Divide and conquer: Spatial and temporal resource partitioning structures benthic cyanobacterial mats.

Benthic cyanobacterial mats are increasing in abundance worldwide with the potential to degrade ecosystem structure and function. Understanding mat community dynamics is thus critical for predicting mat growth and proliferation and for mitigating any associated negative effects. Carbon, nitrogen, and sulfur cycling are the predominant forms of nutrient cycling discussed within the literature, while metabolic cooperation and viral interactions are understudied. Although many forms of nutrient cycling in mats have been assessed, the links between niche dynamics, microbial interactions, and nutrient cycling are not well described. Here, we present an updated review on how nutrient cycling and microbial community interactions in mats are structured by resource partitioning via spatial and temporal heterogeneity and succession. We assess community interactions and nutrient cycling at both intramat and metacommunity scales. Additionally, we present ideas and recommendations for research in this area, highlighting top-down control, boundary layers, and metabolic cooperation as important future directions.

Convergent photophysiology and prokaryotic assemblage structure in epilithic cyanobacterial tufts and algal turf communities.

As global change spurs shifts in benthic community composition on coral reefs globally, a better understanding of the defining taxonomic and functional features that differentiate proliferating benthic taxa is needed to predict functional trajectories of reef degradation better. This is especially critical for algal groups, which feature dramatically on changing reefs. Limited attention has been given to characterizing the features that differentiate tufting epilithic cyanobacterial communities from ubiquitous turf algal assemblages. Here, we integrated an in situ assessment of photosynthetic yield with metabarcoding and shotgun metagenomic sequencing to explore photophysiology and prokaryotic assemblage structure within epilithic tufting benthic cyanobacterial communities and epilithic algal turf communities. Significant differences were not detected in the average quantum yield. However, variability in yield was significantly higher in cyanobacterial tufts. Neither prokaryotic assemblage diversity nor structure significantly differed between these functional groups. The sampled cyanobacterial tufts, predominantly built by Okeania sp., were co-dominated by members of the Proteobacteria, Firmicutes, and Bacteroidota, as were turf algal communities. Few detected ASVs were significantly differentially abundant between functional groups and consisted exclusively of taxa belonging to the phyla Proteobacteria and Firmicutes. Assessment of the distribution of recovered cyanobacterial amplicons demonstrated that alongside sample-specific cyanobacterial diversification, the dominant cyanobacterial members were conserved across tufting cyanobacterial and turf algal communities. Overall, these data suggest a convergence in taxonomic identity and mean photosynthetic potential between tufting epilithic cyanobacterial communities and algal turf communities, with numerous implications for consumer-resource dynamics on future reefs and trajectories of reef functional ecology.

Effects of ocean acidification on growth and photophysiology of two tropical reef macroalgae.

Macroalgae can modify coral reef community structure and ecosystem function through a variety of mechanisms, including mediation of biogeochemistry through photosynthesis and the associated production of dissolved organic carbon (DOC). Ocean acidification has the potential to fuel macroalgal growth and photosynthesis and alter DOC production, but responses across taxa and regions are widely varied and difficult to predict. Focusing on algal taxa from two different functional groups on Caribbean coral reefs, we exposed fleshy (Dictyota spp.) and calcifying (Halimeda tuna) macroalgae to ambient and low seawater pH for 25 days in an outdoor experimental system in the Florida Keys. We quantified algal growth, calcification, photophysiology, and DOC production across pH treatments. We observed no significant differences in the growth or photophysiology of either species between treatments, except for lower chlorophyll b concentrations in Dictyota spp. in response to low pH. We were unable to quantify changes in DOC production. The tolerance of Dictyota and Halimeda to near-future seawater carbonate chemistry and stability of photophysiology, suggests that acidification alone is unlikely to change biogeochemical processes associated with algal photosynthesis in these species. Additional research is needed to fully understand how taxa from these functional groups sourced from a wide range of environmental conditions regulate photosynthesis (via carbon uptake strategies) and how this impacts their DOC production. Understanding these species-specific responses to future acidification will allow us to more accurately model and predict the indirect impacts of macroalgae on coral health and reef ecosystem processes.

