Nanoplastic incorporation into an organismal skeleton.

Studies on the effects of global marine plastic pollution have largely focused on physiological responses of few organism groups (e.g., corals, fishes). Here, we report the first observation of polymer nanoparticles being incorporated into the calcite skeleton of a large benthic foraminifera (LBF), a significant contributor to global carbonate production. While previous work on LBF has documented selectivity in feeding behaviour and a high degree of specialization regarding skeletal formation, in this study, abundant cases of nanoplastic encrustation into the calcite tests were observed. Nanoplastic incorporation was associated with formation of new chambers, in conjunction with rapid nanoplastic ingestion and subsequent incomplete egestion. Microalgae presence in nanoplastic treatments significantly increased the initial feeding response after 1 day, but regardless of microalgae presence, nanoplastic ingestion was similar after 6 weeks of chronic exposure. While ~ 40% of ingesting LBF expelled all nanoplastics from their cytoplasm, nanoplastics were still attached to the test surface and subsequently encrusted by calcite. These findings highlight the need for further investigation regarding plastic pollution impacts on calcifying organisms, e.g., the function of LBF as potential plastic sinks and alterations in structural integrity of LBF tests that will likely have larger ecosystem-level impacts on sediment production.

High-resolution imaging sheds new light on a multi-tier symbiotic partnership between a "walking" solitary coral, a sipunculan, and a bivalve from East Africa.

Marine symbioses are integral to the persistence of ecosystem functioning in coral reefs. Solitary corals of the species Heteropsammia cochlea and Heterocyathus aequicostatus have been observed to live in symbiosis with the sipunculan worm Aspidosiphon muelleri muelleri, which inhabits a cavity within the coral, in Zanzibar (Tanzania). The symbiosis of these photosymbiotic corals enables the coral holobiont to move, in fine to coarse unconsolidated substrata, a process termed as "walking." This allows the coral to escape sediment cover in turbid conditions which is crucial for these light-dependent species. An additional commensalistic symbiosis of this coral-worm holobiont is found between the Aspidosiphon worm and the cryptoendolithic bivalve Jousseaumiella sp., which resides within the cavity of the coral skeleton. To understand the morphological alterations caused by these symbioses, interspecific relationships, with respect to the carbonate structures between these three organisms, are documented using high-resolution imaging techniques (scanning electron microscopy and µCT scanning). Documenting multi-layered symbioses can shed light on how morphological plasticity interacts with environmental conditions to contribute to species persistence.

Ecosystem design as an avenue for improving services provided by carbonate producing marine ecosystems.

Ecosystem Design (ED) is an approach for constructing habitats that places human needs for ecosystem services at the center of intervention, with the overarching goal of establishing self-sustaining habitats which require limited management. This concept was originally developed for use in mangrove ecosystems, and is understandably controversial, as it markedly diverges from other protection approaches that assign human use a minor priority or exclude it. However, the advantage of ED lies within the considered implementation of these designed ecosystems, thus preserving human benefits from potential later disturbances. Here, we outline the concept of ED in tropical carbonate depositional systems and discuss potential applications to aid ecosystem services such as beach nourishment and protection of coastlines and reef islands at risk from environmental and climate change, CO2 sequestration, food production, and tourism. Biological carbonate sediment production is a crucial source of stability of reef islands and reef-rimmed coastlines. Careful implementation of designed carbonate depositional ecosystems could help counterbalance sea-level rise and manage documented erosion effects of coastal constructions. Importantly, adhering to the core ethos of ED, careful dynamic assessments which provide a balanced approach to maximizing ecosystem services (e.g., carbonate production), should identify and avoid any potential damages to existing functioning ecosystems.

Diversity and flexibility of algal symbiont community in globally distributed larger benthic foraminifera of the genus Amphistegina.

BACKGROUND: Understanding the specificity and flexibility of the algal symbiosis-host association is fundamental for predicting how species occupy a diverse range of habitats. Here we assessed the algal symbiosis diversity of three species of larger benthic foraminifera from the genus Amphistegina and investigated the role of habitat and species identity in shaping the associated algal community. RESULTS: We used next-generation sequencing to identify the associated algal community, and DNA barcoding to identify the diatom endosymbionts associated with species of A. lobifera, A. lessonii, and A. radiata, collected from shallow habitats (< 15 m) in 16 sites, ranging from the Mediterranean Sea to French Polynesia. Next-generation sequencing results showed the consistent presence of Ochrophyta as the main algal phylum associated with all species and sites analysed. A significant proportion of phylotypes were classified as Chlorophyta and Myzozoa. We uncovered unprecedented diversity of algal phylotypes found in low abundance, especially of the class Bacillariophyta (i.e., diatoms). We found a significant influence of sites rather than host identity in shaping algal communities in all species. DNA barcoding revealed the consistent presence of phylotypes classified within the order Fragilariales as the diatoms associated with A. lobifera and A. lessonii, while A. radiata specimens host predominately diatoms of the order Triceratiales. CONCLUSIONS: We show that local habitat is the main factor influencing the overall composition of the algal symbiont community. However, host identity and the phylogenetic relationship among hosts is relevant in shaping the specific endosymbiont diatom community, suggesting that the relationship between diatom endosymbiont and hosts plays a crucial role in the evolutionary history of the genus Amphistegina. The capacity of Amphistegina species to associate with a diverse array of diatoms, and possibly other algal groups, likely underpins the ecological success of these crucial calcifying organisms across their extensive geographic range.

