Patterns of magnesium content in Arctic bryozoan skeletons along a depth gradient

A growing body of evidence suggests that ocean acidification acting synergistically with ocean warming alters carbonate biomineralization in a variety of marine biota. Magnesium often substitutes for Ca in the calcite skeletons of marine invertebrates, increasing their solubility. The spatio-environmental distribution of Mg in marine invertebrates has seldom been studied, despite its importance for assessing vulnerabilities to ocean acidification. Because pH decreases with water depth, it is predicted that levels of Mg in calcite skeletons should also decrease to counteract dissolution. Such a pattern has been suggested by evidence from echinoderms. Data on magnesium content and depth in Arctic bryozoans (52 species, 103 individuals, 150 samples) are here used to test this prediction, aided by comparison with six conceptual models explaining all possible scenarios. Analyses were based on a uniform dataset spanning more than 200 m of coastal water depth. No significant relationship was found between depth and Mg content; indeed, the highest Mg content among the analyzed taxa (8.7 % mol MgCO₃) was recorded from the deepest settings (>200 m). Our findings contrast with previously published results from echinoderms in which Mg was found to decrease with depth. The bryozoan results suggest that ocean acidification may have less impact on the studied bryozoans than is generally assumed. In the broad context, our study exemplifies quantitative testing of spatial patterns of skeletal geochemistry for predicting the biological effects of environmental change in the oceans.

The ecological effect of CO2 on the brown algae Fucus serratus and its epibionts: from the habitat to the organismic scale

Carbon dioxide plays a central role in the functioning of organisms and ecosystems. For autotrophs, it is the substrate for photosynthesis while for heterotrophs it is a waste product of respiration. For two centuries Human activities, are responsible for an increase from 280 to 380 μatm of the atmospheric pCO2. A further increase up to 1000 μatm is predicted for the 21th century. The ocean surface and the atmosphere are at the equilibrium for CO2. The CO2 dissolving in seawater reduces the pH and increase of corrosiveness of water for shells and skeletons made of calcium carbonates. Thus, this process of ocean acidification is expected to have detrimental effects on calcifying organism. On the contrary, marine autotrophs are supposed to (slightly) benefit from this extra supply of CO2. In this thesis, we aimed at assessing the influence of CO2 on members of the nearshore macrophytes meadows of the Baltic Sea, an ecosystem naturally exposed to elevated water acidity. In a first part, we investigated the natural variations of the carbonate system in a meadow during three weeks of July, August, and September 2011 in a sheltered bay of the Western Baltic. We observed important day night dynamics together with wider scale variations (days to weeks) of magnitude exceeding future climate change predictions. We were able to explain the variations by the action of light and wind speed and direction. Light drives the uptake and release of carbon by photosynthesis and respiration of the meadow and wind influences the upwelling of offshore hypercapnic seawater. In a second part, we investigated the growth response to elevated pCO2 of one of the main primary producer of the meadows, the brown algae Fucus serratus, in laboratory experiments. The algae were incubated under ambient pCO2, actual upwelling pCO2 and future upwelling pCO2. We observed an increase of growth of 20 % at the pCO2 expected for the year 2100 and up to 50 % at pCO2 possibly occurring during future upwelling events (4000 μatm). However, the effect was transient and a limitation of growth by nutrients occurred after about 20 days. In the third part, we tested the effect of at the same three pCO2 on the growth and recruitment of the main members of the sessile associated communities of Fucus serratus: the calcifying and non-calcifying bryozoan Electra pilosa and Alcyonidium hirsutum and the calcifying tubeworm Spirorbis spirorbis. We tested the hypothesis of greater sensitivity of calcifyers to acidification and found a resistance of all the tested organisms to the future ambient pCO2. In contrast, at the highest pCO2 tested (future upwelling), we observed in Spirorbis severe shell corrosion, reduction of growth and collapse of recruitment. The growth rates of the worm settlings were assessed at light and dark under the three experimental pCO2. A 40 % enhancement of growth was observed at light at any pCO2, possibly due to the algal photosynthetic reduction of pCO2 / increase of pH in the boundary layer surrounding the algal thallus. Our study illustrates the possibility of facilitation between species to resist ocean acidification.

