Microplastic abundance and accumulation patterns in eelgrass (Zostera marina L.) meadows throughout coastal Massachusetts, USA.

Microplastics are fast-emerging as another potential threat to already globally declining seagrass ecosystems, but there is a paucity of in situ surveys showing their accumulations. Here, we surveyed multiple Zostera marina L. meadows in 2020 and 2021 across Massachusetts, USA, for microplastic contamination, as well as identified factors related to patterns of accumulation. We found that microplastics were ubiquitous throughout all sites regardless of proximity to human development, with fibers being the most common microplastic type. In addition, we showed that accumulation of microplastics within seagrass meadows was related to epiphytic cover on leaves, plant morphology, and bulk-density in sediments. The results of this study provide the first in situ baseline microplastic concentrations on Z. marina plants and sediments for the temperate western North Atlantic. Additionally, we identify specific biotic and abiotic factors related to patterns of microplastic accumulation in these ecosystems.

Shifts in predator behaviour following climate induced disturbance on coral reefs.

Coral reefs are increasingly ecologically destabilized across the globe due to climate change. Behavioural plasticity in corallivore behaviour and short-term trophic ecology in response to bleaching events may influence the extent and severity of coral bleaching and subsequent recovery potential, yet our understanding of these interactions in situ remains unclear. Here, we investigated interactions between corallivory and coral bleaching during a severe high thermal event (10.3-degree heating weeks) in Belize. We found that parrotfish changed their grazing behaviour in response to bleaching by selectively avoiding bleached Orbicella spp. colonies regardless of bleaching severity or coral size. For bleached corals, we hypothesize that this short-term respite from corallivory may temporarily buffer coral energy budgets by not redirecting energetic resources to wound healing, and may therefore enable compensatory nutrient acquisition. However, colonies that had previously been heavily grazed were also more susceptible to bleaching, which is likely to increase mortality risk. Thus, short-term respite from corallivory during bleaching may not be sufficient to functionally rescue corals during prolonged bleaching. Such pairwise interactions and behavioural shifts in response to disturbance may appear small scale and short term, but have the potential to fundamentally alter ecological outcomes, especially in already-degraded ecosystems that are vulnerable and sensitive to change.

Patterns, dynamics and consequences of microplastic ingestion by the temperate coral, Astrangia poculata.

Microplastics (less than 5 mm) are a recognized threat to aquatic food webs because they are ingested at multiple trophic levels and may bioaccumulate. In urban coastal environments, high densities of microplastics may disrupt nutritional intake. However, behavioural dynamics and consequences of microparticle ingestion are still poorly understood. As filter or suspension feeders, benthic marine invertebrates are vulnerable to microplastic ingestion. We explored microplastic ingestion by the temperate coral Astrangia poculata. We detected an average of over 100 microplastic particles per polyp in wild-captured colonies from Rhode Island. In the laboratory, corals were fed microbeads to characterize ingestion preference and retention of microplastics and consequences on feeding behaviour. Corals were fed biofilmed microplastics to test whether plastics serve as vectors for microbes. Ingested microplastics were apparent within the mesenterial tissues of the gastrovascular cavity. Corals preferred microplastic beads and declined subsequent offerings of brine shrimp eggs of the same diameter, suggesting that microplastic ingestion can inhibit food intake. The corals co-ingested Escherichia coli cells with microbeads. These findings detail specific mechanisms by which microplastics threaten corals, but also hint that the coral A. poculata, which has a large coastal range, may serve as a useful bioindicator and monitoring tool for microplastic pollution.

Establishment, management, and maintenance of the phoenix islands protected area.

