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Map of the study area at the Castello Aragonese (Ischia island, Italy) with location of the 2 transplant sites, one with seawater of normal pH (the control cage = black circle), and one with seawater of low pH (the vent cage = white circle)
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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 pol...
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Context 1
... 90-95% CO 2 , 3-6% N 2 , 0.6-0.8% O 2 , and 0.2-0.8% CH 4 and is emitted at rate of about 1.4 9 10 6 l days -1 at ambient temperature and atmo- spheric pressure ). This vented gas lowers seawater pH from the normal value of *8.17 to as low as 6.57 at the north and south-western sides of Castello Aragonese, off the north-eastern coast of Ischia ( Fig. 2; Hall-Spencer et al. 2008). Archaeological and historical evidence suggests that vent sites were above sea level in the fourth century B.C., but that the region underwent a tectonic lowering (bradyseism) and was flooded by about 130-150 A.D. (de Alteriis and Toscano 2003;Zucco 2003). Thus, at these sites, subsurface vent activity has ...
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... was carried out from 7 June to 8 September 2009 off the northeastern side of Ischia Island (40°43.84 0 N, 13°57.08 0 E). All colonies of S. errata were collected at 1-2 m depth, 1.6 km north of Castello Aragonese (Fig. 2, inset). Colonies were transported to the laboratory and maintained in 20 l flow-through aquaria, with flow at a rate sufficient to replace 50% of the seawater each hour. Only primarily encrusting colonies (some had upright portions) with a diameter of at least 3 cm and newly formed zooids at their edges (which indicated active growth) were ...
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... but preventing the entry of large predators, such as fishes, sea urchins, ophiuroids (Jompa and McCoo 2002;de Caralt et al. 2010). The two cages were transplanted to the southwest side of Castello Aragonese at 3-4 m depth at two sites, one of which had seawater of normal pH (the control cage), and one with seawater of low pH (the vent cage; Fig. ...
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... \ 0.001), significantly increasing with time in the control cage but decreasing in the vent cage during exposure times of more than 34 days (SNK test: 16 = 34 \ 48 = 57 = 87 days) (Fig. 7). Za/Zt was significantly correlated with pH (ANCOVA F = 4.611, P \ 0.05), while temperature had no significant effect on avicularium production (ANCOVA F = 0.052, P [ 0.05) (Tables 1, 2). ...
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In recent years, ocean acidification has gained continuously increasing attention from scientists and a number of stakeholders and has raised serious concerns about its ef-fects on marine organisms and ecosystems. With the increase in interest and the num-ber of scientific investigations of this environmental problem, the number of opinions, 5 ofte...
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... These preliminary results pose interesting questions regarding the plastic potential of the two Antarctic species, already observed in other bryozoan species [74][75][76]. Future in situ studies will be required to evaluate the vulnerability or resilience (i.e., adaptability) of Antarctic bryozoans under the fast-occurring current climate change in polar areas. ...
Among Antarctic bryozoans, some species are able to develop calcitic bioconstructions promoting habitat complexity, but the processes leading to biomineral formation are mostly unknown. The present work investigated three Antarctic bryozoans, from morphological to skeletal features, including the organic matrix associated with the skeleton (SOM). Cellarinella nutti Rogick, 1956 and Reteporella frigida Waters, 1904 were collected in November 2018 from a shallow site (25 m) and Cellarinella njegovanae Rogick, 1956 from a deep site (110 m) at Terra Nova Bay (Ross Sea, Antarctica). Both Cellarinella species showed 5-6 "growth check lines" (gcl) on their laminae. The morphometrical characterization conducted on the growth bands (gb) and zooids, within the band across bands, revealed a variability in length with time (C. nutti: from 4099 µm for gb1 to 1449 µm for gb6; C. njegovanae: from 1974 µm for gb 3 to 7127 µm for gb2). Zooid length varied within gb, from the proximal to the distal part of the bands, but differences also occurred across bands. The shortest zooids (~625 µm) were found at the proximal part and the longest (~1190 µm) in the middle part of the gb in C. nutti, whereas in C. njegovanae the shortest zooids (~660 µm) were found in the distal part and the longest (~1190 µm) in the proximal part of the gb. Micro-CT analyses indicated the ratio of basal zooidal walls (RbwT gcl/gb) ranged from 3.0 to 4.9 in C. nutti and from 2.3 to 5.9 in C. njegovanae, whereas Reteporella frigida did not form any gcl on either side of the colony. Preliminary characterizations of the SOM for the three species evidenced a mixture of proteins and polysaccharides with properties similar to those of better-known biominerals, in terms of quantity and electrophoretic behavior. In addition, a "lectin fingerprint" has been established for the first time in bryozoans, displaying the presence of chitin or chitin-related saccharides. Understanding the complexity of the processes regulating skeleton formation is a key aspect in comprehending the adaptation of bioconstructional ecosystems and the survival of the associated biodiversity under the future ocean.
