring thereby intensifying the impact of climate change across generations (non‐adaptive TGP). Here, we studied both hypothesis of adaptive and non‐adaptive TGP in the three‐spined stickleback (Gasterosteus aculeatus) fish model along the strong salinity gradient of the Baltic Sea in a space‐for‐time experiment. Each population tolerated desalination well, which was not altered by parental exposure to low salinity. Despite a common marine ancestor, populations locally adapted to low salinity lost their ability to cope with fully marine conditions, resulting in lower survival and reduced relative fitness. Negative transgenerational effects were evident in early life stages, but disappeared after selection via mortality occurred during the first 12‐30 days post hatch. Modeling various strengths of selection, we showed that non‐adaptive transgenerational plasticity accelerated evolution by increasing directional selection within the offspring generation. Qualitatively, when genetic diversity is large, we predict that such effects will facilitate rapid adaptation and population persistence, while below a certain threshold populations suffer a higher risk of local extinction. Overall, our results suggest that transgenerational plasticity and selection are not independent of each other and thereby highlight a current gap in TGP studies

Evolving and sustaining ocean best practices and standards for the next decade

The oceans play a key role in global issues such as climate change, food security, and human health. Given their vast dimensions and internal complexity, efficient monitoring and predicting of the planet's ocean must be a collaborative effort of both regional and global scale. A first and foremost requirement for such collaborative ocean observing is the need to follow well-defined and reproducible methods across activities: from strategies for structuring observing systems, sensor deployment and usage, and the generation of data and information products, to ethical and governance aspects when executing ocean observing. To meet the urgent, planet-wide challenges we face, methods across all aspects of ocean observing should be broadly adopted by the ocean community and, where appropriate, should evolve into "Ocean Best Practices." While many groups have created best practices, they are scattered across the Web or buried in local repositories and many have yet to be digitized. To reduce this fragmentation, we introduce a new open access, permanent, digital repository of best practices documentation (oceanbestpractices.org) that is part of the Ocean Best Practices System (OBPS). The new OBPS provides an opportunity space for the centralized and coordinated improvement of ocean observing methods. The OBPS repository employs user-friendly software to significantly improve discovery and access to methods. The software includes advanced semantic technologies for search capabilities to enhance repository operations. In addition to the repository, the OBPS also includes a peer reviewed journal research topic, a forum for community discussion and a training activity for use of best practices. Together, these components serve to realize a core objective of the OBPS, which is to enable the ocean community to create superior methods for every activity in ocean observing from research to operations to applications that are agreed upon and broadly adopted across communities. Using selected ocean observing examples, we show how the OBPS supports this objective. This paper lays out a future vision of ocean best practices and how OBPS will contribute to improving ocean observing in the decade to come

Impact of Ocean Warming and Ocean Acidification on Larval Development and Calcification in the Sea Urchin Tripneustes gratilla

Background: As the oceans simultaneously warm, acidify and increase in P-CO2, prospects for marine biota are of concern. Calcifying species may find it difficult to produce their skeleton because ocean acidification decreases calcium carbonate saturation and accompanying hypercapnia suppresses metabolism. However, this may be buffered by enhanced growth and metabolism due to warming.Methodology/Principal Findings: We examined the interactive effects of near-future ocean warming and increased acidification/P-CO2 on larval development in the tropical sea urchin Tripneustes gratilla. Larvae were reared in multifactorial experiments in flow-through conditions in all combinations of three temperature and three pH/P-CO2 treatments. Experiments were placed in the setting of projected near future conditions for SE Australia, a global change hot spot. Increased acidity/P-CO2 and decreased carbonate mineral saturation significantly reduced larval growth resulting in decreased skeletal length. Increased temperature (+3 degrees C) stimulated growth, producing significantly bigger larvae across all pH/P-CO2 treatments up to a thermal threshold (+6 degrees C). Increased acidity (-0.3-0.5 pH units) and hypercapnia significantly reduced larval calcification. A +3 degrees C warming diminished the negative effects of acidification and hypercapnia on larval growth.Conclusions and Significance: This study of the effects of ocean warming and CO2 driven acidification on development and calcification of marine invertebrate larvae reared in experimental conditions from the outset of development (fertilization) shows the positive and negative effects of these stressors. In simultaneous exposure to stressors the dwarfing effects of acidification were dominant. Reduction in size of sea urchin larvae in a high P-CO2 ocean would likely impair their performance with negative consequent effects for benthic adult populations

