Rewilding the Sea with Domesticated Seagrass.

It is well known that seagrass meadows sequester atmospheric carbon dioxide, protect coasts, provide nurseries for global fisheries, and enhance biodiversity. Large-scale restoration of lost seagrass meadows is urgently needed to revive these planetary ecosystem services, but sourcing donor material from natural meadows would further decline them. Therefore, we advocate the domestication and mariculture of seagrasses in order to produce the large quantities of seed needed for successful rewilding of the sea with seagrass meadows. We provide a roadmap for our proposed solution and show that 44% of seagrass species have promising reproductive traits for domestication and rewilding by seeds. The principle of partially domesticating species to enable subsequent large-scale rewilding may form a successful shortcut to restore threatened keystone species and their vital ecosystem services.

Motile macrofauna associated with pelagic Sargassum in a Mexican reef lagoon.

Buildup of decaying pelagic Sargassum on the beaches and coasts of the Mexican Caribbean during the massive arrivals of 2015 and 2018 had detrimental impacts on the environment and tourist industry. To avoid ecological and economic impacts from massive beaching of Sargassum, it would be better to remove the pelagic algal masses while still at sea. However, out at sea, pelagic Sargassum rafts constitute an ecosystem with a diversified associated fauna and their removal could impact this fauna. We conducted a survey on the motile macrofauna associated to pelagic Sargassum rafts in the Puerto Morelos reef lagoon, Mexican Caribbean. Pelagic Sargassum was sampled with nets at 2 m, 50 m and 500 m from shore, at four sites during the months of September, October and November 2018. The 108 samples contained 10,296 individuals belonging to 32 taxa distributed over eight Phyla. The main phyla were Arthropoda (48%), Annelida (41%) and Mollusca (15%). Fish abundance was low (10 individuals) with only five species, of which three are typically associated with Sargassum rafts and two are common in seagrass meadows and coral reefs. Species composition and abundance of motile macrofauna varied with month and zone; the nearshore zone had the lowest abundance but there was no difference in the abundance of the fauna associated with rafts 50 or 500 m offshore. Three of the four most abundant species (together accounting for 89% of the individuals) were species typically associated with pelagic Sargassum, and the fourth was an amphipod that was only registered once near shore. Although more studies over larger time and spatial scales are required, these results suggest that the removal of pelagic Sargassum within the reef lagoon may not have a significant effect on local populations of motile macrofauna.

Facultative Annual Life Cycles in Seagrasses.

Plant species usually have either annual or perennial life cycles, but facultative annual species have annual or perennial populations depending on their environment. In terrestrial angiosperms, facultative annual species are rare, with wild rice being one of the few examples. Our review shows that in marine angiosperms (seagrasses) facultative annual species are more common: six (of 63) seagrass species are facultative annual. It concerns Zostera marina, Z. japonica, Halophila decipiens, H. beccarii, Ruppia maritima, and R. spiralis. The annual populations generally produce five times more seeds than their conspecific perennial populations. Facultative annual seagrass species occur worldwide. Populations of seagrasses are commonly perennial, but the facultative annual species had annual populations when exposed to desiccation, anoxia-related factors, shading, or heat stress. A system-wide 'experiment' (closure of two out of three connected estuaries for large-scale coastal protection works) showed that the initial annual Z. marina population could shift to a perennial life cycle within 5 years, depending on environmental circumstances. We discuss potential mechanisms and implications for plant culture. Further exploration of flexible life histories in plant species, and seagrasses in particular, may aid in answering questions about trade-offs between vegetative and sexual reproduction, and preprogrammed senescence.

Diversity of the holopelagic Sargassum microbiome from the Great Atlantic Sargassum Belt to coastal stranding locations.

