Recruitment of crustose coralline algae on tiles material for monitoring coral larvae settlement’s consolidators at Nature Reserve Pulau Sempu, East Java, Indonesia

Crustose coralline algae (Corallinophycideae) are red algae that produced calcium carbonate and are well recognized as foundation species in the epipelagic zone of the marine ecosystem. These algae induced settlement juvenile of coral by released chemical cues from bacterial communities on the surface of their colonies. Their extracellular calcium carbonate also can stabilize reef structure that influencing many invertebrate attaches and growth in the seabed. Crustose coralline algae (CCA) have obtained attention because of their distribution and health compromise to increasing seawater temperature, ocean acidification, and pollutant. As a cryptic species in the ecosystem, the presence of CCA recruit sometimes doesn’t have attention, especially on their capability to occupy the empty space. This study aimed to document coverage and number of CCA recruit in two different recruitment tile’s material. The highest CCA percentage of the cover was showed inside surface than others surface in all stations. Light intensity and low sedimentation were suggested as a key factor of success of high coverage. Overall, station higher CCA recruits have shown from Tiga Warna. Low sedimentation and protection from aerial exposure became the main reason for it. No significant difference number of CCA recruits between marble and sandstone in this study. Successful CCA recruitment in this study can give a wide picture that natural recruitment of coral and other reef biodiversity in Southern Malang might be will succeed because of the abundance of coralline algae that support their life history stage.

Historical Connectivity and Demography of the Ferocious Reef Crab, Eriphia ferox (Crustacea; Eriphiidae), Demonstrate That Taoyuan Algal Reef Is an Essential Population Source Along the East Taiwan Strait

The east Taiwan Strait is largely fringed by sandy and muddy habitats. However, a massive algal reef made of crustose coralline algae has been found along the coast off Taoyuan city in northwestern Taiwan. The porous structure of Taoyuan Algal Reef harbors high abundance and diversity in marine organisms, including the ferocious reef crab, Eriphia ferox. Such a pivotal geographic location and unique ecological features make Taoyuan Algal Reef a potential stepping stone connecting biotic reefs in the east Taiwan Strait, South China Sea to the south, and even the high latitude of Japan to the north. In this study, we examined the population connectivity and historical demography of E. ferox by analyzing mitochondrial cytochrome oxidase I (COI) fragments of 317 individuals sampled from 21 localities in the northwestern Pacific. Our analyses of haplotype network and pairwise FST comparisons revealed a lack of phylogeographical structure among E. ferox populations, implying the existence of a migration corridor connecting the South and East China Seas through the east Taiwan Strait. Multiple lines of evidence, including significant values in neutrality tests, unimodally shaped mismatch distributions, and Bayesian skyline plots elucidated the rapid population growth of E. ferox following the sea-level rise after Last Glacial Maximum (ca. 2–10 Ka). Such demographic expansion in E. ferox coincided with the time when Taoyuan Algal Reef started to build up around 7,500 years ago. Coalescent migration analyses further indicated that the large and continuous E. ferox population exclusively found in Datan Algal Reef, the heart of Taoyuan Algal Reef, was a source population exporting migrants both northward and southward to the adjacent populations. The bidirectional gene flow should be attributed to larval dispersal by ocean currents and secondary contact due to historical population expansion. Instead of serving as a stepping stone, our results support that Taoyuan Algal Reef is an essential population source for biotic reef-associated species along the east Taiwan Strait, and highlight the importance of conserving such a unique ecosystem currently threatened by anthropogenic development.

Living in a Fluctuating Environment Increases Tolerance to Marine Heatwaves in the Free-Living Coralline Alga Phymatolithon lusitanicum

Recently, increased attention is being paid to the importance of environmental history in species’ responses to climate-change related stressors, as more variable and heterogeneous environments are expected to select for higher levels of plasticity in species tolerance traits, compared to stable conditions. For example, organisms inhabiting environments with highly fluctuating thermal regimes might be less susceptible to the increasing frequency and intensity of marine heatwaves (MHWs). In this study, we assessed the metabolic and calcification responses of the rhodolith-bed forming Phymatolithon lusitanicum, from a coastal region that is strongly influenced by frequent changes between upwelling and downwelling conditions, to a simulated MHW scenario, with and without prior exposure to a moderate thermal stress. This allowed determining not only the influence of the species’ long-term thermal history on its resilience against MHWs, but also the rhodoliths capacity for short-term thermal stress memory and its importance during posterior MHW-exposure. Our findings indicate that the rhodoliths experienced negative impacts on daily net primary production (DNP) and calcification (DNC) during the MHW. The effect on the former was only temporary at the beginning of the MHW, while DNC was highly impacted, but exhibited a quick recovery after the event, suggesting a high resilience of the species. Furthermore, prior exposure to a moderate temperature increase, such as those occurring frequently in the natural habitat of the species, mitigated the effects of a subsequent MHW on DNP, while promoting a faster recovery of DNC after the event. Thus, our findings (1) support the hypothesis that benthic organisms living in nearshore habitats may benefit from the natural short-term temperature fluctuations in these environments with an increased resistance to MHW impacts and (2) provide first-time evidence for thermally induced stress memory in coralline algae.