Global declines in coral reef calcium carbonate production under ocean acidification and warming.

Ocean warming and acidification threaten the future growth of coral reefs. This is because the calcifying coral reef taxa that construct the calcium carbonate frameworks and cement the reef together are highly sensitive to ocean warming and acidification. However, the global-scale effects of ocean warming and acidification on rates of coral reef net carbonate production remain poorly constrained despite a wealth of studies assessing their effects on the calcification of individual organisms. Here, we present global estimates of projected future changes in coral reef net carbonate production under ocean warming and acidification. We apply a meta-analysis of responses of coral reef taxa calcification and bioerosion rates to predicted changes in coral cover driven by climate change to estimate the net carbonate production rates of 183 reefs worldwide by 2050 and 2100. We forecast mean global reef net carbonate production under representative concentration pathways (RCP) 2.6, 4.5, and 8.5 will decline by 76, 149, and 156%, respectively, by 2100. While 63% of reefs are projected to continue to accrete by 2100 under RCP2.6, 94% will be eroding by 2050 under RCP8.5, and no reefs will continue to accrete at rates matching projected sea level rise under RCP4.5 or 8.5 by 2100. Projected reduced coral cover due to bleaching events predominately drives these declines rather than the direct physiological impacts of ocean warming and acidification on calcification or bioerosion. Presently degraded reefs were also more sensitive in our analysis. These findings highlight the low likelihood that the world's coral reefs will maintain their functional roles without near-term stabilization of atmospheric CO2 emissions.

Amelioration of ocean acidification and warming effects through physiological buffering of a macroalgae.

Concurrent anthropogenic global climate change and ocean acidification are expected to have a negative impact on calcifying marine organisms. While knowledge of biological responses of organisms to oceanic stress has emerged from single-species experiments, these do not capture ecologically relevant scenarios where the potential for multi-organism physiological interactions is assessed. Marine algae provide an interesting case study, as their photosynthetic activity elevates pH in the surrounding microenvironment, potentially buffering more acidic conditions for associated epiphytes. We present findings that indicate increased tolerance of an important epiphytic foraminifera, Marginopora vertebralis, to the effects of increased temperature (±3°C) and pCO2 (~1,000 µatm) when associated with its common algal host, Laurencia intricata. Specimens of M. vertebralis were incubated for 15 days in flow-through aquaria simulating current and end-of-century temperature and pH conditions. Physiological measures of growth (change in wet weight), calcification (measured change in total alkalinity in closed bottles), photochemical efficiency (Fv/Fm), total chlorophyll, photosynthesis (oxygen flux), and respiration were determined. When incubated in isolation, M. vertebralis exhibited reduced growth in end-of-century projections of ocean acidification conditions, while calcification rates were lowest in the high-temperature, low-pH treatment. Interestingly, association with L. intricata ameliorated these stress effects with the growth and calcification rates of M. vertebralis being similar to those observed in ambient conditions. Total chlorophyll levels in M. vertebralis decreased when in association with L. intricata, while maximum photochemical efficiency increased in ambient conditions. Net production estimates remained similar between M. vertebralis in isolation and in association with L. intricata, although both production and respiration rates of M. vertebralis were significantly higher when associated with L. intricata. These results indicate that the association with L. intricata increases the resilience of M. vertebralis to climate change stress, providing one of the first examples of physiological buffering by a marine alga that can ameliorate the negative effects of changing ocean conditions.

High dispersal capacity and biogeographic breaks shape the genetic diversity of a globally distributed reef-dwelling calcifier.

Understanding the role of dispersal and adaptation in the evolutionary history of marine species is essential for predicting their response to changing conditions. We analyzed patterns of genetic differentiation in the key tropical calcifying species of large benthic foraminifera Amphistegina lobifera to reveal the evolutionary processes responsible for its biogeographic distribution. We collected specimens from 16 sites encompassing the entire range of the species and analyzed hypervariable fragments of the 18S SSU rDNA marker. We identified six hierarchically organized genotypes with mutually exclusive distribution organized along a longitudinal gradient. The distribution is consistent with diversification occurring in the Indo-West Pacific (IWP) followed by dispersal toward the periphery. This pattern can be explained by: (a) high dispersal capacity of the species, (b) habitat heterogeneity driving more recent differentiation in the IWP, and (c) ecological-scale processes such as niche incumbency reinforcing patterns of genotype mutual exclusion. The dispersal potential of this species drives the ongoing range expansion into the Mediterranean Sea, indicating that A. lobifera is able to expand its distribution by tracking increases in temperature. The genetic structure reveals recent diversification and high rate of extinction in the evolutionary history of the clade suggesting a high turnover rate of the diversity at the cryptic level. This diversification dynamic combined with high dispersal potential, allowed the species to maintain a widespread distribution over periods of geological and climatic upheaval. These characteristics are likely to allow the species to modify its geographic range in response to ongoing global warming without requiring genetic differentiation.

