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- Mesophotic coral ecosystems in the Eastern Tropical Pacific: the current state of knowledge and the spatial variability of their depth boundariesPublication . Pérez-Castro, Miguel Ángel; Schubert, Nadine; Ang-Montes de Oca, Gabriela; Leyte-Morales, Gerardo Esteban; Eyal, Gal; Hinojosa-Arango, GustavoIn the Eastern Tropical Pacific (ETP), Mesophotic Coral Ecosystems (MCEs) are limited by oceanographic conditions and are thought to be mostly absent. However, considering the currently discussed more flexible approach to define mesophotic boundaries, based on light availability, we performed a systematic search to assess their current state of knowledge. Using MODIS-Aqua satellite data (Kd490), we calculated the mesophotic boundaries in the ETP, based on optical depths, and performed a bibliographic search of studies carried out at those depths, including those present in turbid waters with KdPAR values up to 0.2 m-1. Seventy-seven papers on MCEs research were compiled in this review, recording a total of 138 species. The studies focus almost exclusively on taxonomy, ecosystem function, and reviews, indicating the need for future research regarding aspects, such as structuring environmental variables, molecular ecology, and natural resource management. Furthermore, remote sensing data show that there exists a high spatial variability of water transparency in the ETP, resulting in significant differences in KdPAR between oceanic and continental locations, mostly related to the occurrence of seasonal upwelling in the latter. Based on KdPAR, we estimated the mesophotic depth boundaries (z10%, z1%, z0.1%) for specific locations within the ETP and found that MCEs can potentially occur as shallow as 13-15 m in coastal regions. Also, we compared the calculated boundaries with the respective deepest records of lightdependent corals. With one exception, the presence of the corals was restricted to the upper mesophotic subzone (z10%-z1%), which agrees with reports for other regions, showing that light availability is one of the main drivers for the bathymetric distribution of MCEs and can be used as a first approach to identify their potential presence, though other local factors (e.g., geomorphology, temperature, internal waves) should also be considered, as they can cause shifts in depth limits.
- Trophic ecology of Caribbean octocorals: autotrophic and heterotrophic seasonal trendsPublication . Rossi, Sergio; Schubert, Nadine; Brown, Darren; Gonzalez-Posada, Alba; Soares, Marcelo O.Studies over the past decades indicate that octocorals are becoming the dominant group in some areas of the Caribbean. Yet, basic knowledge about the trophic ecology of these organisms and their seasonal and species-specific variability is still scarce, though this might play a key role in determining their importance in benthic-pelagic coupling processes and, consequently, their role in carbon cycles. In the present study, two Caribbean gorgonian species (Plexaurella nutans and Pterogorgia anceps) were studied during an annual cycle, to assess seasonal variations in their reliance on heterotrophic versus autotrophic energy inputs. Zooplankton capture rates and bulk tissue stable isotopes were measured on a monthly basis to assess heterotrophic energy input, while autotrophic contribution was quantified monthly by Symbiodiniaceae cell densities and pigment contents, accompanied by seasonal measurements on Symbiodiniaceae (Breviolum sp.) photosynthetic performance and host respiratory demand. The results show that while autotrophy was the main energy source for both species, there was also a non-neglectable input through zooplankton that accounted for 0.2-0.8% and 0.7-3.4% of the energy demands in P. nutans and P. anceps, respectively. Our data further demonstrate that there are species-specific and seasonal differences in the contributions of these two nutrition modes, though there is no indication of shifts in the predominant mode during the year in either species. The energy inputs resulted in a positive energy balance throughout the year, with an energy surplus available for somatic growth, gonads, and/or energy reserves (e.g., lipids). However, the seasonal patterns differed between species, a feature that is most likely related to the different reproduction periods of the octocorals. Altogether, the information gathered here serves for a better understanding of the trophic ecology of mixotrophic octocorals and the seasonal variability of the nutritional modes that will define their potential impact in the carbon cycle and benthic-pelagic coupling processes of coral reefs.