Top-heavy trophic structure within benthic viral dark matter.

A better understanding of system-specific viral ecology in diverse environments is needed to predict patterns of virus-host trophic structure in the Anthropocene. This study characterised viral-host trophic structure within coral reef benthic cyanobacterial mats-a globally proliferating cause and consequence of coral reef degradation. We employed deep longitudinal multi-omic sequencing to characterise the viral assemblage (ssDNA, dsDNA, and dsRNA viruses) and profile lineage-specific host-virus interactions within benthic cyanobacterial mats sampled from Bonaire, Caribbean Netherlands. We recovered 11,012 unique viral populations spanning at least 10 viral families across the orders Caudovirales, Petitvirales, and Mindivirales. Gene-sharing network analyses provided evidence for extensive genomic novelty of mat viruses from reference and environmental viral sequences. Analysis of coverage ratios of viral sequences and computationally predicted hosts spanning 15 phyla and 21 classes revealed virus-host abundance (from DNA) and activity (from RNA) ratios consistently exceeding 1:1, suggesting a top-heavy intra-mat trophic structure with respect to virus-host interactions. Overall, our article contributes a curated database of viral sequences found in Caribbean coral reef benthic cyanobacterial mats (vMAT database) and provides multiple lines of field-based evidence demonstrating that viruses are active members of mat communities, with broader implications for mat functional ecology and demography.

Territoriality drives patterns of fixed space use in Caribbean parrotfishes.

Animals often occupy home ranges where they conduct daily activities. In many parrotfishes, large terminal phase (TP) males defend their diurnal (i.e., daytime) home ranges as intraspecific territories occupied by harems of initial phase (IP) females. However, we know relatively little about the exclusivity and spatial stability of these territories. We investigated diurnal home range behavior in several TPs and IPs of five common Caribbean parrotfish species on the fringing coral reefs of Bonaire, Caribbean Netherlands. We computed parrotfish home ranges to investigate differences in space use and then quantified spatial overlap of home ranges between spatially co-occurring TPs to investigate exclusivity. We also quantified the spatial overlap of home ranges estimated from repeat tracks of a few TPs to investigate their spatial stability. We then discussed these results in the context of parrotfish social behavior. Home range sizes differed significantly among species. Spatial overlap between home ranges was lower for intraspecific than interspecific pairs of TPs. Focal TPs frequently engaged in agonistic interactions with intraspecific parrotfish and interacted longest with intraspecific TP parrotfish. This behavior suggests that exclusionary agonistic interactions may contribute to the observed patterns of low spatial overlap between home ranges. The spatial overlap of home ranges estimated from repeated tracks of several TPs of three study species was high, suggesting that home ranges were spatially stable for at least 1 month. Taken together, our results provide strong evidence that daytime parrotfish space use is constrained within fixed intraspecific territories in which territory holders have nearly exclusive access to resources. Grazing by parrotfishes maintains benthic reef substrates in early successional states that are conducive to coral larval settlement and recruitment. Behavioral constraints on parrotfish space use may drive spatial heterogeneity in grazing pressure and affect local patterns of benthic community assembly. A thorough understanding of the spatial ecology of parrotfishes is, therefore, necessary to elucidate their functional roles on coral reefs.

Are synchronous chats a silver lining of emergency remote instruction? Text-based chatting is disproportionately favored by women in a non-majors introductory biology course.

The coronavirus disease 2019 (COVID-19) pandemic has led to a reimagining of many aspects of higher education, including how instructors interact with their students and how they encourage student participation. Text-based chatting during synchronous remote instruction is a simple form of student-student and student-instructor interaction. The importance of student participation has been documented, as have clear disparities in participation between those well-represented and those under-represented in science disciplines. Thus, we conducted an investigation into who is texting, what students are texting, and how these texts align with course content. We focused on two sections of a large-enrollment, introductory biology class offered remotely during Fall 2020. Using an analysis of in-class chatting, in combination with student survey responses, we find that text-based chatting suggests not only a high level of student engagement, but a type of participation that is disproportionately favored by women. Given the multiple lines of evidence indicating that women typically under-participate in their science courses, any vehicle that counters this trend merits further exploration. We conclude with suggestions for further research, and ideas for carrying forward text-based chatting in the post-COVID-19, in-person classroom.