The Republic of Kiribati's Phoenix Islands Protected Area (PIPA), located in the equatorial central Pacific, is the largest and deepest UNESCO World Heritage site on earth. Created in 2008, it was the first Marine Protected Area (MPA) of its kind (at the time of inception, the largest in the world) and includes eight low-lying islands, shallow coral reefs, submerged shallow and deep seamounts and extensive open-ocean and ocean floor habitat. Due to their isolation, the shallow reef habitats have been protected de facto from severe exploitation, though the surrounding waters have been continually fished for large pelagics and whales over many decades. PIPA was created under a partnership between the Government of Kiribati and the international non-governmental organizations-Conservation International and the New England Aquarium. PIPA has a unique conservation strategy as the first marine MPA to use a conservation contract mechanism with a corresponding Conservation Trust established to be both a sustainable financing mechanism and a check-and-balance to the oversight and maintenance of the MPA. As PIPA moves forward with its management objectives, it is well positioned to be a global model for large MPA design and implementation in similar contexts. The islands and shallow reefs have already shown benefits from protection, though the pending full closure of PIPA (and assessments thereof) will be critical for determining success of the MPA as a refuge for open-ocean pelagic and deep-sea marine life. As global ocean resources are continually being extracted to support a growing global population, PIPA's closure is both timely and of global significance.

Lipopolysaccharide detection by the innate immune system may be an uncommon defence strategy used in nature.

Since the publication of the Janeway's Pattern Recognition hypothesis in 1989, study of pathogen-associated molecular patterns (PAMPs) and their immuno-stimulatory activities has accelerated. Most studies in this area have been conducted in model organisms, which leaves many open questions about the universality of PAMP biology across living systems. Mammals have evolved multiple proteins that operate as receptors for the PAMP lipopolysaccharide (LPS) from Gram-negative bacteria, but LPS is not immuno-stimulatory in all eukaryotes. In this review, we examine the history of LPS as a PAMP in mammals, recent data on LPS structure and its ability to activate mammalian innate immune receptors, and how these activities compare across commonly studied eukaryotes. We discuss why LPS may have evolved to be immuno-stimulatory in some eukaryotes but not others and propose two hypotheses about the evolution of PAMP structure based on the ecology and environmental context of the organism in question. Understanding PAMP structures and stimulatory mechanisms across multi-cellular life will provide insights into the evolutionary origins of innate immunity and may lead to the discovery of new PAMP variations of scientific and therapeutic interest.

A review of microplastic impacts on seagrasses, epiphytes, and associated sediment communities.

Microplastics have been discovered ubiquitously in marine environments. While their accumulation is noted in seagrass ecosystems, little attention has yet been given to microplastic impacts on seagrass plants and their associated epiphytic and sediment communities. We initiate this discussion by synthesizing the potential impacts microplastics have on relevant seagrass plant, epiphyte, and sediment processes and functions. We suggest that microplastics may harm epiphytes and seagrasses via impalement and light/gas blockage, and increase local concentrations of toxins, causing a disruption in metabolic processes. Further, microplastics may alter nutrient cycling by inhibiting dinitrogen fixation by diazotrophs, preventing microbial processes, and reducing root nutrient uptake. They may also harm seagrass sediment communities via sediment characteristic alteration and organism complications associated with ingestion. All impacts will be exacerbated by the high trapping efficiency of seagrasses. As microplastics become a permanent and increasing member of seagrass ecosystems it will be pertinent to direct future research towards understanding the extent microplastics impact seagrass ecosystems.

My Deep Sea, My Backyard: a pilot study to build capacity for global deep-ocean exploration and research.

