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Marine heatwaves have caused massive mortality in coastal benthic ecosystems, altering community composition. Here, we aim to understand the effects of single and sequential sublethal heatwaves in a temperate benthic ecosystem, investigating their disturbance on various levels of ecological hierarchy, i.e. individual physiology, trophic groups' biomass and ecosystem carbon fluxes. To do so, we performed a near-natural experiment using outdoor benthic mesocosms along spring/summer, where communities were exposed to different thermal regimes: without heatwaves (0HW), with one heatwave (1HW) and with three heatwaves (3HWs). Gastropods were negatively impacted by one single heatwave treatment, but the exposure to three sequential heatwaves caused no response, indicating ecological stress memory. The magnitude of ecosystem carbon fluxes mostly decreased after 1HW, with a marked negative impact on mesograzers' feeding, while the overall intensity of carbon fluxes increased after 3HWs. Consumers' acclimation after the exposure to sequential heatwaves increased grazing activity, representing a threat for the macroalgae biomass. The evaluation of physiological responses and ecological interactions is crucial to interpret variations in community composition and to detect early signs of stress. Our results reveal the spread of heatwave effects along the ecological hierarchical levels, helping to predict the trajectories of ecosystem development.This article is part of the theme issue 'Connected interactions: enriching food web research by spatial and social interactions'.

Climate change is altering the functioning of foundational ecosystems. While the direct effects of warming are expected to influence individual species, the indirect effects of warming on species interactions remain poorly understood. In marine systems, as tropical herbivores undergo poleward range expansion, they may change food web structure and alter the functioning of key habitats. While this process ('tropicalization') has been documented within declining kelp forests, we have a limited understanding of how this process might unfold across other systems. Here we use a network of sites spanning 23° of latitude to explore the effects of increased herbivory (simulated via leaf clipping) on the structure of a foundational marine plant (turtlegrass). By working across its geographic range, we also show how gradients in light, temperature and nutrients modified plant responses. We found that turtlegrass near its northern boundary was increasingly affected (reduced productivity) by herbivory and that this response was driven by latitudinal gradients in light (low insolation at high latitudes). By contrast, low-latitude meadows tolerated herbivory due to high insolation which enhanced plant carbohydrates. We show that as herbivores undergo range expansion, turtlegrass meadows at their northern limit display reduced resilience and may be under threat of ecological collapse., (© 2024. The Author(s), under exclusive licence to Springer Nature Limited.)

Plant microbiomes are known to serve several important functions for their host, and it is therefore important to understand their composition as well as the factors that may influence these microbial communities. The microbiome of Thalassia testudinum has only recently been explored, and studies to-date have primarily focused on characterizing the microbiome of plants in a single region. Here, we present the first characterization of the composition of the microbial communities of T. testudinum across a wide geographical range spanning three distinct regions with varying physicochemical conditions. We collected samples of leaves, roots, sediment, and water from six sites throughout the Atlantic Ocean, Caribbean Sea, and the Gulf of Mexico. We then analyzed these samples using 16S rRNA amplicon sequencing. We found that site and region can influence the microbial communities of T. testudinum , while maintaining a plant-associated core microbiome. A comprehensive comparison of available microbial community data from T. testudinum studies determined a core microbiome composed of 14 ASVs that consisted mostly of the family Rhodobacteraceae. The most abundant genera in the microbial communities included organisms with possible plant-beneficial functions, like plant-growth promoting taxa, disease suppressing taxa, and nitrogen fixers., Competing Interests: LC and VM were employed by International Field Studies, Inc. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision., (Copyright © 2024 Ugarelli, Campbell, Rhoades, Munson, Altieri, Douglass, Heck, Paul, Barry, Christ, Fourqurean, Frazer, Linhardt, Martin, McDonald, Main, Manuel, Marco-Méndez, Reynolds, Rodriguez, Rodriguez Bravo, Sawall, Smith, Wied, Choi and Stingl.)