Cyanobacterial mats as benthic reservoirs and vectors for coral black band disease pathogens.

The concurrent rise in the prevalence of conspicuous benthic cyanobacterial mats and the incidence of coral diseases independently mark major axes of degradation of coral reefs globally. Recent advances have uncovered the potential for the existence of interactions between the expanding cover of cyanobacterial mats and coral disease, especially black band disease (BBD), and this intersection represents both an urgent conservation concern and a critical challenge for future research. Here, we propose links between the transmission of BBD and benthic cyanobacterial mats. We provide molecular and ecophysiological evidence suggesting that cyanobacterial mats may create and maintain physically favorable benthic refugia for BBD pathogens while directly harboring BBD precursor assemblages, and discuss how mats may serve as direct (mediated via contact) and indirect (mediated via predator-prey-pathogen relationships) vectors for BBD pathogens. Finally, we identify and outline future priority research directions that are aligned with actionable management practices and priorities to support evidence-based coral conservation practices.

Gulf of Mexico coralline algae are robust to sunscreen pollution.

Sunscreens generate a potentially important source of environmental contamination across marine and aquatic systems. Oxybenzone (benzophenone-3; BP-3) is one of the most common organic filters in chemical sunscreen and has been detected in seawater at high concentrations. In this study, we asked whether BP-3 contamination affected the photosynthesis, respiration, and photophysiology of rhodoliths collected offshore from popular Gulf of Mexico beaches in North Florida. We found no evidence for negative effects of the common organic UV filter BP-3 on Gulf of Mexico rhodoliths. This result is promising for the fate of these important algae who act as habitat builders and foundational components of global reef ecosystems.

Differential impacts of alternate primary producers on carbon cycling.

Disturbance impacts the spatial distribution of primary producers, which can have cascading effects on ecosystem function. The lower-intertidal zone on the rocky shores of the Pacific Northwest is one such place where wave energy creates a mosaic-like distribution between two assemblages: surfgrass (Phyllospadix scouleri) meadows and macroalgal forests dominated by kelp. We simulated wave disturbance by experimentally removing patches of surfgrass monocultures, resulting in a macroalgal assemblage with increased diversity, biomass, and net primary productivity in the following year. Although surfgrass had a higher C:N compared to macroalgal assemblages, macroalgal assemblages achieved a higher biomass, fixed carbon at a faster rate, and released more dissolved organic carbon (DOC) during photosynthesis. Thus, despite similar standing amounts of carbon, macroalgal assemblages have increased carbon turnover-from fixation to DOC release. Comparative photophysiology indicated that surfgrasses have a competitive advantage over other macrophytes at low light levels, allowing them to persist when disturbance is reduced. Unexpectedly, disturbance in this system increased the potential for carbon sequestration when surfgrass monocultures were replaced by diverse macroalgae.

Shotgun metagenomic sequencing reveals the full taxonomic, trophic, and functional diversity of a coral reef benthic cyanobacterial mat from Bonaire, Caribbean Netherlands.