The deep ocean is the largest ecosystem on the planet, constituting greater than 90% of all habitable space. Over three-quarters of countries globally have deep ocean within their Exclusive Economic Zones. While maintaining deep-ocean function is key to ensuring planetary health, deficiencies in knowledge and governance, as well as inequitable global capacity, challenge our ability to safeguard the resilience of this vast realm, leaving the fate of the deep ocean in the hands of a few. Historically, deep-ocean scientific exploration and research have been the purview of a limited number of nations, resulting in most of humankind not knowing the deep ocean within their national jurisdiction or beyond. In this article, we highlight the inequities and need for increased deep-ocean knowledge generation, and discuss experiences in piloting an innovative project 'My Deep Sea, My Backyard' toward this goal. Recognizing that many deep-ocean endeavours take place in countries without deep-ocean access, this project aimed to reduce dependency on external expertise and promote local efforts in two small island developing states, Trinidad and Tobago and Kiribati, to explore their deep-sea backyards using comparatively low-cost technology while building lasting in-country capacity. We share lessons learned so future efforts can bring us closer to achieving this goal. This article is part of the theme issue 'Nurturing resilient marine ecosystems'.

Deep-sea microbes as tools to refine the rules of innate immune pattern recognition.

The assumption of near-universal bacterial detection by pattern recognition receptors is a foundation of immunology. The limits of this pattern recognition concept, however, remain undefined. As a test of this hypothesis, we determined whether mammalian cells can recognize bacteria that they have never had the natural opportunity to encounter. These bacteria were cultivated from the deep Pacific Ocean, where the genus Moritella was identified as a common constituent of the culturable microbiota. Most deep-sea bacteria contained cell wall lipopolysaccharide (LPS) structures that were expected to be immunostimulatory, and some deep-sea bacteria activated inflammatory responses from mammalian LPS receptors. However, LPS receptors were unable to detect 80% of deep-sea bacteria examined, with LPS acyl chain length being identified as a potential determinant of immunosilence. The inability of immune receptors to detect most bacteria from a different ecosystem suggests that pattern recognition strategies may be defined locally, not globally.

High resolution spatiotemporal patterns of seawater temperatures across the Belize Mesoamerican Barrier Reef.

Coral reefs are under increasingly severe threat from climate change and other anthropogenic stressors. Anomalously high seawater temperatures in particular are known to cause coral bleaching (loss of algal symbionts in the family Symbiodiniaceae), which frequently leads to coral mortality. Remote sensing of sea surface temperature (SST) has served as an invaluable tool for monitoring physical conditions that can lead to bleaching events over relatively large scales (e.g. few kms to 100 s of kms). But, it is also well known that seawater temperatures within a site can vary significantly across depths due to the combined influence of solar heating of surface waters, water column thermal stratification, and cooling from internal waves and upwelling. We deployed small autonomous benthic temperature sensors at depths ranging from 0-40 m in fore reef, back reef, and lagoonal reef habitats on the Belize Mesoamerican Barrier Reef System from 2000-2019. These data can be used to calculate depth-specific climatologies across reef depths and sites, and emphasize the dynamic and spatially-variable nature of coral reef physical environments.

Considering the rates of growth in two taxa of coral across Pacific islands.

Reef-building coral taxa demonstrate considerable flexibility and diversity in reproduction and growth mechanisms. Corals take advantage of this flexibility to increase or decrease size through clonal expansion and loss of live tissue area (i.e. via reproduction and mortality of constituent polyps). The biological lability of reef-building corals may be expected to map onto varying patterns of demography across environmental contexts which can contribute to geographic variation in population dynamics. Here we explore the patterns of growth of two common coral taxa, corymbose Pocillopora and massive Porites, across seven islands in the central and south Pacific. The islands span a natural gradient of environmental conditions, including a range of pelagic primary production, a metric linked to the relative availability of inorganic nutrients and heterotrophic resources for mixotrophic corals, and sea surface temperature and thermal histories. Over a multi-year sampling interval, most coral colonies experienced positive growth (greater planar area of live tissue in second relative to first time point), though the distributions of growth varied across islands. Island-level median growth did not relate simply to estimated pelagic primary productivity or temperature. However, at locations that experienced an extreme warm-water event during the sampling interval, most Porites colonies experienced net losses of live tissue and nearly all Pocillopora colonies experienced complete mortality. While descriptive statistics of demographics offer valuable insights into trends and variability in colony change through time, simplified models predicting growth patterns based on summarized oceanographic metrics appear inadequate for robust demographic prediction. We propose that the complexity of life history strategies among colonial reef-building corals introduces unique demographic flexibility for colonies to respond to a wide breadth of environmental conditions.