- Levelling-up rhodolith-bed science to address global-scale conservation challengesPublication . Tuya, Fernando; Schubert, Nadine; Aguirre, Julio; Basso, Daniela; Bastos, Eduardo O.; Berchez, Flávio; Bernardino, Angelo F.; Bosch, Néstor E.; Burdett, Heidi L.; Espino, Fernando; Fernández-Gárcia, Cindy; Francini-Filho, Ronaldo B.; Gagnon, Patrick; Hall-Spencer, Jason M.; Haroun, Ricardo; Hofmann, Laurie C.; Horta, Paulo A.; Kamenos, Nicholas A.; Le Gall, Line; Magris, Rafael A.; Martin, Sophie; Nelson, Wendy A.; Neves, Pedro; Olivé, Irene; Otero-Ferrer, Francisco; Peña, Viviana; Pereira-Filho, Guilherme H.; Ragazzola, Federica; Rebelo, Ana Cristina; Ribeiro, Cláudia; Rinde, Eli; Schoenrock, Kathryn; Silva, João; Sissini, Marina N.; Tâmega, Frederico T. S.Global marine conservation remains fractured by an imbalance in research efforts and policy actions, limiting progression towards sustainability. Rhodolith beds represent a prime example, as they have ecological importance on a global scale, provide a wealth of ecosystem functions and services, including biodiversity provision and potential climate change mit-igation, but remain disproportionately understudied, compared to other coastal ecosystems (tropical coral reefs, kelp for-ests, mangroves, seagrasses). Although rhodolith beds have gained some recognition, as important and sensitive habitats at national/regional levels during the last decade, there is still a notable lack of information and, consequently, specific conservation efforts. We argue that the lack of information about these habitats, and the significant ecosystem services they provide, is hindering the development of effective conservation measures and limiting wider marine conservation success. This is becoming a pressing issue, considering the multiple severe pressures and threats these habitats are exposed to (e.g., pollution, fishing activities, climate change), which may lead to an erosion of their ecological function and eco-system services. By synthesizing the current knowledge, we provide arguments to highlight the importance and urgency of levelling-up research efforts focused on rhodolith beds, combating rhodolith bed degradation and avoiding the loss of associated biodiversity, thus ensuring the sustainability of future conservation programs.
- Multi-level phenotypic plasticity and the persistence of seagrasses along environmental gradients in a subtropical lagoonPublication . Bercovich, Manuel Vivanco; Schubert, Nadine; Almeida Saa, Antonella C.; Silva, Joao; Horta, Paulo A.As seagrasses decline worldwide, determining their phenotypic variability in response to human altered environmental factors becomes important to better understand their acclimation strategies. Many studies have reported seagrass responses to environmental gradients of single parameters, using either single or multiple metrics. However, studies of species' phenotypic variations along environmental gradients that include several environmental factors are rather scarce. In this study, we evaluated and compared the responses of Halodule wrightii and Ruppia maritima at different organizational levels (meadow/shoot, leaf and biochemical level) to key environmental factors, such as urbanization, light availability, salinity and sediment characteristics in a subtropical Brazilian coastal lagoon. Both species tolerated the variable environmental conditions across the lagoon, but showed species-specific differences in the adjustments at certain organizational levels. Halodule wrightii, an opportunistic species, expressed phenotypic responses mostly at the meadows/shoot and biochemical level, while the colonizer R. maritima exhibited phenotypic variability mostly constrained to the biochemical level. Also, determinations on a few selected meadows showed species-specific photosynthetic responses to environmental conditions. These differences might be related to the species' life history, with R. maritima performing adjustments at organizational levels with a fast response time, while the longer life span of H. wrightii makes also investments in modifications at the shoot and meadow level useful. Thus, this study demonstrates differences in seagrass acclimation strategies in response to environmental variability and, as a first study in this region, it also provides useful baseline data that will allow detecting potential changes and/or deterioration of the habitat.
- Unraveling interactions: do temperature and competition with native species affect the performance of the non-indigenous sun coral Tubastraea coccinea?Publication . Almeida Saa, Antonella C.; Crivellaro, Marcelo S.; Winter, Bruna B.; Pereira, Grazyelle R.; Bercovich, Manuel Vivanco; Horta, Paulo A.; Bastos, Eduardo O.; Schubert, NadineThe impact of invasive species has been increasing in recent decades due to globalization, threatening marine biodiversity. Tubastraea spp. (sun corals) have been spreading worldwide, showing rapid increases in abundance and/or spatial occupancy and adverse effects on recipient native ecosystems. In Brazil, they have become major invaders, extending discontinuously for more than 3000 km along the coast. Despite increased research efforts on sun coral ecology/biology over the last decade, information about the species' environmental tolerance and interactions with native species is still scarce. In this context, temperature may be an important driver, as it affects species interactions, primarily through its influence on organismal physiology. Thus, in the present study we assessed the effects of temperature in the invasive T. coccinea and the native zoanthid Palythoa caribaeorum, as well as on their interactions, via a 3-week mesocosm experiment, exposing the species (individually and grafted together) to a temperature range of 16-31 degrees C. This was accompanied by measuring key physiological traits (metabolism, growth, feeding rates and competitive behavior) that underlie species performance, and hence, competitive strength. The results showed that at Arvoredo Island, Brazil, currently the southern distribution limit of both species, (1) T. coccinea exhibited limited capacity to adjust to sudden temperature changes, (2) T. coccinea's physical attacks did not affect P. caribaeorum, but induced increased metabolic costs in the former, while triggering increased growth in the latter, leading to eventual overgrowth of the sun coral and (3) that temperature interacted synergistically with the presence of the competitor in both species under high-temperature stress. These findings suggest that T. coccinea's successful invasion is mainly associated with r-selected life-history traits, rather than competitive strength or a high plasticity to temperature changes, and thus, communities with specific native competitors and/or a variable thermal regime may be more resistant to sun coral invasion.
