In situ decrease in rhodolith growth associated with Arctic climate change.

Rhodoliths built by crustose coralline algae (CCA) are ecosystem engineers of global importance. In the Arctic photic zone, their three-dimensional growth emulates the habitat complexity of coral reefs but with a far slower growth rate, growing at micrometers per year rather than millimeters. While climate change is known to exert various impacts on the CCA's calcite skeleton, including geochemical and structural alterations, field observations of net growth over decade-long timescales are lacking. Here, we use a temporally explicit model to show that rising ocean temperatures over nearly 100 years were associated with reduced rhodolith growth at different depths in the Arctic. Over the past 90 years, the median growth rate was 85 µm year-1 but each °C increase in summer seawater temperature decreased growth by a mean of 8.9 µm (95% confidence intervals = 1.32-16.60 µm °C-1, p < .05). The decrease was expressed for rhodolith occurrences in 11 and 27 m water depth but not at 46 m, also having the shortest time series (1991-2015). Although increasing temperatures can spur plant growth, we suggest anthropogenic climate change has either exceeded the population thermal optimum for these CCA, or synergistic effects of warming, ocean acidification, and/or increasing turbidity impair rhodolith growth. Rhodoliths built by calcitic CCA are important habitat providers worldwide, so decreased growth would lead to yet another facet of anthropogenic habitat loss.

A carbonate corrosion experiment at a marine methane seep: The role of aerobic methanotrophic bacteria.

Methane seeps are typified by the formation of authigenic carbonates, many of which exhibit corrosion surfaces and secondary porosity believed to be caused by microbial carbonate dissolution. Aerobic methane oxidation and sulfur oxidation are two processes capable of inducing carbonate corrosion at methane seeps. Although the potential of aerobic methanotrophy to dissolve carbonate was confirmed in laboratory experiments, this process has not been studied in the environment to date. Here, we report on a carbonate corrosion experiment carried out in the REGAB Pockmark, Gabon-Congo-Angola passive margin, in which marble cubes were deployed for 2.5 years at two sites (CAB-B and CAB-C) with apparent active methane seepage and one site (CAB-D) without methane seepage. Marble cubes exposed to active seepage (experiment CAB-C) were found to be affected by a new type of microbioerosion. Based on 16S rRNA gene analysis, the biofilms adhering to the bioeroded marble mostly consisted of aerobic methanotrophic bacteria, predominantly belonging to the uncultured Hyd24-01 clade. The presence of abundant 13 C-depleted lipid biomarkers including fatty acids (n-C16:1ω8c , n-C18:1ω8c , n-C16:1ω5t ), various 4-mono- and 4,4-dimethyl sterols, and diplopterol agrees with the dominance of aerobic methanotrophs in the CAB-C biofilms. Among the lipids of aerobic methanotrophs, the uncommon 4α-methylcholest-8(14)-en-3ß,25-diol is interpreted to be a specific biomarker for the Hyd24-01 clade. The combination of textural, genetic, and organic geochemical evidence suggests that aerobic methanotrophs are the main drivers of carbonate dissolution observed in the CAB-C experiment at the REGAB pockmark.

'Ten Years After'-a long-term settlement and bioerosion experiment in an Arctic rhodolith bed (Mosselbukta, Svalbard).