Anthropogenic forcing is spurring cyanobacterial proliferation in aquatic ecosystems worldwide. While planktonic cyanobacterial blooms have received substantial research attention, benthic blooms of mat-forming cyanobacteria have received considerably less attention, especially benthic mat blooms on coral reefs. Resultingly, numerous aspects of coral reef benthic cyanobacterial bloom ecology remain unknown, including underlying biodiversity in the mat communities. Most previous characterizations of coral reef cyanobacterial mat composition have only considered the cyanobacterial component. Without an unbiased characterization of full community diversity, we cannot predict whole-community response to anthropogenic inputs or effectively determine appropriate mitigation strategies. Here, we advocate for the implementation of shotgun sequencing techniques to study coral reef cyanobacterial mats worldwide, utilizing a case study of a coral reef benthic cyanobacterial mat sampled from the island of Bonaire, Caribbean Netherlands. Read-based taxonomic profiling revealed that Cyanobacteria was present at only 47.57% relative abundance in a coral reef cyanobacterial mat, with non-cyanobacterial members of the sampled mat community, including diatoms (0.78%), fungi (0.25%), Archaea (0.34%), viruses (0.08%), and other bacteria (45.78%), co-dominating the community. We found numerous gene families for regulatory systems and for functional pathways (both aerobic and anaerobic). These gene families were involved in community coordination; photosynthesis; nutrient scavenging; and the cycling of sulfur, nitrogen, phosphorous, and iron. We also report bacteriophage (including prophage) sequences associated with this subtidal coral reef cyanobacterial mat, which could contribute to intra-mat nutrient cycling and bloom dynamics. Overall, our results suggest that Cyanobacteria-focused analysis of coral reef cyanobacterial mats underestimates mat diversity and fails to capture community members possessing broad metabolic potential for intra-mat nutrient scavenging, recycling, and retention that likely contribute to the contemporary success of cyanobacterial mats on reefs. We advocate for increased collaboration between microbiologists and coral reef ecologists to unite insights from each discipline and improve efforts to understand mat ecology.

Caribbean reefs of the Anthropocene: Variance in ecosystem metrics indicates bright spots on coral depauperate reefs.

Dramatic coral loss has significantly altered many Caribbean reefs, with potentially important consequences for the ecological functions and ecosystem services provided by reef systems. Many studies examine coral loss and its causes-and often presume a universal decline of ecosystem services with coral loss-rather than evaluating the range of possible outcomes for a diversity of ecosystem functions and services at reefs varying in coral cover. We evaluate 10 key ecosystem metrics, relating to a variety of different reef ecosystem functions and services, on 328 Caribbean reefs varying in coral cover. We focus on the range and variability of these metrics rather than on mean responses. In contrast to a prevailing paradigm, we document high variability for a variety of metrics, and for many the range of outcomes is not related to coral cover. We find numerous "bright spots," where herbivorous fish biomass, density of large fishes, fishery value, and/or fish species richness are high, despite low coral cover. Although it remains critical to protect and restore corals, understanding variability in ecosystem metrics among low-coral reefs can facilitate the maintenance of reefs with sustained functions and services as we work to restore degraded systems. This framework can be applied to other ecosystems in the Anthropocene to better understand variance in ecosystem service outcomes and identify where and why bright spots exist.

Evolutionary Phycology: Toward a Macroalgal Species Conceptual Framework.

Species concepts formalize evolutionary and ecological processes, but often conflict with one another when considering the mechanisms that ultimately lead to species delimitation. Evolutionary biologists are, however, recognizing that the conceptualization of a species is separate and distinct from the delimitation of species. Indeed, if species are generally defined as separately evolving metapopulation lineages, then characteristics, such as reproductive isolation or monophyly, can be used as evidence of lineage separation and no longer conflict with the conceptualization of a species. However, little of this discussion has addressed the formalization of this evolutionary conceptual framework for macroalgal species. This may be due to the complexity and variation found in macroalgal life cycles. While macroalgal mating system variation and patterns of hybridization and introgression have been identified, complex algal life cycles generate unique eco-evolutionary consequences. Moreover, the discovery of frequent macroalgal cryptic speciation has not been accompanied by the study of the evolutionary ecology of those lineages, and, thus, an understanding of the mechanisms underlying such rampant speciation remain elusive. In this perspective, we aim to further the discussion and interest in species concepts and speciation processes in macroalgae. We propose a conceptual framework to enable phycological researchers and students alike to portray these processes in a manner consistent with dialogue at the forefront of evolutionary biology. We define a macroalgal species as an independently evolving metapopulation lineage, whereby we can test for reproductive isolation or the occupation of distinct adaptive zones, among other mechanisms, as secondary lines of supporting evidence.