Global habitat degradation heightens the need to better understand patterns of genetic connectivity and diversity of marine biota across geographical ranges to guide conservation efforts. Corals across the Red Sea are subject to pronounced environmental differences, but studies so far suggest that animal populations are largely connected, excepting evidence for a genetic break between the northern-central and southern regions. Here, we investigated population structure and holobiont assemblage of two common pocilloporid corals, Pocillopora verrucosa and Stylophora pistillata, across the Red Sea. We found little evidence for population differentiation in P. verrucosa, except for the southernmost site. Conversely, S. pistillata exhibited a complex population structure with evidence for within-reef and regional genetic differentiation, in line with differences in their reproductive mode (P. verrucosa is a broadcast spawner and S. pistillata is a brooder). Analysis for genomic loci under positive selection identified 85 sites (18 of which were in coding sequences) that distinguished the southern P. verrucosa population from the remainder of the Red Sea population. By comparison, we found 128 loci (24 of which were residing in coding sequences) in S. pistillata with evidence for local adaptation at various sites. Functional annotation of the underlying proteins revealed putative roles in the response to stress, lipid metabolism, transport, cytoskeletal rearrangement, and ciliary function (among others). Microbial assemblages of both coral species showed pervasive association with microalgal symbionts from the genus Symbiodinium (former clade A) and bacteria from the genus Endozoicomonas that exhibited significant differences according to host genotype and environment. The disparity of population genetic and holobiont assemblage patterns even between closely related species (family Pocilloporidae) highlights the need for multispecies investigations to better understand the role of the environment in shaping evolutionary trajectories. It further emphasizes the importance of networks of reef reserves to achieve conservation of genetic variants critical to the future survival of coral ecosystems., (© 2023 The Authors. Molecular Ecology published by John Wiley & Sons Ltd.)

Coral reefs are declining worldwide primarily because of bleaching and subsequent mortality resulting from thermal stress. Currently, extensive efforts to engage in more holistic research and restoration endeavors have considerably expanded the techniques applied to examine coral samples. Despite such advances, coral bleaching and restoration studies are often conducted within a specific disciplinary focus, where specimens are collected, preserved, and archived in ways that are not always conducive to further downstream analyses by specialists in other disciplines. This approach may prevent the full utilization of unexpended specimens, leading to siloed research, duplicative efforts, unnecessary loss of additional corals to research endeavors, and overall increased costs. A recent US National Science Foundation-sponsored workshop set out to consolidate our collective knowledge across the disciplines of Omics, Physiology, and Microscopy and Imaging regarding the methods used for coral sample collection, preservation, and archiving. Here, we highlight knowledge gaps and propose some simple steps for collecting, preserving, and archiving coral-bleaching specimens that can increase the impact of individual coral bleaching and restoration studies, as well as foster additional analyses and future discoveries through collaboration. Rapid freezing of samples in liquid nitrogen or placing at -80 °C to -20 °C is optimal for most Omics and Physiology studies with a few exceptions; however, freezing samples removes the potential for many Microscopy and Imaging-based analyses due to the alteration of tissue integrity during freezing. For Microscopy and Imaging, samples are best stored in aldehydes. The use of sterile gloves and receptacles during collection supports the downstream analysis of host-associated bacterial and viral communities which are particularly germane to disease and restoration efforts. Across all disciplines, the use of aseptic techniques during collection, preservation, and archiving maximizes the research potential of coral specimens and allows for the greatest number of possible downstream analyses., Competing Interests: Robert J. Toonen is a PeerJ Section Editor. The authors declare that they have no competing interests.

Temperature is a key driver of metabolic rates. So far, we know little about potential physiological adjustments of subtropical corals to seasonal temperature changes (>8°C) that substantially exceed temperature fluctuation experienced by their counterparts in the tropics. This study investigated the effect of temperature reductions on Montastraea cavernosa and Porites astreoides in Bermuda (32°N; sea surface temperature ∼19-29°C) over 5 weeks, applying the following treatments: (i) constant control temperature at 28°C, and (ii) temperature reduction (0.5°C day-1) followed by constant temperature (20 days; acclimatization period) at 24°C and (iii) at 20°C. Both species decreased photosynthesis and respiration during temperature reduction as expected, which continued to decrease during the acclimatization period, indicating adjustment to a low energy turnover rather than thermal compensation. Trajectories of physiological adjustments and level of thermal compensation, however, differed between species. Montastraea cavernosa zooxanthellae metrics showed a strong initial response to temperature reduction, followed by a return to close to control values during the acclimatization period, reflecting a high physiological flexibility and low thermal compensation. Porites astreoides zooxanthellae, in contrast, showed no initial response, but an increase in pigment concentration per zooxanthellae and similar photosynthesis rates at 24°C and 20°C at the end of the experiment, indicating low acute thermal sensitivity and the ability for thermal compensation at the lowest temperature. Respiration decreased more strongly than photosynthesis, leading to significant build-up of biomass in both species (energy reserves). Results are important in the light of potential poleward migration of corals and of potential latitudinal and species-specific differences in coral thermal tolerance., Competing Interests: Competing interests The authors declare no competing or financial interests., (© 2022. Published by The Company of Biologists Ltd.)