Rhodolith beds and bioherms formed by ecosystem engineering crustose coralline algae support the northernmost centres of carbonate production, referred to as polar cold-water carbonate factories. Yet, little is known about biodiversity and recruitment of these hard-bottom communities or the bioeroders degrading them, and there is a demand for carbonate budgets to include respective rates of polar carbonate build-up and bioerosion. To address these issues, a 10-year settlement and bioerosion experiment was carried out at the Arctic Svalbard archipelago in and downslope of a rhodolith bed. The calcifiers recorded on experimental settlement tiles (56 taxa) were dominated by bryozoans, serpulids and foraminiferans. The majority of the bioerosion traces (30 ichnotaxa) were microborings, followed by attachment etchings and grazing traces. Biodiversity metrics show that calcifier diversity and bioerosion ichnodiversity are both elevated in the rhodolith bed, if compared to adjacent aphotic waters, but these differences are statistically insignificant. Accordingly, there were only low to moderate dissimilarities in the calcifier community structure and bioerosion trace assemblages between the two depth stations (46 and 127 m), substrate orientations (up- and down-facing) and substrate types (PVC and limestone), in that order of relevance. In contrast, surface coverage as well as the carbonate accretion and bioerosion rates were all significantly elevated in the rhodolith bed, reflecting higher abundance or size of calcifiers and bioerosion traces. All three measures were highest for up-facing substrates at 46 m, with a mean coverage of 78.2% (on PVC substrates), a mean accretion rate of 24.6 g m-2   year-1 (PVC), and a mean bioerosion rate of -35.1 g m-2  year-1 (limestone). Differences in these metrics depend on the same order of factors than the community structure. Considering all limestone substrates of the two platforms, carbonate accretion and bioerosion were nearly in balance at a net rate of -2.5 g m-2  year-1 . A latitudinal comparison with previous settlement studies in the North Atlantic suggests that despite the harsh polar environment there is neither a depletion in the diversity of hard-bottom calcifier communities nor in the ichnodiversity of grazing traces, attachment etchings and microborings formed by organotrophs. In contrast, microborings produced by phototrophs are strongly depleted because of limitations in the availability of light (condensed photic zonation, polar night, shading by sea ice). Also, macroborings were almost absent, surprisingly. With respect to carbonate production, the Svalbard carbonate factory marks the low end of a latitudinal gradient while bioerosion rates are similar or even higher than at comparable depth or photic regime at lower latitudes, although this might not apply to shallow euphotic waters (not covered in our experiment), given the observed depletion in bioeroding microphytes and macroborers. While echinoid grazing is particularly relevant for the bioerosion in the rhodolith bed, respective rates are far lower than those reported from tropical shallow-water coral reefs. The slow pace of carbonate production but relatively high rates of bioerosion (both promoted by low carbonate supersaturation states in Arctic waters), in concert with high retention of skeletal carbonates on the seafloor and no calcite cements forming in open pore space created by microborers, suggest a low fossilisation potential for polar carbonates, such as those formed in the Mosselbukta rhodolith beds.

Exploring confocal laser scanning microscopy (CLSM) and fluorescence staining as a tool for imaging and quantifying traces of marine microbioerosion and their trace-making microendoliths.

Microscopic organisms that penetrate calcareous structures by actively dissolving the carbonate matrix, namely microendoliths, have an important influence on the breakdown of marine carbonates. The study of these microorganisms and the bioerosion traces they produce is crucial for understanding the impact of their bioeroding activity on the carbonate recycling in environments under global climate change. Traditionally, either the extracted microendoliths were studied by conventional microscopy or their traces were investigated using scanning electron microscopy (SEM) of epoxy resin casts. A visualisation of the microendoliths in situ, that is within their complex microbioerosion structures, was previously limited to the laborious and time-consuming double-inclusion cast-embedding technique. Here, we assess the applicability of various fluorescence staining methods in combination with confocal laser scanning microscopy (CLSM) for the study of fungal microendoliths in situ in partly translucent mollusc shells. Among the tested methods, specific staining with dyes against the DNA (nuclei) of the trace making organisms turned out to be a useful and reproducible approach. Bright and clearly delineated fluorescence signals of microendolithic nuclei allow, for instance, a differentiation between abandoned and still populated microborings. Furthermore, infiltrating the microborings with fluorescently stained resin seems to be of great capability for the visualisation and quantification of microbioerosion structures in their original spatial orientation. Potential fields of application are rapid assessments of endolithic bio- and ichnodiversity and the quantification of the impact of microendoliths on the overall calcium carbonate turnover. The method can be applied after CLSM of the stained microendoliths and retains the opportunity for a subsequent investigation of epoxy casts with SEM. This allows a three-fold approach in studying microendoliths in the context of their microborings, thereby fostering the integration of biological and ichnological aspects of microbial bioerosion.