Citation: Lombardi, C.; Kuklinski, P.; Spirandelli, E.; Bruzzone, G.; Raiteri, G.; Bordone, A.; Mazzoli, C.; López Correa, M.; van Geldern, R.; Plasseraud, L.; et al. Antarctic Bioconstructional Bryozoans from Terra Nova Bay (Ross Sea): Morphology, Skeletal Structures and Biomineralization. Minerals 2023, 13, 246; doi:10.3390/min13020246
... Many species are considered bioindicators for environmental changes, as they often respond faster to environmental and human-mediated pressures [21][22][23]. Because of their calcium carbonate hulls, they are sensitive to ocean acidification [24][25][26] and hold an essential part in fossil records [27]. Some bryozoan species have been reported as habitat-forming organisms playing a pivotal role in promoting biodiversity [24], e.g., by overgrowing P. oceanica shoots and preventing the settlement of other species [28] ( Figure 1D). ...
With its geographically isolated location and geological history, the Mediterranean Sea harbors well-known biodiversity hotspots, such as Posidonia oceanica seagrass meadows. Recently, long-living mats formed by the fleshy red alga Phyllophora crispa have been described to be associated with a high diversity of sessile invertebrates in the Tyrrhenian Sea. One of the key taxa among these sessile invertebrates are bryozoans: their abundance, diversity, and spatial distribution in P. crispa mats represent a gap in scientific knowledge. Thus, we conducted a pilot study on bryozoan assemblages associated with P. crispa mats around Giglio Island (Tuscan Archipelago, Italy) in 2018, followed by a comparative study on four sites distributed around the island in the subsequent year, 2019. We compared these findings to bryozoan abundance and diversity on P. oceanica shoots and leaves during the second expedition. The findings revealed more than 46 families, with a significantly higher number of taxa identified in P. crispa mats (33) than in P. oceanica meadows (29). The Shannon diversity index was similar between P. crispa and P. oceanica shoots, while Pielou’s evenness index was lower in P. crispa mats. The most abundant families reported across all habitats were Crisiidae, Aetidae, and Lichenoporidae; but the most abundant family on P. crispa was Chlidoniidae (Chlidonia pyriformis). The assemblages associated with P. crispa differed among sites, with higher abundances but lower diversity on the exposed southernmost site. The total bryozoan abundance was significantly higher on P. crispa (average 2.83 × 106 ± 1.99 × 106 colonies per m2 seafloor) compared to P. oceanica meadows (average 0.54 × 106 ± 0.34 × 106 colonies per m2 seafloor). Our results show a high diversity of bryozoans on P. crispa thalli compared to P. oceanica meadows, which was consistent throughout the study. These findings confirm the value of the red alga-generated habitat for associated bryozoans and may have implications for future biodiversity assessments and conservation measures.
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... Additionally, the negative correlation between the avicularia density and colonial growth along the sampling moments suggests a trade-off between clonal reproduction and colony defense, demonstrating that while modules can be functionally independent, they are energetically integrated (Burgess et al., 2017;Lidgard et al., 2012). A similar trade-off has already been observed for S. errata, with a switch in resource allocation from defense to colonial growth under low pH conditions (Lombardi, Gambi, Vasapollo, Taylor, & Cocito, 2011). ...