- Photoacclimation strategies in northeastern Atlantic seagrasses: Integrating responses across plant organizational levelsPublication . Schubert, Nadine; Freitas, Cátia; Silva, André; Costa, Monya; Barrote, Isabel; Horta, Paulo A.; Rodrigues, Ana Cláudia; Santos, Rui; Silva, JoãoSeagrasses live in highly variable light environments and adjust to these variations by expressing acclimatory responses at different plant organizational levels (meadow, shoot, leaf and chloroplast level). Yet, comparative studies, to identify species' strategies, and integration of the relative importance of photoacclimatory adjustments at different levels are still missing. The variation in photoacclimatory responses at the chloroplast and leaf level were studied along individual leaves of Cymodocea nodosa, Zostera marina and Z. noltei, including measurements of variable chlorophyll fluorescence, photosynthesis, photoprotective capacities, non-photochemical quenching and D1-protein repair, and assessments of variation in leaf anatomy and chloroplast distribution. Our results show that the slower-growing C. nodosa expressed rather limited physiological and biochemical adjustments in response to light availability, while both species of faster-growing Zostera showed high variability along the leaves. In contrast, the inverse pattern was found for leaf anatomical adjustments in response to light availability, which were more pronounced in C. nodosa. This integrative plant organizational level approach shows that seagrasses differ in their photoacclimatory strategies and that these are linked to the species' life history strategies, information that will be critical for predicting the responses of seagrasses to disturbances and to accordingly develop adequate management strategies.
- Changes of energy fluxes in marine animal forests of the Anthropocene: factors shaping the future seascapePublication . Rossi, Sergio; Isla, Enrique; Bosch-Belmar, Mar; Galli, Giovanni; Gori, Andrea; Gristina, Michele; Ingrosso, Gianmarco; Milisenda, Giacomo; Piraino, Stefano; Rizzo, Lucia; Schubert, Nadine; Soares, Marcelo; Solidoro, Cosimo; Thurstan, Ruth H; Viladrich, Núria; Willis, Trevor J; Ziveri, PatriziaClimate change is already transforming the seascapes of our oceans by changing the energy availability and the metabolic rates of the organisms. Among the ecosystem-engineering species that structure the seascape, marine animal forests (MAFs) are the most widespread. These habitats, mainly composed of suspension feeding organisms, provide structural complexity to the sea floor, analogous to terrestrial forests. Because primary and secondary productivity is responding to different impacts, in particular to the rapid ongoing environmental changes driven by climate change, this paper presents some directions about what could happen to different MAFs depending on these fast changes. Climate change could modify the resistance or resilience of MAFs, potentially making them more sensitive to impacts from anthropic activities (i.e. fisheries and coastal management), and vice versa, direct impacts may amplify climate change constraints in MAFs. Such changes will have knock-on effects on the energy budgets of active and passive suspension feeding organisms, as well as on their phenology, larval nutritional condition, and population viability. How the future seascape will be shaped by the new energy fluxes is a crucial question that has to be urgently addressed to mitigate and adapt to the diverse impacts on natural systems.