Bioerosion describes the process of active erosion of hard substrates induced by the activity of living organisms. Beside numerous marine macroscopic bioeroding organisms such as sponges, annelids or bivalves, there is an astonishing 'hidden diversity' of microscopic bioeroding organisms which produce minute tunnels and chambers, for example in calcareous shells and skeletons of other marine organisms. These so-called microendoliths belong to bacteria, microalgae, foraminiferans, or fungi. Due to their lifestyle hidden inside the hard substrate, scientific investigation is often laborious and involves complex preparation techniques, electron microscopy, or even nano-computed tomography. Photo-autotrophic microendoliths (eg cyanobacteria and algae) have been studied with fluorescence microscopy using autofluorescence properties, for example of their chloroplasts. However, microendoliths of aphotic depths, mostly of fungal origin, do not show autofluorescence. With the present study we test different fluorescent dyes staining the microbioeroders 'in situ', that is, inside their microscopic tunnels, and visualise them using three-dimensional confocal laser scanning microscopy (CLSM). Very good results have been obtained with the dye Sybr Green I that stains DNA molecules and thereby the cell nuclei of the microendoliths. This method can be used, for instance, to measure the infestation rate of a given substrate by discriminating between abandoned microborings and those still inhabited by microendoliths. Another approach that was successfully tested in the course of the present study was the infiltration of the cleaned microborings with resin that was previously mixed with the fluorescent dye Safranin-O. The datasets obtained with the CLSM were used to reconstruct 3D-surface models of the microborings of three different microendoliths. Such models can be used to analyse the original spatial arrangement inside the hard substrate and to measure exact volumes. The resulting possibility to make exact quantifications is of high value for future investigations that focus on the role and proportion of microbioerosion in the (re)cycling of marine carbonates.

Microplastic contamination of the drilling bivalve Hiatella arctica in Arctic rhodolith beds.

There is an increasing number of studies reporting microplastic (MP) contamination in the Arctic environment. We analysed MP abundance in samples from a marine Arctic ecosystem that has not been investigated in this context and that features a high biodiversity: hollow rhodoliths gouged by the bivalve Hiatella arctica. This bivalve is a filter feeder that potentially accumulates MPs and may therefore reflect MP contamination of the rhodolith ecosystem at northern Svalbard. Our analyses revealed that 100% of the examined specimens were contaminated with MP, ranging between one and 184 MP particles per bivalve in samples from two water depths. Polymer composition and abundance differed strongly between both water depths: samples from 40 m water depth showed a generally higher concentration of MPs and were clearly dominated by polystyrene, samples from 27 m water depth were more balanced in composition, mainly consisting of polyethylene, polyethylene terephthalate, and polypropylene. Long-term consequences of MP contamination in the investigated bivalve species and for the rhodolith bed ecosystem are yet unclear. However, the uptake of MPs may potentially impact H. arctica and consequently its functioning as ecosystem engineers in Arctic rhodolith beds.

Compositional variability of Mg/Ca, Sr/Ca, and Na/Ca in the deep-sea bivalve Acesta excavata (Fabricius, 1779).

Acesta excavata (Fabricius, 1779) is a slow growing bivalve from the Limidae family and is often found associated with cold-water coral reefs along the European continental margin. Here we present the compositional variability of frequently used proxy elemental ratios (Mg/Ca, Sr/Ca, Na/Ca) measured by laser-ablation mass spectrometry (LA-ICP-MS) and compare it to in-situ recorded instrumental seawater parameters such as temperature and salinity. Shell Mg/Ca measured in the fibrous calcitic shell section was overall not correlated with seawater temperature or salinity; however, some samples show significant correlations with temperature with a sensitivity that was found to be unusually high in comparison to other marine organisms. Mg/Ca and Sr/Ca measured in the fibrous calcitic shell section display significant negative correlations with the linear extension rate of the shell, which indicates strong vital effects in these bivalves. Multiple linear regression analysis indicates that up to 79% of elemental variability is explicable with temperature and salinity as independent predictor values. Yet, the overall results clearly show that the application of Element/Ca (E/Ca) ratios in these bivalves to reconstruct past changes in temperature and salinity is likely to be complicated due to strong vital effects and the effects of organic material embedded in the shell. Therefore, we suggest to apply additional techniques, such as clumped isotopes, in order to exactly determine and quantify the underlying vital effects and possibly account for these. We found differences in the chemical composition between the two calcitic shell layers that are possibly explainable through differences of the crystal morphology. Sr/Ca ratios also appear to be partly controlled by the amount of magnesium, because the small magnesium ions bend the crystal lattice which increases the space for strontium incorporation. Oxidative cleaning with H2O2 did not significantly change the Mg/Ca and Sr/Ca composition of the shell. Na/Ca ratios decreased after the oxidative cleaning, which is most likely a leaching effect and not caused by the removal of organic matter.