Benthic invertebrates in a high-CO2 world

Ocean acidification (OA), whereby increases in atmospheric carbon dioxide (cO2) over the past 200 years have led to a decline in the pH and carbonate ion availability of the oceans, has emerged as one of the major drivers of twenty- first century marine scientific research. Here we describe the current understanding of OA effects on benthic marine invertebrates, in particular the calcifiers thought to be most sensitive to altered carbonate chemistry. We describe the responses of benthic invertebrates to OA conditions predicted up to the end of the century, examining individual organism response through to ecosystem- level impacts. Research over the past decade has found great variability in the physiological and functional response of different species and communities to OA, with further variability evident between life stages. Over both geological and recent timescales, the presence and calcification rates of marine calcifiers have been inextricably linked to the carbon chemistry of the oceans. Under short-term experimentally enhanced cO2 conditions, many organisms have shown trade-offs in their physiological responses, such as reductions in calcification rate and reproductive output. In addition, carry-over effects from fertilization, larval and juvenile stages, such as enhanced development time and morphological changes, highlight the need for broad- scale studies over multiple life stages. These organism- level responses may propagate through to altered benthic communities under naturally enhanced cO2 conditions, evident in studies of upwelling regions and at shallow- water volcanic cO2 vents. Only by establishing which benthic invertebrates have the ability to acclimate or adapt, via natural selection, to changes from OA, in combination with other environmental stressors, can we begin to predict the consequences of future climate change for these communities.

Effects of ocean acidification on growth, organic tissue and protein profile of the Mediterranean ­bryo­zoan Myriapora truncata

The possible effects of ocean acidification on growth, organic tissue and protein profile in the bryozoan Myriapora truncata (Pallas, 1766) were studied in samples transplanted along a gradient of different pH conditions in an area of natural volcanic CO₂ vents at Ischia Island (Tyrrhenian Sea, Italy). Living colonies from normal (mean pH 8.10), intermediate (pH 7.83) and low (pH 7.32) pH sites were investigated after intervals of 34, 57 and 87 d of exposure. M. truncata formed new and complete zooids at the normal site, whereas at the intermediate and low pH sites, neither partial nor complete zooids were produced. After 34 d at intermediate and low pH conditions, the organic cuticle which envelops the skeleton increased in thickness when compared to normal colonies, suggesting a protective role against dissolution of the high-Mg calcite skeleton. Significant changes in the protein profile and expression displayed by samples from intermediate and low pH conditions suggest that M. truncata makes an initial attempt to overcome the decrease in pH by up-regulating protein production but eventually, especially in the lowest pH condition, exhausts biochemical energy to maintain this rate of protein production, leading to eventual death.

Skeletal alterations and polymorphism in a Mediterranean bryozoan at natural CO2 vents

Colonies of the cheilostome bryozoan Schizoporella errata were grown at a site near Ischia Island (Tyrrhenian Sea, Italy) where volcanogenic CO₂ emissions lower seawater pH to 7.76, simulating levels of ocean acidification predicted for the end of the present century. Compared with colonies from a control site (mean pH = 8.09), putative defensive polymorphs (avicularia) were significantly fewer, and retarded growth of zooidal basal and lateral walls was evident at the low pH site. The lower proportion of avicularia suggests a switch in resource allocation away from defence to favouring rapid growth. In addition, corrosion of the skeleton was observed in both new and old zooids at the low pH site, and feeding zooids were slightly smaller but had larger orifices for the protrusion of feeding lophophores. These findings corroborate previous studies demonstrating potential dissolution of carbonate skeletons in low pH seawater, while providing new insight into the possible ability of colonial species to respond to ocean acidification by adjusting resource allocation between zooids of different types.

Growing up in the temperate zone: Age, growth, calcification and carbonate mineralogy of Melicerita chathamensis (Bryozoa) in southern New Zealand