Marine heatwaves have been observed worldwide and are expected to increase in both frequency and intensity due to climate change. Such events may cause ecosystem reconfigurations arising from species range contraction or redistribution, with ecological, economic and social implications. Macrophytes such as the brown seaweed Fucus vesiculosus and the seagrass Zostera marina are foundation species in many coastal ecosystems of the temperate northern hemisphere. Hence, their response to extreme events can potentially determine the fate of associated ecosystems. Macrophyte functioning is intimately linked to the maintenance of photosynthesis, growth and reproduction, and resistance against pathogens, epibionts and grazers. We investigated morphological, physiological, pathological and chemical defence responses of western Baltic Sea F. vesiculosus and Z. marina populations to simulated near-natural marine heatwaves. Along with (a) the control, which constituted no heatwave but natural stochastic temperature variability (0HW), two treatments were applied: (b) two late-spring heatwaves (June, July) followed by a summer heatwave (August; 3HW) and (c) a summer heatwave only (1HW). The 3HW treatment was applied to test whether preconditioning events can modulate the potential sensitivity to the summer heatwave. Despite the variety of responses measured in both species, only Z. marina growth was impaired by the accumulative heat stress imposed by the 3HW treatment. Photosynthetic rate, however, remained high after the last heatwave indicating potential for recovery. Only epibacterial abundance was significantly affected in F. vesiculosus. Hence both macrophytes, and in particular F. vesiculosus, seem to be fairly tolerant to short-term marine heatwaves at least at the intensities applied in this experiment (up to 5°C above mean temperature over a period of 9 days). This may partly be due to the fact that F. vesiculosus grows in a highly variable environment, and may have a high phenotypic plasticity., (© 2019 John Wiley & Sons Ltd.)

More than a decade ago, a new mitochondrial Open Reading Frame (mtORF) was discovered in corals of the family Pocilloporidae and has been used since then as an effective barcode for these corals. Recently, mtORF sequencing revealed the existence of two differentiated Stylophora lineages occurring in sympatry along the environmental gradient of the Red Sea (18.5°C to 33.9°C). In the endemic Red Sea lineage RS_LinB , the mtORF and the heat shock protein gene hsp70 uncovered similar phylogeographic patterns strongly correlated with environmental variations. This suggests that the mtORF too might be involved in thermal adaptation. Here, we used computational analyses to explore the features and putative function of this mtORF. In particular, we tested the likelihood that this gene encodes a functional protein and whether it may play a role in adaptation. Analyses of full mitogenomes showed that the mtORF originated in the common ancestor of Madracis and other pocilloporids, and that it encodes a transmembrane protein differing in length and domain architecture among genera. Homology-based annotation and the relative conservation of metal-binding sites revealed traces of an ancient hydrolase catalytic activity. Furthermore, signals of pervasive purifying selection, lack of stop codons in 1830 sequences analyzed, and a codon-usage bias similar to that of other mitochondrial genes indicate that the protein is functional, i.e., not a pseudogene. Other features, such as intrinsically disordered regions, tandem repeats, and signals of positive selection particularly in Stylophora RS_LinB populations, are consistent with a role of the mtORF in adaptive responses to environmental changes., Competing Interests: The authors declare no conflict of interest.

The most important source of energy to tropical shallow water coral reefs is light, the transformation of which ultimately limits reef biomass and growth. Therefore, measurements of productivity (primary production, P) for benthic reef organisms and communities are critical to understand reef functioning. Short-term (minutes to hours) P measurements of reef photosynthesizers virtually always produce the classic hyperbolic tangent (or similar) P-E (irradiance) relationship, with P rapidly rising to a saturation point as E increases. Longer-term (days to weeks), larger-scale investigations of natural reef communities typically do not explore P-E relationships, but the few that do show no saturation of time-integrated P with high time-integrated E. In this paper we present a modeling study to reconcile this apparent contradiction. We used 52 published short-term (instantaneous) P-E curves of organisms (corals, algae) and communities (corals, mixed corals and algae) from different reefs in the Indo-Pacific and the Caribbean, each coupled with 928 diel light curves comprising a wide range of cloud cover scenarios. The diel light curves provided instantaneous E at 1-minute intervals, from which we calculated corresponding instantaneous P using the different published P-E relationships. We integrated both variables to calculate time-integrated E and P. Time-integrated E varied up to 18-fold due to changes in cloud cover and season. We found that, despite routine saturation of instantaneous P, day-scale P-E relationships were near linear in all cases, with slightly decreased linearity in cases where instantaneous light saturation occurred very early during the day. This indicates that the Functional Convergence Hypothesis (FCH) developed by terrestrial ecologists may also apply for reef photosynthesizers. The FCH states that despite short-term light saturation, plants on average do not absorb more light than they can use, since resource allocations are strictly coordinated and tailored towards an optimal use. Thus, there is no contradiction: At the growth time scale (≥ day), P should be expected to be a near linear function of E. One implication is that reef P can be estimated using rapid optical measurements, as opposed to traditional, laborious respirometry methods. The requirement going forward is to derive appropriate values for light-use efficiency, which is the rate at which the plant or community converts absorbed light into fixed carbon., Competing Interests: The authors have declared that no competing interests exist.