Quantifying ecospace utilization and ecosystem engineering during the early Phanerozoic-The role of bioturbation and bioerosion.

The Cambrian explosion (CE) and the great Ordovician biodiversification event (GOBE) are the two most important radiations in Paleozoic oceans. We quantify the role of bioturbation and bioerosion in ecospace utilization and ecosystem engineering using information from 1367 stratigraphic units. An increase in all diversity metrics is demonstrated for the Ediacaran-Cambrian transition, followed by a decrease in most values during the middle to late Cambrian, and by a more modest increase during the Ordovician. A marked increase in ichnodiversity and ichnodisparity of bioturbation is shown during the CE and of bioerosion during the GOBE. Innovations took place first in offshore settings and later expanded into marginal-marine, nearshore, deep-water, and carbonate environments. This study highlights the importance of the CE, despite its Ediacaran roots. Differences in infaunalization in offshore and shelf paleoenvironments favor the hypothesis of early Cambrian wedge-shaped oxygen minimum zones instead of a horizontally stratified ocean.

In situ growth and bioerosion rates of Lophelia pertusa in a Norwegian fjord and open shelf cold-water coral habitat.

Coral reef resilience depends on the balance between carbonate precipitation, leading to reef growth, and carbonate degradation, for example, through bioerosion. Changes in environmental conditions are likely to affect the two processes differently, thereby shifting the balance between reef growth and degradation. In cold-water corals estimates of accretion-erosion processes in their natural habitat are scarce and solely live coral growth rates were studied with regard to future environmental changes in the laboratory so far, limiting our ability to assess the potential of cold-water coral reef ecosystems to cope with environmental changes. In the present study, growth rates of the two predominant colour morphotypes of live Lophelia pertusa as well as bioerosion rates of dead coral framework were assessed in different environmental settings in Norwegian cold-water coral reefs in a 1-year in situ experiment. Net growth (in weight gain and linear extension) of live L. pertusa was in the lower range of previous estimates and did not significantly differ between inshore (fjord) and offshore (open shelf) habitats. However, slightly higher net growth rates were obtained inshore. Bioerosion rates were significantly higher on-reef in the fjord compared to off-reef deployments in- and offshore. Besides, on-reef coral fragments yielded a broader range of individual growth and bioerosion rates, indicating higher turnover in live reef structures than off-reef with regard to accretion-bioerosion processes. Moreover, if the higher variation in growth rates represents a greater variance in (genetic) adaptations to natural environmental variability in the fjord, inshore reefs could possibly benefit under future ocean change compared to offshore reefs. Although not significantly different due to high variances between replicates, growth rates of orange branches were consistently higher at all sites, while mortality was statistically significantly lower, potentially indicating higher stress-resistance than the less pigmented white phenotype. Comparing the here measured rates of net accretion of live corals (regardless of colour morphotype) with net erosion of dead coral framework gives a first estimate of the dimensions of both processes in natural cold-water coral habitats, indicating that calcium carbonate loss through bioerosion amounts to one fifth to one sixth of the production rates by coral calcification (disregarding accretion processes of other organisms and proportion of live and dead coral framework in a reef). With regard to likely accelerating bioerosion and diminishing growth rates of corals under ocean acidification, the balance of reef accretion and degradation may be shifted towards higher biogenic dissolution in the future.

Rapid bioerosion in a tropical upwelling coral reef.