The cheilostome bryozoan Melicerita chathamensis from the continental shelf around southern New Zealand is unusual in having macroscopic annual growth checks. It thus presents an opportunity to examine annual variations in age, growth, calcification and carbonate mineralogy in a temperate bryozoan. Forty-one colonies dredged south of Snares Islands, New Zealand (47° 49.537′S, 166° 45.910′E, 166 m water depth, 2 February 2008) ranged from 2 to 9 years old and were up to 40 mm long. Segment length varied from 0.94 to 13.67 mm, with a mean growth rate of 5.27 mm yr^− 1, whereas segment weight varied from 0.1 to 37 mg, with an average calcification rate of 9.2 mg yr^− 1. Low-Mg calcite ranged from 0.8 to 3.6 wt.% MgCO₃, with a mean of 2.1 wt.% MgCO₃, whereas high-Mg calcite ranged from 6.6 wt.% MgCO₃ to 9.7 wt.% MgCO₃ with a mean of 8.1 wt.% MgCO₃. The well-studied polar Melicerita obliqua, in contrast, grows more slowly over a much longer period and calcifies more rapidly, suggesting that polar bryozoans may be more effective at sequestering carbon than their temperate counterparts. The proportion of each mineral in skeletal segments generally varied with age, from almost entirely high-Mg calcite in the oldest segments to entirely low-Mg calcite at the growing tips, with a mean of 60.7% high-Mg calcite. This unusual dual-calcite mineralogy appears to be analogous to some other cheilostomes which also produce a primary skeleton of low-Mg calcite but their secondary mineral is aragonite. Such bimineralic bryozoans, which are sophisticated mineralisers that exert a great deal of control over their skeletal composition, may be able to mineralise despite decreasing sea-water pH. Bimineral skeletal sediments, however, could be especially vulnerable to dissolution, as both aragonite and high-Mg calcite are more soluble than low-Mg calcite. Weakening of the skeleton by dissolution of secondary thickening could increase the likely effects of temperate abrasion and bioerosion.

Will variation among genetic individuals influence species responses to global climate change?

Increased anthropogenic CO2 emissions in the last two centuries have lead to rising sea surface temperature and falling ocean pH, and it is predicted that current global trends will worsen over the next few decades. There is limited understanding of how genetic variation among individuals will influence the responses of populations and species to these changes. A microcosm system was set up to study the effects of predicted temperature and CO2 levels on the bryozoan Celleporella hyalina. In this marine species, colonies grow by the addition of male, female and feeding modular individuals (zooids) and can be physically subdivided to produce a clone of genetically identical colonies. We studied colony growth rate (the addition of zooids), reproductive investment (the ratio of sexual to feeding zooids) and sex ratio (male to female zooids) in four genetically distinct clonal lines. There was a significant effect of clone on growth rate, reproductive investment and sex ratio, with clones showing contrasting responses to the various temperature and pH combinations. Overall, decreasing pH and increasing temperature caused reduction of growth, and eventual cessation of growth was often observed at the highest temperature, especially during the latter half of the 15-day trials. Reproductive investment increased with increasing temperature and decreasing pH, varying more widely with temperature at the lowest pH. The increased production of males, a general stress response of the bryozoan, was seen upon exposure to reduced pH, but was not expressed at the highest temperature tested, presumably due to the frequent cessation of growth. Further to the significant effect of pH on the measured whole-colony parameters, observation by scanning electron microscopy revealed surface pitting of the calcified exoskeleton in colonies that were exposed to increased acidity. Studying ecologically relevant processes of growth and reproduction, we demonstrate the existence of relevant levels of variation among genetic individuals which may enable future adaptation via non-mutational natural selection to falling pH and rising temperature.

Structural and geochemical alterations in the Mg calcite bryozoan Myriapora truncata under elevated seawater pCO2 simulating ocean acidification

The possible effects of ocean acidification on the calcareous skeleton of the Mediterranean bryozoan Myriapora truncata (Pallas, 1766) were studied by transplanting live and dead colonies into an area of natural volcanic CO2 vents at Ischia (Gulf of Naples, Tyrrhenian Sea), Italy. Morphology and geochemistry were compared between colonies from normal (mean pH = 8.07, min. pH 7.95), below-normal (mean pH 7.66, min. pH 7.32) and acidic (mean pH 7.43, min. pH 6.83) conditions after colonies had been exposed in situ for 45 and 128 days. Both distal (juvenile) and proximal (adult) parts of the branches were investigated. Skeletons of live colonies in acidic pH site after 45 days of exposure were less corroded than those of dead colonies, suggesting that the organic tissues enveloping the skeleton play a protective role. Colonies remained alive at the below-normal and acidic pH sites during the 45-day experiment but corrosion was very striking after 128 days, with colonies from the acidic site showing significant loss of skeleton. Compared to the control, these colonies also had lower levels of Mg (mean 8 versus 9.5 wt% Mg) within their skeletons. Electron microprobe mapping showed Mg to be higher in the outer layers of the skeletal walls in colonies from the normal pH site. Corrosion of outer layers of the walls probably explains the lower Mg level found in colonies exposed to acidic conditions. As solubility of calcite increases with Mg content, the enrichment of Mg in outer layers of the skeleton should enhance the vulnerability of Myriapora truncata to dissolution. These findings raise concerns over the survival of bryozoans with Mg calcite skeletons in the face of predicted decreases in oceanic pH levels.