Climate change will not only shift environmental means but will also increase the intensity of extreme events, exerting additional stress on ecosystems. While field observations on the ecological consequences of heat waves are emerging, experimental evidence is rare, and lacking at the community level. Using a novel "near-natural" outdoor mesocosms approach, this study tested whether marine summer heat waves have detrimental consequences for macrofauna of a temperate coastal community, and whether sequential heat waves provoke an increase or decrease of sensitivity to thermal stress. Three treatments were applied, defined and characterized through a statistical analysis of 15 years of temperature records from the experimental site: (1) no heat wave, (2) two heat waves in June and July followed by a summer heat wave in August and (3) the summer heat wave only. Overall, 50% of the species showed positive, negative or positive/negative responses in either abundance and/or biomass. We highlight four possible ways in which single species responded to either three subsequent heat waves or one summer heat wave: (1) absence of a response (tolerance, 50% of species), (2) negative accumulative effects by three subsequent heat waves (tellinid bivalve), (3) buffering by proceeding heat waves due to acclimation and/or shifts in phenology (spionid polychaete) and (4) an accumulative positive effect by subsequent heat waves (amphipod). The differential responses to single or sequential heat waves at the species level entailed shifts at the community level. Community-level differences between single and triple heat waves were more pronounced than those between regimes with vs. without heat waves. Detritivory was reduced by the single heat wave while suspension feeding was less common in the triple heat wave regime. Critical extreme events occur already today and will occur more frequently in a changing climate, thus, leading to detrimental impacts on coastal marine systems., (© 2018 John Wiley & Sons Ltd.)

Global warming was reported to cause growth reductions in tropical shallow water corals in both, cooler and warmer, regions of the coral species range. This suggests regional adaptation with less heat-tolerant populations in cooler and more thermo-tolerant populations in warmer regions. Here, we investigated seasonal changes in the in situ metabolic performance of the widely distributed hermatypic coral Pocillopora verrucosa along 12° latitudes featuring a steep temperature gradient between the northern (28.5°N, 21-27°C) and southern (16.5°N, 28-33°C) reaches of the Red Sea. Surprisingly, we found little indication for regional adaptation, but strong indications for high phenotypic plasticity: Calcification rates in two seasons (winter, summer) were found to be highest at 28-29°C throughout all populations independent of their geographic location. Mucus release increased with temperature and nutrient supply, both being highest in the south. Genetic characterization of the coral host revealed low inter-regional variation and differences in the Symbiodinium clade composition only at the most northern and most southern region. This suggests variable acclimatization potential to ocean warming of coral populations across the Red Sea: high acclimatization potential in northern populations, but limited ability to cope with ocean warming in southern populations already existing at the upper thermal margin for corals.

Large scale patterns of ecologically relevant traits may help identify drivers of their variability and conditions beneficial or adverse to the expression of these traits. Antimicrofouling defenses in scleractinian corals regulate the establishment of the associated biofilm as well as the risks of infection. The Saudi Arabian Red Sea coast features a pronounced thermal and nutritional gradient including regions and seasons with potentially stressful conditions to corals. Assessing the patterns of antimicrofouling defenses across the Red Sea may hint at the susceptibility of corals to global change. We investigated microfouling pressure as well as the relative strength of 2 alternative antimicrofouling defenses (chemical antisettlement activity, mucus release) along the pronounced environmental gradient along the Saudi Arabian Red Sea coast in 2 successive years. Microfouling pressure was exceptionally low along most of the coast but sharply increased at the southernmost sites. Mucus release correlated with temperature. Chemical defense tended to anti-correlate with mucus release. As a result, the combined action of mucus release and chemical antimicrofouling defense seemed to warrant sufficient defense against microbes along the entire coast. In the future, however, we expect enhanced energetic strain on corals when warming and/or eutrophication lead to higher bacterial fouling pressure and a shift towards putatively more costly defense by mucus release.