Coral reefs persist in an accretion-erosion balance, which is critical for understanding the natural variability of sediment production, reef accretion, and their effects on the carbonate budget. Bioerosion (i.e. biodegradation of substrate) and encrustation (i.e. calcified overgrowth on substrate) influence the carbonate budget and the ecological functions of coral reefs, by substrate formation/consolidation/erosion, food availability and nutrient cycling. This study investigates settlement succession and carbonate budget change by bioeroding and encrusting calcifying organisms on experimentally deployed coral substrates (skeletal fragments of Stylophora pistillata branches). The substrates were deployed in a marginal coral reef located in the Gulf of Papagayo (Costa Rica, Eastern Tropical Pacific) for four months during the northern winter upwelling period (December 2013 to March 2014), and consecutively sampled after each month. Due to the upwelling environmental conditions within the Eastern Tropical Pacific, this region serves as a natural laboratory to study ecological processes such as bioerosion, which may reflect climate change scenarios. Time-series analyses showed a rapid settlement of bioeroders, particularly of lithophagine bivalves of the genus Lithophaga/Leiosolenus (Dillwyn, 1817), within the first two months of exposure. The observed enhanced calcium carbonate loss of coral substrate (>30%) may influence seawater carbon chemistry. This is evident by measurements of an elevated seawater pH (>8.2) and aragonite saturation state (Ωarag >3) at Matapalo Reef during the upwelling period, when compared to a previous upwelling event observed at a nearby site in distance to a coral reef (Marina Papagayo). Due to the resulting local carbonate buffer effect of the seawater, an influx of atmospheric CO2 into reef waters was observed. Substrates showed no secondary cements in thin-section analyses, despite constant seawater carbonate oversaturation (Ωarag >2.8) during the field experiment. Micro Computerized Tomography (µCT) scans and microcast-embeddings of the substrates revealed that the carbonate loss was primarily due to internal macrobioerosion and an increase in microbioerosion. This study emphasizes the interconnected effects of upwelling and carbonate bioerosion on the reef carbonate budget and the ecological turnovers of carbonate producers in tropical coral reefs under environmental change.

Syn-vivo bioerosion of Nautilus by endo- and epilithic foraminiferans (New Caledonia and Vanuatu).

A variety of syn-vivo bioerosion traces produced by foraminiferans is recorded in shells of Nautilus sampled near New Caledonia and Vanuatu. These are two types of attachment scars of epilithic foraminiferans and two forms of previously undescribed microborings, a spiral-shaped and a dendritic one, both most likely being the work of endolithic 'naked' foraminiferans. Scanning electron microscopy of epoxy-resin casts of the latter revealed that these traces occur in clusters of up to many dozen individuals and potentially are substrate-specific. The foraminiferan traces are the sole signs of bioerosion in the studied Nautilus conchs, and neither traces of phototrophic nor other chemotrophic microendoliths were found. While the complete absence of photoautotrophic endoliths would be in good accordance with the life habit of Nautilus, which resides in aphotic deep marine environments and seeks shallower waters in the photic zone for feeding only during night-time, the absence of any microbial bioerosion may also be explained by an effective defence provided by the nautilid periostracum. Following this line of reasoning, the recorded foraminiferan bioerosion traces in turn would identify their trace makers as being specialized in their ability to penetrate the periostracum barrier and to bioerode the shell of modern Nautilus.

Effects of water depth, seasonal exposure, and substrate orientation on microbial bioerosion in the Ionian Sea (Eastern Mediterranean).

The effects of water depth, seasonal exposure, and substrate orientation on microbioerosion were studied by means of a settlement experiment deployed in 15, 50, 100, and 250 m water depth south-west of the Peloponnese Peninsula (Greece). At each depth, an experimental platform was exposed for a summer period, a winter period, and about an entire year. On the up- and down-facing side of each platform, substrates were fixed to document the succession of bioerosion traces, and to measure variations in bioerosion and accretion rates. In total, 29 different bioerosion traces were recorded revealing a dominance of microborings produced by phototrophic and organotrophic microendoliths, complemented by few macroborings, attachment scars, and grazing traces. The highest bioerosion activity was recorded in 15 m up-facing substrates in the shallow euphotic zone, largely driven by phototrophic cyanobacteria. Towards the chlorophyte-dominated deep euphotic to dysphotic zones and the organotroph-dominated aphotic zone the intensity of bioerosion and the diversity of bioerosion traces strongly decreased. During summer the activity of phototrophs was higher than during winter, which was likely stimulated by enhanced light availability due to more hours of daylight and increased irradiance angles. Stable water column stratification and a resulting nutrient depletion in shallow water led to lower turbidity levels and caused a shift in the photic zonation that was reflected by more phototrophs being active at greater depth. With respect to the subordinate bioerosion activity of organotrophs, fluctuations in temperature and the trophic regime were assumed to be the main seasonal controls. The observed patterns in overall bioeroder distribution and abundance were mirrored by the calculated carbonate budget with bioerosion rates exceeding carbonate accretion rates in shallow water and distinctly higher bioerosion rates at all depths during summer. These findings highlight the relevance of bioerosion and accretion for the carbonate budget of the Ionian Sea.