Intra-Annual Variation in Mesophotic Benthic Assemblages on the Insular Slope of Southwest Puerto Rico as a Function of Depth and Geomorphology

There is limited information on the intra-annual variability of mesophotic coral ecosystems (MCEs), worldwide. The benthic communities, measured as % cover, of two geomorphologically different mesophotic sites (El Hoyo and Hole-in-the-Wall) were examined during 2009–2010 in southwest Puerto Rico. Depths sampled were 50 and 70 m. At each site/depth combination, two permanent transects, measuring 10-m long by 40-cm wide, were surveyed by successive photoquadrants, 0.24 m2 in area. Scleractinian corals, octocorals, macroalgae, crustose coralline algae (CCA), sponges and unconsolidated sediment were the main components along the transects. Significant community differences were observed both among sites and among depths. Differences among sites were greater at 50 m than at 70 m. The El Hoyo site at 50 m was the most divergent, and this was due to a lower coral and sponge cover and a higher algal cover (Amphiroa spp., Peyssonnelia iridescens, turf) relative to the other site/depth combinations. As a consequence, the differences in community structure with depth were larger at El Hoyo than at Hole-in-the-Wall. The communities at 70 m were distinguished from those at 50 m by the greater proportion of the corals Agaricia undata, Madracis pharensis and CCA, and a reduced cover of the cyanobacterium Schizothrix. Temporal variation in the benthic assemblages was documented throughout the year. For both mesophotic sites, the magnitude of change at 50 m was significantly greater than at 70 m. For both depths, the magnitude of change at El Hoyo was significantly greater than at Hole-in-the-Wall. All assemblages experienced almost the same temporal patterns, despite the differences in species composition across sites and depths. Changes in temporal patterns are driven by an increase in the percent cover of the macroalgae Dictyota spp., and a decrease in the percent cover of non-colonized substrata (sand, pavement or rubble). Relatively rapid, intra-annual changes are dictated by the negative correlation between cyclic Dictyota spp. cover and open substrata cover. Other observed mechanisms for rapid community changes in the photoquadrants were diseases and collapses of substrata along with their associated fauna indicating that small-scale disturbance processes may play an important role within MCEs.

Deep Learning Applied to SEM Images for Supporting Marine Coralline Algae Classification

The classification of coralline algae commonly relies on the morphology of cells and reproductive structures, along with thallus organization, observed through Scanning Electron Microscopy (SEM). Nevertheless, species identification based on morphology often leads to uncertainty, due to their general plasticity. Evolutionary and environmental studies featured coralline algae for their ecological significance in both recent and past Oceans and need to rely on robust taxonomy. Research efforts towards new putative diagnostic tools have recently been focused on cell wall ultrastructure. In this work, we explored a new classification tool for coralline algae, using fine-tuning pretrained Convolutional Neural Networks (CNNs) on SEM images paired to morphological categories, including cell wall ultrastructure. We considered four common Mediterranean species, classified at genus and at the species level (Lithothamnion corallioides, Mesophyllum philippii, Lithophyllum racemus, Lithophyllum pseudoracemus). Our model produced promising results in terms of image classification accuracy given the constraint of a limited dataset and was tested for the identification of two ambiguous samples referred to as L. cf. racemus. Overall, explanatory image analyses suggest a high diagnostic value of calcification patterns, which significantly contributed to class predictions. Thus, CNNs proved to be a valid support to the morphological approach to taxonomy in coralline algae.

A stable ultrastructural pattern despite variable cell size in <i>Lithothamnion corallioides</i>

Recent advances on the mechanism and pattern of calcification in coralline algae led to contradictory conclusions. The evidence of a biologically controlled calcification process, resulting in distinctive patterns at the scale of family, was observed. However, the coralline calcification process has been also interpreted as biologically induced because of the dependency of its elemental composition on environmental variables. To clarify the matter, five collections of Lithothamnion corallioides from the Atlantic Ocean and the Mediterranean Sea, across a wide depth range (12–66 m), have been analyzed for morphology, anatomy and cell wall crystal patterns in both perithallial and epithallial cells to detect possible ultrastructural changes. L. corallioides shows the alternation of tiers of short-squared and long-ovoid/rectangular cells along the perithallus, forming a typical banding. The perithallial cell length decreases according to water depth and growth rate, whereas the diameter remains constant. Our observations confirm that both epithallial and perithallial cells show primary (PW) and secondary (SW) calcite walls. Rectangular tiles, with the long axis parallel to the cell membrane forming a multi-layered structure, characterize the PW. Flattened squared bricks characterize the SW, with roundish outlines enveloping the cell and showing a zigzag and cross orientation. Long and short cells have different thicknesses of PW and SW, increasing in short cells. Epithallial cells are one to three flared cells with the same shape of the PW and SW crystals. Despite the diverse seafloor environments and the variable L. corallioides growth rate, the cell walls maintain a consistent ultrastructural pattern with unaffected crystal shape and arrangement. A comparison with two congeneric species, L. minervae and L. valens, showed similar ultrastructural patterns in the SW but evident differences in the PW crystal shape. Our observations point to a biologically control rather than an induction of the calcification process in coralline algae and suggest a possible new morphological diagnostic tool for species identification, with relevant importance for paleontological applications. Finally, secondary calcite, in the form of dogtooth crystals that fill the cell lumen, has been observed. It represents a form of early alteration in living collections which can have implications in the reliability of climate and paleoclimate studies based on geochemical techniques.