Modular organization provides flexibility for colonial animals to deal with variable and unpredictable environmental conditions since each module has specific tasks within the colony, such as feeding, defending or reproducing. Depending on the selecting pressures, sessile organisms may phenotypically adjust the morphology of each module or modify their density, increasing individual fitness. Here we used the marine bryozoan Schizoporella errata (Cheilostomata, Schizoporellidae) to test how the divergent conditions between two artificial habitats, the location inside a marina (IM) and the external wall of the breakwater (BW), affect colony size and the density of the distinct modules. The density of avicularia and ovicells, modules related to defense and reproduction, respectively, did not differ between habitats. However, colonies growing in the turbulent waters of BW were, in general, larger and had higher density of feeding autozooids than those at IM. Reciprocal transplants of bryozoan clones indicated that trait variation is genotype-dependent but varies according to the environmental conditions at the assigned location. The occurrence of larger colonies with more zooids in BW is probably linked to the easier feeding opportunity offered by the small diffusive boundary layer around the colony at this location. Since in colonial polymorphic organisms each module (zooid) performs a specific function, the phenotypic response is not uniform across colonies, affecting only those modules that are susceptible to variations in the main selective pressures. Understanding the importance of colony-level plasticity is relevant to predict how modularity will contribute to organisms to deal with human-induced environmental changes in coastal habitats.
... This biomineralic species is mainly aragonitic (60 wt%) and has a high content of Mg (12 wt%) in the calcite part of the skeleton. Schizoporella errata is extremely vulnerable to high pCO 2 conditions (Lombardi et al. 2011b) ( Table 2); thus its bioconstructions may be corroded and unable to mineralize under future oceanic conditions (RCP 8.5, IPCC 2014). Calpensia nobilis, widespread in the Mediterranean from 10 to 30 m of depth, is also present in eastern Atlantic southwards along the northwest African coast and northwards to the Gulf of Saint-Malo and the Channel Islands (Zabala 1986;Poluzzi and Coppa 1991). ...
Bryozoan constructions have been present in all major climatic zones of marine ecosystems for the past 450 million years, since the Early Ordovician. Some fossil species possessed large bioconstructional colonies that would have provided habitats for other marine animals and plants, just as similar colonies do at the present day. Today, biogenic calcareous structures vary greatly in size, ranging from a few centimetres to many kilometres, and in complexity, forming composite structures that are distributed globally. Despite the role of bioconstructional bryozoan species in promoting marine biodiversity worldwide, they have been excluded from several protection strategies. Information emerging from the literature provides only a very incomplete picture of the role of bryozoans as bioconstructors at the global level. The ability of bryozoans to form long-lasting carbonate structures makes them important carbonate producers, with a significant role in the carbon cycle. Bryozoan reefs are facing the challenges of climate change, which will be detrimental for some species and their associated biota. Better knowledge of the contribution of bryozoans to the carbon stock and the ecosystem services they provide will be of great importance to ensure their protection and to understand their potential in adaptation strategies under future ocean scenarios.
... Previous studies showed that temperature has effects on zooid size, skeletal growth, biomineral deposition and carbonate production on many species of bryozoans 35,36 . However, some of them showed that only a positive interaction between temperature and pH caused the corrosion of the M. truncata skeleton 31,37 highlighting the need to improve our understanding of the mechanisms behind the physiological responses of P. fascialis to thermal stress. On the other way, although the differences were not significant, we observed higher values of Mg in both species and of aragonite in P. fascialis respectively when the colonies were exposed to high temperatures. ...
... The samples were stored and prepared to be observed with a Scanning Electron Microscope (SEM). Specifically, we selected 3 replicates of 1 × 1 mm 2 per colony and zone, and we registered structural variables such as the density of zooids, ovicells, avicularia, damaged or broken zooids, and the mean area of the primary orifice 29,37 . Moreover, to evaluate the non-lethal effects in the skeletal content, we quantified calcite and Mg content of the calcite (type 1: low-magnesium calcite; type 2: high-magnesium calcite) 54 and aragonite on colonies subjected to thermal stress experiment (25 °C) at the end of the experiment. ...