First glimpse into Lower Jurassic deep-sea biodiversity: in situ diversification and resilience against extinction.

Owing to the assumed lack of deep-sea macrofossils older than the Late Cretaceous, very little is known about the geological history of deep-sea communities, and most inference-based hypotheses argue for repeated recolonizations of the deep sea from shelf habitats following major palaeoceanographic perturbations. We present a fossil deep-sea assemblage of echinoderms, gastropods, brachiopods and ostracods, from the Early Jurassic of the Glasenbach Gorge, Austria, which includes the oldest known representatives of a number of extant deep-sea groups, and thus implies that in situ diversification, in contrast to immigration from shelf habitats, played a much greater role in shaping modern deep-sea biodiversity than previously thought. A comparison with coeval shelf assemblages reveals that, at least in some of the analysed groups, significantly more extant families/superfamilies have endured in the deep sea since the Early Jurassic than in the shelf seas, which suggests that deep-sea biota are more resilient against extinction than shallow-water ones. In addition, a number of extant deep-sea families/superfamilies found in the Glasenbach assemblage lack post-Jurassic shelf occurrences, implying that if there was a complete extinction of the deep-sea fauna followed by replacement from the shelf, it must have happened before the Late Jurassic.

Avoiding coral reef functional collapse requires local and global action.

Coral reefs face multiple anthropogenic threats, from pollution and overfishing to the dual effects of greenhouse gas emissions: rising sea temperature and ocean acidification. While the abundance of coral has declined in recent decades, the implications for humanity are difficult to quantify because they depend on ecosystem function rather than the corals themselves. Most reef functions and ecosystem services are founded on the ability of reefs to maintain their three-dimensional structure through net carbonate accumulation. Coral growth only constitutes part of a reef's carbonate budget; bioerosion processes are influential in determining the balance between net structural growth and disintegration. Here, we combine ecological models with carbonate budgets and drive the dynamics of Caribbean reefs with the latest generation of climate models. Budget reconstructions using documented ecological perturbations drive shallow (6-10 m) Caribbean forereefs toward an increasingly fragile carbonate balance. We then projected carbonate budgets toward 2080 and contrasted the benefits of local conservation and global action on climate change. Local management of fisheries (specifically, no-take marine reserves) and the watershed can delay reef loss by at least a decade under "business-as-usual" rises in greenhouse gas emissions. However, local action must be combined with a low-carbon economy to prevent degradation of reef structures and associated ecosystem services.

Ocean acidification accelerates reef bioerosion.

In the recent discussion how biotic systems may react to ocean acidification caused by the rapid rise in carbon dioxide partial pressure (pCO(2)) in the marine realm, substantial research is devoted to calcifiers such as stony corals. The antagonistic process - biologically induced carbonate dissolution via bioerosion - has largely been neglected. Unlike skeletal growth, we expect bioerosion by chemical means to be facilitated in a high-CO(2) world. This study focuses on one of the most detrimental bioeroders, the sponge Cliona orientalis, which attacks and kills live corals on Australia's Great Barrier Reef. Experimental exposure to lowered and elevated levels of pCO(2) confirms a significant enforcement of the sponges' bioerosion capacity with increasing pCO(2) under more acidic conditions. Considering the substantial contribution of sponges to carbonate bioerosion, this finding implies that tropical reef ecosystems are facing the combined effects of weakened coral calcification and accelerated bioerosion, resulting in critical pressure on the dynamic balance between biogenic carbonate build-up and degradation.