Growing up in the temperate zone: Age, growth, calcification and carbonate mineralogy of Melicerita chathamensis (Bryozoa) in southern New Zealand

The cheilostome bryozoan Melicerita chathamensis from the continental shelf around southern New Zealand is unusual in having macroscopic annual growth checks. It thus presents an opportunity to examine annual variations in age, growth, calcification and carbonate mineralogy in a temperate bryozoan. Forty-one colonies dredged south of Snares Islands, New Zealand (47° 49.537′S, 166° 45.910′E, 166 m water depth, 2 February 2008) ranged from 2 to 9 years old and were up to 40 mm long. Segment length varied from 0.94 to 13.67 mm, with a mean growth rate of 5.27 mm y^-1, whereas segment weight varied from 0.1 to 37 mg, with an average calcification rate of 9.2 mg y^-1. Low-Mg calcite ranged from 0.8 to 3.6 wt% MgCO₃, with a mean of 2.1 wt% MgCO₃, whereas high-Mg calcite ranged from 6.6 wt% MgCO₃ to 9.7 wt% MgCO₃ with a mean of 8.1 wt% MgCO₃. The well-studied polar M. obliqua, in contrast, grows more slowly over a much longer period and calcifies more rapidly, suggesting that polar bryozoans may be more effective at sequestering carbon than their temperate counterparts. The proportion of each mineral in skeletal segments generally varied with age, from almost entirely high-Mg calcite in the oldest segments to entirely low-Mg calcite at the growing tips, with a mean of 60.7% high Mg calcite. This unusual dual-calcite mineralogy appears to be analogous to some other cheilostomes which also produce a primary skeleton of low-Mg calcite but their secondary mineral is aragonite. Such bimineralic bryozoans, which are sophisticated mineralisers that exert a great deal of control over their skeletal composition, may be able to mineralise despite decreasing sea-water pH. Bimineral skeletal sediments, however, could be especially vulnerable to dissolution, as both aragonite and high-Mg calcite are more soluble than low-Mg calcite. Weakening of the skeleton by dissolution of secondary thickening could increase the likely effects of temperate abrasion and bioerosion.

Understanding a bimineralic bryozoan: Skeletal structure and carbonate mineralogy of Odontionella cyclops (Foveolariidae: Cheilostomata: Bryozoa) in New Zealand

Skeletal carbonate mineralogy of the
bryozoan Odontionella cyclops (Busk, 1854) (family Foveolariidae)
is extremely variable, with calcite:aragonite ratio ranging from 27 to
100 wt% calcite (mean = 57 wt% calcite, sd = 15, n = 118), and Mg
content in calcite varying from 3.6 to 8.8 wt% MgCO₃
(mean = 6.2 wt% MgCO₃, sd = 1.1, n = 118). This study
examines the sources of this wide variability and the possible effects
of ocean acidification on bimineral invertebrates. Variation in
calcite:aragonite ratio in O. cyclops is neither environmental
nor related to colonial growth form, but appears to be astogenetic.
Primary calcification of the zooecial ‘box’ is all calcite, followed by
progressive construction of a secondary aragonitic superstructure which
includes avicularia. Consequently, young parts of the colony are
dominated by calcite, with increasing amounts of aragonite with age.
Very old parts of the colony may have the aragonite eroded or chipped
away to become again entirely calcitic. In contrast with many other
bryozoans that are entirely calcitic or mainly aragonitic, this
bipartite structure may result in increased vulnerability to ocean
acidification. Given the southern-temperate shelf-to-slope distribution
of this species, O. cyclops (and others like it) will begin to be
subjected to decreasing pH in only a few decades. The consequence could
be a modern sediment assemblage similar to a diagenetically-altered
fossil assemblage – missing aragonitic skeletal parts and species.