Marine ecosystems are directly threatened by multiple and interactive human stressors at global and local scales. Hence, it is vital to study biodiversity and ecological patterns through a multi-disciplinary approach, from understanding global diversity patterns to evaluating the ecological responses of species to different impacts in order to protect marine ecosystems. In this thesis, we focused on bryozoans, an abundant group of sessile marine invertebrates distributed worldwide, but generally understudied. Accordingly, in this thesis we provide different approaches to understand discovery and macroecological patterns at global scales, and the response of species to different stressors at local scales, combining the use of open databases, the in situ monitoring of natural populations, experiments in aquaria and the development of restoration techniques. At global scale, in Chapter I we unraveled discovery patterns of fossil and extant bryozoans and showed the highest number of fossil species described, highlighting that the current biodiversity represents only a small proportion of Earth’s past biodiversity. Beyond these differences, both groups showed an increase in the taxonomic effort during the past century. Despite this progress, future projections of discovery patterns of both groups showed a large proportion of species remaining to be discovered by the final of this century. In Chapter II, most of the global diversity patterns of marine sessile groups, including bryozoans, showed a non-unimodal latitudinal pattern with a dip in the number of species at the equator and a higher diversity in the Southern ocean. Moreover, this region will be less affected by global warming at the final of this century. In contrast, our analyses showed that the most sampled region for both marine sessile species and bryozoans was North Temperate Atlantic, highlighting the importance to quantify environmental drivers considering sampling effort biases. For this reason, we tested the effect of using the popular method of rarefaction (ES50) vs the incorporation of a frequency index of sampling effort as co-variate in quantitative models. Despite we obtained the same best predictors for both approaches (depth, nitrate, and SST), the models using the correction of sampling biases through frequency index showed better fitting, encouraging to incorporate this methodology in future studies. Focusing on the Mediterranean Sea, in Chapter 3 we studied the responses of bryozoans to different stressors. First, we showed that two abundant and common bryozoans, Pentapora fascialis and Myriapora truncata, displayed different tolerances to warming through the combination of in situ monitoring and experiments in aquaria. Moreover, in Chapter 4 the in situ monitoring of Pentapora fascialis populations revealed its fast population dynamics, with high recruitment and growth rates, and a high capacity of recovery. Accordingly, we observed an increase in the density of its populations in the Medes Island Marine Reserve since the 1990s. However, we evidenced that diving can impact on the density, recruitment, survival, and size of the colonies, registering lower values in frequented localities. Our results highlight that the over frequentation of divers compromises the future viability of populations, highlighting the need to explore other active management strategies. For this reason, in Chapter 5, we tested and developed different restoration techniques for P. fascialis, focusing on the recruitment enhancement through the installation of recruitment surfaces and the transplantation of adult colonies. The successful results and the affordable and economic cost of tested techniques aim to encourage the managers of Marine Protected Areas to apply similar methodologies. The results presented in this thesis show the importance to combine different approaches to understand the global and local ecological patterns of understudied but abundant groups, such as bryozoans. Our findings enlarge the current ecological knowledge of bryozoans at different scales, and highlight that more effort is needed to protect vulnerable populations.
... Due to the ecological and economic importance of many marine calcifiers (e.g. commercial shellfishing), there has been extensive work examining the potential effects of OA on shell production across a range of taxa [6][7][8][9]. The results of these studies differ, probably due to the complexity and number of variables in biological systems. ...