Ocean acidification effects on in situ coral reef metabolism.

The Anthropocene climate has largely been defined by a rapid increase in atmospheric CO2, causing global climate change (warming) and ocean acidification (OA, a reduction in oceanic pH). OA is of particular concern for coral reefs, as the associated reduction in carbonate ion availability impairs biogenic calcification and promotes dissolution of carbonate substrata. While these trends ultimately affect ecosystem calcification, scaling experimental analyses of the response of organisms to OA to consider the response of ecosystems to OA has proved difficult. The benchmark of ecosystem-level experiments to study the effects of OA is provided through Free Ocean CO2 Enrichment (FOCE), which we use in the present analyses for a 21-d experiment on the back reef of Mo'orea, French Polynesia. Two natural coral reef communities were incubated in situ, with one exposed to ambient pCO2 (393 µatm), and one to high pCO2 (949 µatm). Our results show a decrease in 24-h net community calcification (NCC) under high pCO2, and a reduction in nighttime NCC that attenuated and eventually reversed over 21-d. This effect was not observed in daytime NCC, and it occurred without any effect of high pCO2 on net community production (NCP). These results contribute to previous studies on ecosystem-level responses of coral reefs to the OA conditions projected for the end of the century, and they highlight potential attenuation of high pCO2 effects on nighttime net community calcification.

3D photogrammetry quantifies growth and external erosion of individual coral colonies and skeletons.

Growth and contraction of ecosystem engineers, such as trees, influence ecosystem structure and function. On coral reefs, methods to measure small changes in the structure of microhabitats, driven by growth of coral colonies and contraction of skeletons, are extremely limited. We used 3D reconstructions to quantify changes in the external structure of coral colonies of tabular Acropora spp., the dominant habitat-forming corals in shallow exposed reefs across the Pacific. The volume and surface area of live colonies increased by 21% and 22%, respectively, in 12 months, corresponding to a mean annual linear extension of 5.62 cm yr-1 (±1.81 SE). The volume and surface area of dead skeletons decreased by 52% and 47%, respectively, corresponding to a mean decline in linear extension of -29.56 cm yr-1 (±7.08 SE), which accounted for both erosion and fragmentation of dead colonies. This is the first study to use 3D photogrammetry to assess fine-scale structural changes of entire individual colonies in situ, quantifying coral growth and contraction. The high-resolution of the technique allows for detection of changes on reef structure faster than other non-intrusive approaches. These results improve our capacity to measure the drivers underpinning ecosystem biodiversity, status and trajectory.

Fate of calcifying tropical symbiont-bearing large benthic foraminifera: living sands in a changing ocean.

Concerns regarding the response of calcifiers in future warmer and more acidic oceans have been raised in many studies. Tropical large benthic foraminifera (LBF) are important carbonate producers that reside in coral reefs worldwide. Similar to corals, these organisms live in symbioses with microalgae, which promote high calcification rates. The contribution of LBFs to reef sediments is under threat due to climate change. In this review, we synthesize research conducted on the effects of increased temperature and acidification on these organisms, and assess the potential impacts on reef carbonate production. A meta-analysis of all available experimental data (18 publications, 84 individual experiments) on the effects of ocean warming and acidification on LBF holobiont health was performed using log-transformed response ratios (LnRR) comparing present-day ambient and projected future scenarios. For the latter, we used Representative Concentration Pathway 8.5 from the Intergovernmental Panel on Climate Change, which projects changes of +4 °C and -0.3 pH units by the year 2100. Overall, a general negative trend on holobiont growth was observed across most species of LBFs in response to both stressors. The only exception was the hyaline species (porous CaCO3 test composed of interlocking microcrystals) that have diatom symbionts. Species in this group appear resilient to future ocean acidification scenarios. Differences in the response of LBF species to warming and acidifying oceans may be due to (1) differences in the carbonate species' use in formation of the CaCO3 skeleton (CO2 vs. CO3(2-)), (2) varied responses of the symbiont types (diatom, dinoflagellate, rhodophyte) to stressors, or (3) the degree of nutritional dependence of the host to its symbiont. We also summarize current estimates of carbonate production by LBFs to provide a context of their contribution to reefs. Finally, we outline major gaps in knowledge in addressing the potential for LBF species persistence in a changing ocean.