Algal symbionts (zooxanthellae, genus Symbiodinium) of scleractinian corals respond strongly to temperature, nutrient and light changes. These factors vary greatly along the north-south gradient in the Red Sea and include conditions, which are outside of those typically considered optimal for coral growth. Nevertheless, coral communities thrive throughout the Red Sea, suggesting that zooxanthellae have successfully acclimatized or adapted to the harsh conditions they experience particularly in the south (high temperatures and high nutrient supply). As such, the Red Sea is a region, which may help to better understand how zooxanthellae and their coral hosts successfully acclimatize or adapt to environmental change (e.g. increased temperatures and localized eutrophication). To gain further insight into the physiology of coral symbionts in the Red Sea, we examined the abundance of dominant Symbiodinium types associated with the coral Pocillopora verrucosa, and measured Symbiodinium physiological characteristics (i.e. photosynthetic processes, cell density, pigmentation, and protein composition) along the latitudinal gradient of the Red Sea in summer and winter. Despite the strong environmental gradients from north to south, our results demonstrate that Symbiodinium microadriaticum (type A1) was the predominant species in P. verrucosa along the latitudinal gradient. Furthermore, measured physiological characteristics were found to vary more with prevailing seasonal environmental conditions than with region-specific differences, although the measured environmental parameters displayed much higher spatial than temporal variability. We conclude that our findings might present the result of long-term acclimatization or adaptation of S. microadriaticum to regionally specific conditions within the Red Sea. Of additional note, high nutrients in the South correlated with high zooxanthellae density indicating a compensation for a temperature-driven loss of photosynthetic performance, which may prove promising for the resilience of these corals under increase of temperature increase and eutrophication.

Coral recruitment was assessed in highly diverse and economically important Spermonde Archipelago, a reef system subjected to land-based sources of siltation/pollution and destructive fishing, over a period of 2 years. Recruitment on settlement tiles reached up to 705 spat m(-2) yr(-1) and was strongest in the dry season (July-October), except off-shore, where larvae settled earlier. Pocilloporidae dominated near-shore, while a more diverse community of Acroporidae, Poritidae and others settled in the less polluted mid-shelf and off-shore reefs. Non-coral fouling community appeared to hardly influence initial coral settlement on the tiles, although, this does not necessarily infer low coral post-settlement mortality, which may be enhanced at the near- and off-shore reefs as indicated by increased abundances of potential space competitors on natural substrate. Blast fishing showed no local reduction in coral recruitment and live hard coral cover increased in oligotrophic reefs, indicating potential for coral recovery, if managed effectively., (Copyright © 2013 Elsevier Ltd. All rights reserved.)

Biofilms play an important role as a settlement cue for invertebrate larvae and significantly contribute to the nutrient turnover in aquatic ecosystems. Nevertheless, little is known about how biofilm community structure generally responds to environmental changes. This study aimed to identify patterns of bacterial dynamics in coral reef biofilms in response to associated macrofouling community structure, microhabitat (exposed vs. sheltered), seasonality, and eutrophication. Settlement tiles were deployed at four reefs along a cross-shelf eutrophication gradient and were exchanged every 4 months over 20 months. The fouling community composition on the tiles was recorded and the bacterial community structure was assessed with the community fingerprinting technique Automated Ribosomal Intergenic Spacer Analysis (ARISA). Bacterial operational taxonomic unit (OTU) number was higher on exposed tiles, where the fouling community was homogenous and algae-dominated, than in sheltered habitats, which were occupied by a variety of filter feeders. Furthermore, OTU number was also highest in eutrophied near-shore reefs, while seasonal variations in community structure were most pronounced in the oligotrophic mid-shelf reef. In contrast, the macrofouling community structure did not change significantly with seasons. Changes in bacterial community patterns were mostly affected by microhabitat, seasonal and anthropogenically derived changes in nutrient availability, and to a lesser extent by changes in the macrofouling community structure. Path analysis revealed a complex interplay of various environmental and biological factors explaining the spatial and temporal variations in bacterial biofilm communities under natural conditions.