Ocean acidification threatens many ecologically and economically important marine calcifiers. The increase in shell dissolution under the resulting reduced pH is an important and increasingly recognized threat. The biocomposites that make up calcified hardparts have a range of taxon-specific compositions and microstructures, and it is evident that these may influence susceptibilities to dissolution. Here, we show how dissolution (thickness loss), under both ambient and predicted end-century pH (approx. 7.6), varies between seven different bivalve molluscs and one crustacean biocomposite and investigate how this relates to details of their microstructure and composition. Over 100 days, the dissolution of all microstructures was greater under the lower pH in the end-century conditions. Dissolution of lobster cuticle was greater than that of any bivalve microstructure, despite its calcite mineralogy, showing the importance of other microstructural characteristics besides carbonate polymorph. Organic content had the strongest positive correlation with dissolution when all microstructures were considered, and together with Mg/Ca ratio, explained 80-90% of the variance in dissolution. Organic content, Mg/Ca ratio, crystal density and mineralogy were all required to explain the maximum variance in dissolution within only bivalve microstructures, but still only explained 50-60% of the variation in dissolution.
... These habitats provide various ecosystem services (e.g. food provisioning, recreational diving, research material) ( Paoli et al., 2016; Thierry de Ville ' Avray et al., 2019), yet they are threatened by global ocean warming and acidification (Martin & Gattuso, 2009;Lombardi et al., 2011;Martin et al., 2013;Linares et al., 2015;Rodríguez-Prieto, 2016) and local human activities (e.g. fishing, anchoring or sewage outfalls) (Hong, 1980;Ballesteros, 2006;Balata et al., 2005;Balata et al., 2007). ...
... Alternatively, OA stress may have compromised the structural integrity of spines, enabling higher consumption rates of defended zooids. OA has been shown to negatively affect defensive polymorphs in the bryozoan Schizoporella errata (Lombardi et al. 2011). While prey detection in Corambe may be sensitive to OA, like in other molluscs that have exhibited decreased sensory ability in OA conditions (Manríquez et al. 2013), our experiments did not test for impaired prey detection as Corambe was confined to a small area on top of colonies requiring only short-range detection of prey. ...
Ocean acidification (OA) from increased oceanic CO2 concentrations imposes significant physiological stresses on many calcifying organisms. OA effects on individual organisms may be synergistically amplified or reduced by inter- and intraspecies interactions as they propagate up to population and community levels, altering predictions by studies of cal-cifier responses in isolation. The calcifying colonial bryozoan Membranipora membranacea and the predatory nudibranch Corambe steinbergae comprise a trophic system strongly regulated by predator-induced defensive responses and space limitation, presenting a unique system to investigate OA effects on these regulatory mechanisms at individual and population levels. We experimentally quantified OA effects across a range of pH from 7.0 to 7.9 on growth, calcification, senescence and predator-induced spine formation in Membranipora, with or without waterborne predator cue, and on zooid consumption rates in Corambe at Friday Harbor Laboratories, San Juan Island, WA. Membranipora exhibited maximum growth and calcification at moderately low pH (7.6), and continued spine formation in all pH treatments. Spines reduced Corambe zooid consumption rates, with lower pH weakening this effect. Using a spatially explicit model of colony growth, where colony area serves as a proxy for colony fitness, we assessed the population-level impacts of these experimentally determined individual-level effects in the context of space limitation. The area-based fitness costs associated with defense measured at the individual level led to amplified effects predicted for the population level due to competition. Our coupled experimental and modeling results demonstrate the need to consider population-level processes when assessing ecological responses to stresses from changing environments. © The authors 2018. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are unrestricted. Authors and original publication must be credited.
... Previous studies showed that temperature has effects on zooid size, skeletal growth, biomineral deposition and carbonate production on many species of bryozoans 35,36 . However, some of them showed that only a positive interaction between temperature and pH caused the corrosion of the M. truncata skeleton 31,37 highlighting the need to improve our understanding of the mechanisms behind the physiological responses of P. fascialis to thermal stress. On the other way, although the differences were not significant, we observed higher values of Mg in both species and of aragonite in P. fascialis respectively when the colonies were exposed to high temperatures. ...
... The samples were stored and prepared to be observed with a Scanning Electron Microscope (SEM). Specifically, we selected 3 replicates of 1 × 1 mm 2 per colony and zone, and we registered structural variables such as the density of zooids, ovicells, avicularia, damaged or broken zooids, and the mean area of the primary orifice 29,37 . Moreover, to evaluate the non-lethal effects in the skeletal content, we quantified calcite and Mg content of the calcite (type 1: low-magnesium calcite; type 2: high-magnesium calcite) 54 and aragonite on colonies subjected to thermal stress experiment (25 °C) at the end of the experiment. ...