Emerging Priorities for Microbiome Research.

Microbiome research has increased dramatically in recent years, driven by advances in technology and significant reductions in the cost of analysis. Such research has unlocked a wealth of data, which has yielded tremendous insight into the nature of the microbial communities, including their interactions and effects, both within a host and in an external environment as part of an ecological community. Understanding the role of microbiota, including their dynamic interactions with their hosts and other microbes, can enable the engineering of new diagnostic techniques and interventional strategies that can be used in a diverse spectrum of fields, spanning from ecology and agriculture to medicine and from forensics to exobiology. From June 19-23 in 2017, the NIH and NSF jointly held an Innovation Lab on Quantitative Approaches to Biomedical Data Science Challenges in our Understanding of the Microbiome. This review is inspired by some of the topics that arose as priority areas from this unique, interactive workshop. The goal of this review is to summarize the Innovation Lab's findings by introducing the reader to emerging challenges, exciting potential, and current directions in microbiome research. The review is broken into five key topic areas: (1) interactions between microbes and the human body, (2) evolution and ecology of microbes, including the role played by the environment and microbe-microbe interactions, (3) analytical and mathematical methods currently used in microbiome research, (4) leveraging knowledge of microbial composition and interactions to develop engineering solutions, and (5) interventional approaches and engineered microbiota that may be enabled by selectively altering microbial composition. As such, this review seeks to arm the reader with a broad understanding of the priorities and challenges in microbiome research today and provide inspiration for future investigation and multi-disciplinary collaboration.

Photosynthetic Responses of Turf-forming Red Macroalgae to High CO2 Conditions.

Seaweeds are important components of near-shore ecosystems as primary producers, foundation species, and biogeochemical engineers. Seaweed communities are likely to alter under predicted climate change scenarios. We tested the physiological responses of three perennial, turf-building, intertidal rhodophytes, Mastocarpus stellatus, Osmundea pinnatifida, and the calcified Ellisolandia elongata, to elevated pCO2 over 6 weeks. Responses varied between these three species. E. elongata was strongly affected by high pCO2 , whereas non-calcified species were not. Elevated pCO2 did not induce consistent responses of photosynthesis and respiration across these three species. While baseline photophysiology differed significantly between species, we found few clear effects of elevated pCO2 on this aspect of macroalgal physiology. We found effects of within-species variation in elevated pCO2 response in M. stellatus, but not in the other species. Overall, our data confirm the sensitivity of calcified macroalgae to elevated pCO2 , but we found no evidence suggesting that elevated pCO2 conditions will have a strong positive or negative impact on photosynthetic parameters in non-calcified macroalgae.

Thermal plasticity is independent of environmental history in an intertidal seaweed.

Organisms inhabiting the intertidal zone have been used to study natural ecophysiological responses and adaptations to thermal stress because these organisms are routinely exposed to high-temperature conditions for hours at a time. While intertidal organisms may be inherently better at withstanding temperature stress due to regular exposure and acclimation, they could be more vulnerable to temperature stress, already living near the edge of their thermal limits. Strong gradients in thermal stress across the intertidal zone present an opportunity to test whether thermal tolerance is a plastic or canalized trait in intertidal organisms. Here, we studied the intertidal pool-dwelling calcified alga, Ellisolandia elongata, under near-future temperature regimes, and the dependence of its thermal acclimatization response on environmental history. Two timescales of environmental history were tested during this experiment. The intertidal pool of origin was representative of long-term environmental history over the alga's life (including settlement and development), while the pool it was transplanted into accounted for recent environmental history (acclimation over many months). Unexpectedly, neither long-term nor short-term environmental history, nor ambient conditions, affected photosynthetic rates in E. elongata. Individuals were plastic in their photosynthetic response to laboratory temperature treatments (mean 13.2°C, 15.7°C, and 17.7°C). Further, replicate ramets from the same individual were not always consistent in their photosynthetic performance from one experimental time point to another or between treatments and exhibited no clear trend in variability over experimental time. High variability in climate change responses between individuals may indicate the potential for resilience to future conditions and, thus, may play a compensatory role at the population or species level over time.