Quantifying Rates of Evolutionary Adaptation in Response to Ocean Acidification

The global acidification of the earth's oceans is predicted to impact biodiversity via physiological effects impacting growth, survival, reproduction, and immunology, leading to changes in species abundances and global distributions. However, the degree to which these changes will play out critically depends on the evolutionary rate at which populations will respond to natural selection imposed by ocean acidification, which remains largely unquantified. Here we measure the potential for an evolutionary response to ocean acidification in larval development rate in two coastal invertebrates using a full-factorial breeding design. We show that the sea urchin species Strongylocentrotus franciscanus has vastly greater levels of phenotypic and genetic variation for larval size in future CO2 conditions compared to the mussel species Mytilus trossulus. Using these measures we demonstrate that S. franciscanus may have faster evolutionary responses within 50 years of the onset of predicted year-2100 CO2 conditions despite having lower population turnover rates. Our comparisons suggest that information on genetic variation, phenotypic variation, and key demographic parameters, may lend valuable insight into relative evolutionary potentials across a large number of species

Acanthaster planci Outbreak: Decline in Coral Health, Coral Size Structure Modification and Consequences for Obligate Decapod Assemblages

Although benthic motile invertebrate communities encompass the vast majority of coral reef diversity, their response to habitat modification has been poorly studied. A variety of benthic species, particularly decapods, provide benefits to their coral host enabling them to cope with environmental stressors, and as a result benefit the overall diversity of coral-associated species. However, little is known about how invertebrate assemblages associated with corals will be affected by global perturbations, (either directly or indirectly via their coral host) or their consequences for ecosystem resilience. Analysis of a ten year dataset reveals that the greatest perturbation at Moorea over this time was an outbreak of the corallivorous sea star Acanthaster planci from 2006 to 2009 impacting habitat health, availability and size structure of Pocillopora spp. populations and highlights a positive relationship between coral head size and survival. We then present the results of a mensurative study in 2009 conducted at the end of the perturbation (A. planci outbreak) describing how coral-decapod communities change with percent coral mortality for a selected coral species, Pocillopora eydouxi. The loss of coral tissue as a consequence of A. planci consumption led to an increase in rarefied total species diversity, but caused drastic modifications in community composition driven by a shift from coral obligate to non-obligate decapod species. Our study highlights that larger corals left with live tissue in 2009, formed a restricted habitat where coral obligate decapods, including mutualists, could subsist. We conclude that the size structure of Pocillopora populations at the time of an A. planci outbreak may greatly condition the magnitude of coral mortality as well as the persistence of local populations of obligate decapods

Thermal and Sedimentation Stress Are Unlikely Causes of Brown Spot Syndrome in the Coral Reef Sponge, Ianthella basta

Background: Marine diseases are being increasingly linked to anthropogenic factors including global and local stressors. On the Great Barrier Reef, up to 66% of the Ianthella basta population was recently found to be afflicted by a syndrome characterized by brown spot lesions and necrotic tissue.\ud \ud Methodology/Principal Findings: Manipulative experiments were undertaken to ascertain the role of environmental stressors in this syndrome. Specifically, the effects of elevated temperature and sedimentation on sponge health and symbiont stability in I. basta were examined. Neither elevated temperature nor increased sedimentation were responsible for the brown spot lesions, but sponges exposed to 32°C developed substantial discoloration and deterioration of their tissues, resulting in death after eight days and a higher microbial diversity in those samples. No shifts in the microbial community of I. basta were observed across a latitudinal gradient or with increased sedimentation, with three previously described symbionts dominating the community of all sponges (Alphaproteobacteria, Gammaproteobacteria and Thaumarchaea).\ud \ud Conclusions/Significance: Results from this study highlight the stable microbial community of I. basta and indicate that thermal and sedimentation stress are not responsible for the brown spot lesions currently affecting this abundant and ecologically important sponge species

Increasing Costs Due to Ocean Acidification Drives Phytoplankton to Be More Heavily Calcified: Optimal Growth Strategy of Coccolithophores

Ocean acidification is potentially one of the greatest threats to marine ecosystems and global carbon cycling. Amongst calcifying organisms, coccolithophores have received special attention because their calcite precipitation plays a significant role in alkalinity flux to the deep ocean (i.e., inorganic carbon pump). Currently, empirical effort is devoted to evaluating the plastic responses to acidification, but evolutionary considerations are missing from this approach. We thus constructed an optimality model to evaluate the evolutionary response of coccolithophorid life history, assuming that their exoskeleton (coccolith) serves to reduce the instantaneous mortality rates. Our model predicted that natural selection favors constructing more heavily calcified exoskeleton in response to increased acidification-driven costs. This counter-intuitive response occurs because the fitness benefit of choosing a better-defended, slower growth strategy in more acidic conditions, outweighs that of accelerating the cell cycle, as this occurs by producing less calcified exoskeleton. Contrary to the widely held belief, the evolutionarily optimized population can precipitate larger amounts of CaCO3 during the bloom in more acidified seawater, depending on parameter values. These findings suggest that ocean acidification may enhance the calcification rates of marine organisms as an adaptive response, possibly accompanied by higher carbon fixation ability. Our theory also provides a compelling explanation for the multispecific fossil time-series record from ∼200 years ago to present, in which mean coccolith size has increased along with rising atmospheric CO2 concentration