Climate change threatens the structure and function of marine ecosystems, highlighting the importance of understanding the response of species to changing environmental conditions. However, thermal tolerance determining the vulnerability to warming of many abundant marine species is still poorly understood. In this study, we quantified in the field the effects of a temperature anomaly recorded in the Mediterranean Sea during the summer of 2015 on populations of two common sympatric bryozoans, Myriapora truncata and Pentapora fascialis. Then, we experimentally assessed their thermal tolerances in aquaria as well as different sublethal responses to warming. Differences between species were found in survival patterns in natural populations, P. fascialis showing significantly lower survival rates than M. truncata. The thermotolerance experiments supported field observations: P. fascialis started to show signs of necrosis when the temperature was raised to 25–26 °C and completely died between 28–29 °C, coinciding with the temperature when we observed first signs of necrosis in M. truncata. The results from this study reflect different responses to warming between these two co-occurring species, highlighting the importance of combining multiple approaches to assess the vulnerability of benthic species in a changing climate world.
... For another bryozoan, Schizoporella errata, transplanted from control (pH T 8.09) to a mean pH T of 7.76, growth of the zooidal basal and lateral walls was retarded, and there were fewer avicularia (defensive polymorphs) (Lombardi et al. 2011b). The smaller number of avicularia found in the bryozoans at the low-pH site suggests a change in resource allocation from defence to sustain growth (Lombardi et al. 2011b). ...
... For another bryozoan, Schizoporella errata, transplanted from control (pH T 8.09) to a mean pH T of 7.76, growth of the zooidal basal and lateral walls was retarded, and there were fewer avicularia (defensive polymorphs) (Lombardi et al. 2011b). The smaller number of avicularia found in the bryozoans at the low-pH site suggests a change in resource allocation from defence to sustain growth (Lombardi et al. 2011b). Thus, this species of bryozoan could reallocate resources in response to OA, favouring growth over defence. ...
... This is seen in the reallocation of resources to growth over other functions (e.g. bryozoan Schizoporella errata and several polychaetes species; Lombardi et al. 2011b, Ricevuto et al. 2015a). Thus, we can expect to see an increase in the abundance of smaller-bodied or slower-growing individuals in populations in a future ocean. ...
As the ocean continues to take up carbon dioxide (CO2), it is difficult to predict the future of marine ecosystems. Natural CO2 vent sites, mainly of volcanic origin, that provide a pH gradient are useful as a proxy to investigate ecological effects of ocean acidification. The effects of decreased pH can be assessed at increasing levels of organisation, from the responses of individuals of a species up through populations and communities to whole ecosystems. As a natural laboratory, CO 2 vent sites incorporate a range of environmental factors, such as gradients of nutrients, currents and species interactions that cannot be replicated in the laboratory or mesocosms, with the caveat that some vent systems have confounding factors such as hydrogen sulphide and metals. The first CO 2 vent sites to be investigated in an ocean acidification context were the vents at the Castello Aragonese on the island of Ischia, Italy. The gas released is primarily CO 2 with no evidence of toxic substances. They have been the focus of a wealth of studies, which are reviewed here and in context with research at other vent systems. Investigations of the species that occur along the pH gradients at Ischia show that, as the pH decreases, there is a reduction in calcifying species, reflecting the trends seen at other vent systems and in laboratory studies. The species assemblages at the Castello vents living at near future (2100) ocean acidification conditions (mean pH 7.8), show the resilience of many species to elevated CO \2 , including many calcifying species (e.g. sea urchins, serpulids, bryozoans, foraminifera and corals). These taxa show different physiological and ecological mechanisms for acclimatisation and adaptation to low pH. As the oceans continue to acidify to pH levels <7.8, species assemblages are likely to become dominated by fleshy algae and smaller-bodied, generalist invertebrates. These observations suggest that ocean acidification will result in a simplification of marine food webs and trophic complexity.