National-scale marine bioregions for the Southwest Pacific.

Existing marine bioregions covering the Pacific Ocean are conceptualised at spatial scales that are too broad for national marine spatial planning. Here, we developed the first combined oceanic and coastal marine bioregionalisation at national scales, delineating 262 deep-water and 103 reef-associated bioregions across the southwest Pacific. The deep-water bioregions were informed by thirty biophysical environmental variables. For reef-associated environments, records for 806 taxa at 7369 sites were used to predict the probability of observing taxa based on environmental variables. Both deep-water and reef-associated bioregions were defined with cluster analysis applied to the environmental variables and predicted species observation probabilities, respectively to classify areas with high taxonomic similarity. Local experts further refined the delineation of the bioregions at national scales for four countries. This work provides marine bioregions that enable the design of ecologically representative national systems of marine protected areas within offshore and inshore environments in the Pacific.

Evidence and patterns of tuna spawning inside a large no-take Marine Protected Area.

The Phoenix Islands Protected Area (PIPA), one of the world's largest marine protected areas, represents 11% of the exclusive economic zone of the Republic of Kiribati, which earns much of its GDP by selling tuna fishing licenses to foreign nations. We have determined that PIPA is a spawning area for skipjack (Katsuwonus pelamis), bigeye (Thunnus obesus), and yellowfin (Thunnus albacares) tunas. Our approach included sampling larvae on cruises in 2015-2017 and using a biological-physical model to estimate spawning locations for collected larvae. Temperature and chlorophyll conditions varied markedly due to observed ENSO states: El Niño (2015) and neutral (2016-2017). However, larval tuna distributions were similar amongst years. Generally, skipjack larvae were patchy and more abundant near PIPA's northeast corner, while Thunnus larvae exhibited lower and more even abundances. Genetic barcoding confirmed the presence of bigeye (Thunnus obesus) and yellowfin (Thunnus albacares) tuna larvae. Model simulations indicated that most of the larvae collected inside PIPA in 2015 were spawned inside, while stronger currents in 2016 moved more larvae across PIPA's boundaries. Larval distributions and relative spawning output simulations indicated that both focal taxa spawned inside PIPA in all 3 study years, demonstrating that PIPA is protecting viable tuna spawning habitat.

Free-living tube worm endosymbionts found at deep-sea vents.

Recent evidence suggests that deep-sea vestimentiferan tube worms acquire their endosymbiotic bacteria from the environment each generation; thus, free-living symbionts should exist. Here, free-living tube worm symbiont phylotypes were detected in vent seawater and in biofilms at multiple deep-sea vent habitats by PCR amplification, DNA sequence analysis, and fluorescence in situ hybridization. These findings support environmental transmission as a means of symbiont acquisition for deep-sea tube worms.

Thalassia testudinum as a potential vector for incorporating microplastics into benthic marine food webs.

Seagrasses are among the most productive shallow water ecosystems, serving a diverse assemblage of fish and invertebrates. Tropical seagrass communities are dominated by the turtle grass Thalassia testudinum, whose wide, flattened blades host diverse epibiont communities. Amidst its epibionts, T. testudinum may also be accumulating microplastics, which are a ubiquitous marine pollutant even in remote locales. To assess the extent of microplastic accumulation, seagrass samples were collected from Turneffe Atoll, which lies offshore but parallel with a major urban center. Seventy-five percent of Thalassia blades had encrusted microplastics, with microfibers occurring more than microbeads and chips by a ratio of 59:14. Grazers consumed seagrasses with higher densities of epibionts. Potential mechanisms for microplastic accumulation include entrapment by epibionts, or attachment via biofilms. This study is the first to document microplastics on marine vascular plants, suggesting that macroherbivory is a viable pathway for microplastic pollution to enter marine food webs.