Ocean acidification and hypoxia alter organic carbon fluxes in marine soft sediments.

Anthropogenic stressors can alter the structure and functioning of infaunal communities, which are key drivers of the carbon cycle in marine soft sediments. Nonetheless, the compounded effects of anthropogenic stressors on carbon fluxes in soft benthic systems remain largely unknown. Here, we investigated the cumulative effects of ocean acidification (OA) and hypoxia on the organic carbon fate in marine sediments, through a mesocosm experiment. Isotopically labelled macroalgal detritus (13 C) was used as a tracer to assess carbon incorporation in faunal tissue and in sediments under different experimental conditions. In addition, labelled macroalgae (13 C), previously exposed to elevated CO2 , were also used to assess the organic carbon uptake by fauna and sediments, when both sources and consumers were exposed to elevated CO2 . At elevated CO2 , infauna increased the uptake of carbon, likely as compensatory response to the higher energetic costs faced under adverse environmental conditions. By contrast, there was no increase in carbon uptake by fauna exposed to both stressors in combination, indicating that even a short-term hypoxic event may weaken the ability of marine invertebrates to withstand elevated CO2 conditions. In addition, both hypoxia and elevated CO2 increased organic carbon burial in the sediment, potentially affecting sediment biogeochemical processes. Since hypoxia and OA are predicted to increase in the face of climate change, our results suggest that local reduction of hypoxic events may mitigate the impacts of global climate change on marine soft-sediment systems.

Consumption of benthic cyanobacterial mats on a Caribbean coral reef.

Herbivory is an important process in the general structuring of coral reef benthic communities. However, evidence of its ability to control coral reef benthic cyanobacterial mats, which have recently proliferated on reefs worldwide, remains ambivalent. Here, we report that the French Angelfish (Pomacanthus paru), Striped Parrotfish (Scarus iseri), Rock Beauty (Holacanthus tricolor), Ocean Surgeonfish (Acanthurus bahianus), Blue Parrotfish (Scarus coeruleus), and Atlantic Blue Tang (Acanthurus coeruleus) consume benthic cyanobacterial mats on coral reefs in Bonaire, Netherlands. We documented the foraging patterns of P. paru and S. iseri, and found that benthic cyanobacterial mats comprised 36.7% ± 5.8% and 15.0% ± 1.53% (mean ± standard error) of the total bites taken by P. paru and S. iseri respectively. This magnitude of consumption suggests that grazing by reef fishes may represent a potentially important, but previously undocumented, top-down control on benthic cyanobacterial mats on Caribbean reefs.

Understanding the margin squeeze: Differentiation in fitness-related traits between central and trailing edge populations of Corallina officinalis.

ABSTRACT: Assessing population responses to climate-related environmental change is key to understanding the adaptive potential of the species as a whole. Coralline algae are critical components of marine shallow water ecosystems where they function as important ecosystem engineers. Populations of the calcifying algae Corallina officinalis from the center (southern UK) and periphery (northern Spain) of the North Atlantic species natural distribution were selected to test for functional differentiation in thermal stress response. Physiological measurements of calcification, photosynthesis, respiration, growth rates, oxygen, and calcification evolution curves were performed using closed cell respirometry methods. Species identity was genetically confirmed via DNA barcoding. Through a common garden approach, we identified distinct vulnerability to thermal stress of central and peripheral populations. Southern populations showed a decrease in photosynthetic rate under environmental conditions of central locations, and central populations showed a decline in calcification rates under southern conditions. This shows that the two processes of calcification and photosynthesis are not as tightly coupled as previously assumed. How the species as whole will react to future climatic changes will be determined by the interplay of local environmental conditions and these distinct population adaptive traits. OPEN RESEARCH BADGES: This article has earned an Open Materials Badge for making publicly available the components of the research methodology needed to reproduce the reported procedure and analysis. All materials are available at https://doi.pangaea.de/10.1594/PANGAEA.899568.