Insights into the Migration Routes and Historical Dispersion of Species Surviving the Messinian Crisis: The Case of Patella ulyssiponensis and Epizoic Rhodolith Lithophyllum hibernicum

The genus Patella (Patellogastropoda, Mollusca) is represented by a group of species exclusive to the Northeast Atlantic Ocean (including Macaronesian archipelagos) and Mediterranean Sea. The species Patella ulyssiponensis and Patella aspera are common in European waters, with the first inhabiting continental coast, and the second endemic to Macaronesian archipelagos. However, the acceptance of these two lineages as separate species is still highly debated. The red coralline species algae Lithophyllum hibernicum, distributed from Northeast Atlantic to the Mediterranean, is usually found as epilithic crusts or unattached forms (named rhodolith beds), although it also forms epizoic crusts on other organisms, e.g., shell surfaces. In order to study the historic dispersal and migration routes of the Patella ulyssiponensis-aspera complex, taxonomic, genetic and biogeographic approaches were employed based on haplotype network analyses and estimations for the most common recent ancestor (TMRCA), using Cytochrome Oxydase I. A synonymy for these two species is proposed, with the presence of a shared haplotype between the continental (P. ulyssiponensis) and insular (P. aspera) lineages, and with basis of morphological and nomenclatural data. We propose an evolutionary scenario for its dispersal based on a high haplotype diversity for the Mediterranean regions, indicating its possible survival during the Messinian Salinity Crisis (6–5.3 Mya), followed by a colonization of the Proto-Macaronesian archipelagos. The epizoic association of L. hibernicum on P. ulyssiponensis shell adult surface is recorded in this study, likewise the promotion of settlement conditions provided by these coralline algae to P. ulyssiponensis larvae, may explain the reach of P. ulyssiponensis distribution through rhodolith transportation.

Factors Affecting Coral Recruitment and Calcium Carbonate Accretion Rates on a Central Pacific Coral Reef

<p>Coral recruitment and calcium carbonate (CaCO₃) accretion are fundamental processes that help maintain coral reefs. Many reefs worldwide have experienced degradation, including a decrease in coral cover and biodiversity. Successful coral recruitment helps degraded reefs to recover, while CaCO₃ accretion by early successional benthic organisms maintains the topographic complexity of a coral reef system. It is therefore important to understand the processes that affect coral recruitment and CaCO₃ accretion rates in order to understand how coral reefs recover from disturbances. The aim of this thesis was to determine how biophysical forcing factors affect coral recruitment, calcification and bioerosion on a pristine coral reef. I used artificial settlement tiles to measure coral recruitment and CaCO₃ accretion at ten sites (four on the fore reef, four on the Western Reef Terrace and two at the Entrance Channel) at Palmyra Atoll. Fungia skeletons and pieces of dead coral rock were used to measure bioerosion rates, which were combined with the CaCO₃ accretion rates to obtain a net CaCO₃ budget of the reef substratum. Interactions between coral recruits and other benthic organisms on the settlement tiles were recorded to determine the settlement preferences and competitive strength of coral recruits. The settlement preference of Pocillopora damicornis for divots shaped like steephead and bumphead parrotfish bites marks was determined by adding P. damicornis larvae to a container with a settlement tile with the aforementioned divots. I found that coral recruitment and CaCO₃ accretion are influenced by biophysical forcing factors. Most pocilloporids likely recruit close to their parents while the origin of poritid larvae is much more distant. Pocilloporid recruitment rates were also significantly correlated with the successional stage of the benthic community on the settlement tiles, especially the cover of biofilm and bryozoa. Biofilm and crustose coralline algae (CCA) were preferred as settlement substrata by coral larvae, however both pocilloporids and poritids settled on a large number of different benthic substrata. P. damicornis larvae showed a significant settlement preference for divots shaped like parrotfish bite marks over a flat settlement surface. Coral recruits were good competitors against encrusting algae but were often outcompeted by filamentous and upright algae. Settlement tiles were almost entirely colonised by benthic organisms within three to twelve months of deployment. The mass of CaCO₃ deposited onto the settlement tiles negatively correlated with herbivore grazing pressure on the benthic community. Bioerosion rates within pieces of coral (internal bioerosion) increased over time but overall bioerosion rates (internal and external) rarely exceeded CaCO₃ deposition by CCA. My results show how variability in biophysical forcing factors leads to natural variation in coral recruitment and CaCO₃ accretion. This thesis highlights the importance of measuring herbivore grazing, CCA and turf algae cover to gain a better understanding of reef resilience. I conclude that models constructed for Caribbean reefs may not be suited to predict resilience in Pacific reefs and that within the Pacific, two different kinds of resilience models need to be constructed, one for human-inhabited coral reefs and one for uninhabited coral reefs.</p>