The impact of autotrophic versus heterotrophic nutritional pathways on colony health and wound recovery in corals.

For animals that harbor photosynthetic symbionts within their tissues, such as corals, the different relative contributions of autotrophy versus heterotrophy to organismal energetic requirements have direct impacts on fitness. This is especially true for facultatively symbiotic corals, where the balance between host-caught and symbiont-produced energy can be altered substantially to meet the variable demands of a shifting environment. In this study, we utilized a temperate coral-algal system (the northern star coral, Astrangia poculata, and its photosynthetic endosymbiont, Symbiodinium psygmophilum) to explore the impacts of nutritional sourcing on the host's health and ability to regenerate experimentally excised polyps. For fed and starved colonies, wound healing and total colony tissue cover were differentially impacted by heterotrophy versus autotrophy. There was an additive impact of positive nutritional and symbiotic states on a coral's ability to initiate healing, but a greater influence of symbiont state on the recovery of lost tissue at the lesion site and complete polyp regeneration. On the other hand, regardless of symbiont state, fed corals maintained a higher overall colony tissue cover, which also enabled more active host behavior (polyp extension) and endosymbiont behavior (photosynthetic ability of Symbiondinium). Overall, we determined that the impact of nutritional state and symbiotic state varied between biological functions, suggesting a diversity in energetic sourcing for each of these processes.

Shipboard design and fabrication of custom 3D-printed soft robotic manipulators for the investigation of delicate deep-sea organisms.

Soft robotics is an emerging technology that has shown considerable promise in deep-sea marine biological applications. It is particularly useful in facilitating delicate interactions with fragile marine organisms. This study describes the shipboard design, 3D printing and integration of custom soft robotic manipulators for investigating and interacting with deep-sea organisms. Soft robotics manipulators were tested down to 2224m via a Remotely-Operated Vehicle (ROV) in the Phoenix Islands Protected Area (PIPA) and facilitated the study of a diverse suite of soft-bodied and fragile marine life. Instantaneous feedback from the ROV pilots and biologists allowed for rapid re-design, such as adding "fingernails", and re-fabrication of soft manipulators at sea. These were then used to successfully grasp fragile deep-sea animals, such as goniasterids and holothurians, which have historically been difficult to collect undamaged via rigid mechanical arms and suction samplers. As scientific expeditions to remote parts of the world are costly and lengthy to plan, on-the-fly soft robot actuator printing offers a real-time solution to better understand and interact with delicate deep-sea environments, soft-bodied, brittle, and otherwise fragile organisms. This also offers a less invasive means of interacting with slow-growing deep marine organisms, some of which can be up to 18,000 years old.

Season, but not symbiont state, drives microbiome structure in the temperate coral Astrangia poculata.

BACKGROUND: Understanding the associations among corals, their photosynthetic zooxanthella symbionts (Symbiodinium), and coral-associated prokaryotic microbiomes is critical for predicting the fidelity and strength of coral symbioses in the face of growing environmental threats. Most coral-microbiome associations are beneficial, yet the mechanisms that determine the composition of the coral microbiome remain largely unknown. Here, we characterized microbiome diversity in the temperate, facultatively symbiotic coral Astrangia poculata at four seasonal time points near the northernmost limit of the species range. The facultative nature of this system allowed us to test seasonal influence and symbiotic state (Symbiodinium density in the coral) on microbiome community composition. RESULTS: Change in season had a strong effect on A. poculata microbiome composition. The seasonal shift was greatest upon the winter to spring transition, during which time A. poculata microbiome composition became more similar among host individuals. Within each of the four seasons, microbiome composition differed significantly from that of surrounding seawater but was surprisingly uniform between symbiotic and aposymbiotic corals, even in summer, when differences in Symbiodinium density between brown and white colonies are the highest, indicating that the observed seasonal shifts are not likely due to fluctuations in Symbiodinium density. CONCLUSIONS: Our results suggest that symbiotic state may not be a primary driver of coral microbial community organization in A. poculata, which is a surprise given the long-held assumption that excess photosynthate is of importance to coral-associated microbes. Rather, other environmental or host factors, in this case, seasonal changes in host physiology associated with winter quiescence, may drive microbiome diversity. Additional studies of A. poculata and other facultatively symbiotic corals will provide important comparisons to studies of reef-building tropical corals and therefore help to identify basic principles of coral microbiome assembly, as well as functional relationships among holobiont members.