- Rhodolith physiology across the atlantic: towards a better mechanistic understanding of Intra- and interspecific differencesPublication . Schubert, Nadine; Peña, Viviana; Salazar, Vinícius W.; Horta, Paulo A.; Neves, Pedro; Ribeiro, Cláudia; Otero-Ferrer, Francisco; Tuya, Fernando; Espino, Fernando; Schoenrock, Kathryn; Hofmann, Laurie C.; Le Gall, Line; Santos, Rui; Silva, JoãoCoralline algae are important components in a large variety of ecosystems. Among them, rhodoliths are a group of free-living coralline red algae that cover extensive coastal areas, from tropical to polar regions. In contrast to other ecosystem engineers, limited research efforts preclude our understanding of their physiology, underlying mechanisms, drivers and potential differences related to species under varying environments. In this study, we investigated the photosynthetic and calcification mechanisms of six Atlantic rhodolith species from different latitudes, as well as intra-specific differences in one species from four locations. Laboratory incubations under varying light levels provided simultaneous photosynthesis- and calcification-irradiance curves, allowing the assessment of inter- and intra-specific differences on the coupling between these two processes. Stable isotope analysis and specific inhibitor experiments were performed to characterize and compare carbon-concentrating mechanisms (CCMs), as well as the involvement of specific ion-transporters for calcification. Our findings showed significant differences in rhodolith physiological mechanisms that were partially driven by local environmental conditions (light, temperature). High variability was found in the coupling between photosynthesis and calcification, in CCM-strategies, and in the importance of specific ion transporters and enzymes involved in calcification. While calcification was strongly correlated with photosynthesis in all species, the strength of this link was species-specific. Calcification was also found to be reliant on hotosynthesis- and light-independent processes. The latter showed a high plasticity in their expression among species, also influenced by the local environment. Overall, our findings demonstrate that (1) rhodolith calcification is a biologically-controlled process and (2) the mechanisms associated with photosynthesis and calcification display a large variability among species, suggesting potential differences not only in their individual, but also community responses to environmental changes, such as climate change.
- Editorial: coralline algae: globally distributed ecosystem engineersPublication . Schubert, Nadine; Schoenrock, Kathryn M.; Aguirre, Julio; Kamenos, Nicholas A.; Silva, João; Horta, Paulo A.; Hofmann, Laurie C.From the early days of phycology, coralline algae (CA) have been considered the most formidable and widely distributed algae (Woelkerling, 1988). They compose an abundant and highly diverse group, divided into geniculate (articulated) and non-geniculate species (crusts and rhodolith/maërl forms). CA are present in almost every coastal ecosystem around the world, from the intertidal to mesophotic zones (Johansen et al., 1981; Steneck, 1986; Foster, 2001). They are important ecosystem engineers that provide hard, three-dimensional substrates for a highly diverse fauna and flora (Nelson, 2009), building habitats like the globally distributed rhodolith (or maërl) beds (Foster, 2001), and the large algal bioconstructions that abound in the Mediterranean (coralligenous assemblages, intertidal rims; Ingrosso et al., 2018). In addition, the CaCO3 precipitation within cell walls leads to a high fossilization potential of CA, which are considered the best fossil record among macrobenthic autotrophs since they first appeared in the Lower Cretaceous (Aguirre et al., 2000). It also makes CA major carbonate producers (van der Heijden and Kamenos, 2015), which, considering their abundance and wide distribution, gives them an important role in oceanic carbon cycling and reef building (Adey, 1998; Chisholm, 2003; Martin et al., 2006; Perry et al., 2008) and makes them a group of significant economic interest (Coletti and Frixa, 2017). Like many other marine ecosystems, CA habitats will be negatively affected by future climate change, e.g., due to reduced CA calcification/growth (Martin andHall-Spencer, 2017; Cornwall et al., 2019) that may eventually lead to ecosystem degradation and reduction of habitat complexity and biodiversity.
- Calcification in free-living coralline algae is strongly influenced by morphology: implications for susceptibility to ocean acidificationPublication . Schubert, Nadine; Hofmann, Laurie C.; Almeida Saá, Antonella C.; Moreira, Anderson Camargo; Arenhart, Rafael Güntzel; Fernandes, Celso Peres; de Beer, Dirk; Horta, Paulo A.; Silva, JoãoRhodolith beds built by free-living coralline algae are important ecosystems for marine biodiversity and carbonate production. Yet, our mechanistic understanding regarding rhodolith physiology and its drivers is still limited. Using three rhodolith species with different branching morphologies, we investigated the role of morphology in species' physiology and the implications for their susceptibility to ocean acidification (OA). For this, we determined the effects of thallus topography on diffusive boundary layer (DBL) thickness, the associated microscale oxygen and pH dynamics and their relationship with species' metabolic and light and dark calcification rates, as well as species' responses to short-term OA exposure. Our results show that rhodolith branching creates low-flow microenvironments that exhibit increasing DBL thickness with increasing branch length. This, together with species' metabolic rates, determined the light-dependent pH dynamics at the algal surface, which in turn dictated species' calcification rates. While these differences did not translate in species-specific responses to short-term OA exposure, the differences in the magnitude of diurnal pH fluctuations (~ 0.1-1.2 pH units) between species suggest potential differences in phenotypic plasticity to OA that may result in different susceptibilities to long-term OA exposure, supporting the general view that species' ecomechanical characteristics must be considered for predicting OA responses.