A connection between colony biomass and death in Caribbean reef-building corals.

Increased sea-surface temperatures linked to warming climate threaten coral reef ecosystems globally. To better understand how corals and their endosymbiotic dinoflagellates (Symbiodinium spp.) respond to environmental change, tissue biomass and Symbiodinium density of seven coral species were measured on various reefs approximately every four months for up to thirteen years in the Upper Florida Keys, United States (1994-2007), eleven years in the Exuma Cays, Bahamas (1995-2006), and four years in Puerto Morelos, Mexico (2003-2007). For six out of seven coral species, tissue biomass correlated with Symbiodinium density. Within a particular coral species, tissue biomasses and Symbiodinium densities varied regionally according to the following trends: Mexico≥Florida Keys≥Bahamas. Average tissue biomasses and symbiont cell densities were generally higher in shallow habitats (1-4 m) compared to deeper-dwelling conspecifics (12-15 m). Most colonies that were sampled displayed seasonal fluctuations in biomass and endosymbiont density related to annual temperature variations. During the bleaching episodes of 1998 and 2005, five out of seven species that were exposed to unusually high temperatures exhibited significant decreases in symbiotic algae that, in certain cases, preceded further decreases in tissue biomass. Following bleaching, Montastraea spp. colonies with low relative biomass levels died, whereas colonies with higher biomass levels survived. Bleaching- or disease-associated mortality was also observed in Acropora cervicornis colonies; compared to A. palmata, all A. cervicornis colonies experienced low biomass values. Such patterns suggest that Montastraea spp. and possibly other coral species with relatively low biomass experience increased susceptibility to death following bleaching or other stressors than do conspecifics with higher tissue biomass levels.

Crawling to collapse: ecologically unsound ornamental invertebrate fisheries.

BACKGROUND: Fishery management has historically been an inexact and reactionary discipline, often taking action only after a critical stock suffers overfishing or collapse. The invertebrate ornamental fishery in the State of Florida, with increasing catches over a more diverse array of species, is poised for collapse. Current management is static and the lack of an adaptive strategy will not allow for adequate responses associated with managing this multi-species fishery. The last decade has seen aquarium hobbyists shift their display preference from fish-only tanks to miniature reef ecosystems that include many invertebrate species, creating increased demand without proper oversight. The once small ornamental fishery has become an invertebrate-dominated major industry supplying five continents. METHODOLOGY/PRINCIPAL FINDINGS: Here, we analyzed the Florida Marine Life Fishery (FLML) landing data from 1994 to 2007 for all invertebrate species. The data were organized to reflect both ecosystem purpose (in the wild) and ecosystem services (commodities) for each reported species to address the following question: Are ornamental invertebrates being exploited for their fundamental ecosystem services and economic value at the expense of reef resilience? We found that 9 million individuals were collected in 2007, 6 million of which were grazers. CONCLUSIONS/SIGNIFICANCE: The number of grazers now exceeds, by two-fold, the number of specimens collected for curio and ornamental purposes altogether, representing a major categorical shift. In general, landings have increased 10-fold since 1994, though the number of licenses has been dramatically reduced. Thus, despite current management strategies, the FLML Fishery appears to be crawling to collapse.