The holopelagic brown macroalgae Sargassum natans and Sargassum fluitans form essential habitats for attached and mobile fauna which contributes to a unique biodiversity in the Atlantic Ocean. However, holopelagic Sargassum natans (genotype I & VIII) and Sargassum fluitans (genotype III) have begun forming large accumulations with subsequent strandings on the western coast of Africa, the Caribbean and northern Brazil, threatening local biodiversity of coastal ecosystems and triggering economic losses. Moreover, stranded masses of holopelagic Sargassum may introduce or facilitate growth of bacteria that are not normally abundant in coastal regions where Sargassum is washing ashore. Hitherto, it is not clear how the holopelagic Sargassum microbiome varies across its growing biogeographic range and what factors drive the microbial composition. We determined the microbiome associated with holopelagic Sargassum from the Great Atlantic Sargassum Belt to coastal stranding sites in Mexico and Florida. We characterized the Sargassum microbiome via amplicon sequencing of the 16S V4 region hypervariable region of the rRNA gene. The microbial community of holopelagic Sargassum was mainly composed of photo(hetero)trophs, organic matter degraders and potentially pathogenic bacteria from the Pseudomonadaceae, Rhodobacteraceae and Vibrionaceae. Sargassum genotypes S. natans I, S. natans VIII and S. fluitans III contained similar microbial families, but relative abundances and diversity varied. LEfSE analyses further indicated biomarker genera that were indicative of Sargassum S. natans I/VIII and S. fluitans III. The holopelagic Sargassum microbiome showed biogeographic patterning with high relative abundances of Vibrio spp., but additional work is required to determine whether that represents health risks in coastal environments. Our study informs coastal management policy, where the adverse sanitary effects of stranded Sargassum might impact the health of coastal ecosystems.

Element concentrations in pelagic Sargassum along the Mexican Caribbean coast in 2018-2019.

The massive influx of pelagic Sargassum spp. (sargasso) into the Mexican Caribbean Sea has caused major deterioration of the coastal environment and has affected the tourism industry as well as livelihoods since 2015. Species of Sargassum have high capacity to absorb metals; thus, leachates of sargasso may contribute to contamination by potentially toxic metals when they drain into the sea and into the groundwater when dumped in inadequate land deposits. Valorization of sargasso would contribute to sustainable management; therefore, knowledge on potentially toxic metal content is necessary to define possible uses of the algae. We present concentrations of 28 elements measured using a non-destructive X-ray fluorescence analyzer (XRF) in 63 samples of sargasso collected between August 2018 and June 2019 from eight localities along ∼370 km long coastline of the Mexican Caribbean Sea. The sargasso tissues contained detectable concentrations of Al, As, Ca, Cl, Cu, Fe, K, Mg, Mn, Mo, P, Pb, Rb, S, Si, Sr, Th, U, V, and Zn. The element concentration in sargasso varied on spatial and temporal scales, which likely depended on the previous trajectory of the pelagic masses, and whether these had (or had not) passed through contaminated areas. Total arsenic concentration varied between 24-172 ppm DW, exceeding the maximum limit for seaweed intended as animal fooder (40 ppm DW) in 86% of the samples. For valorization, we recommend analyses of metal contents as a mandatory practice or avoiding uses for nutritional purposes. The high arsenic content is also of concern for environmental contamination of the sea and aquifer.

Mimicry of emergent traits amplifies coastal restoration success.

Restoration is becoming a vital tool to counteract coastal ecosystem degradation. Modifying transplant designs of habitat-forming organisms from dispersed to clumped can amplify coastal restoration yields as it generates self-facilitation from emergent traits, i.e. traits not expressed by individuals or small clones, but that emerge in clumped individuals or large clones. Here, we advance restoration science by mimicking key emergent traits that locally suppress physical stress using biodegradable establishment structures. Experiments across (sub)tropical and temperate seagrass and salt marsh systems demonstrate greatly enhanced yields when individuals are transplanted within structures mimicking emergent traits that suppress waves or sediment mobility. Specifically, belowground mimics of dense root mats most facilitate seagrasses via sediment stabilization, while mimics of aboveground plant structures most facilitate marsh grasses by reducing stem movement. Mimicking key emergent traits may allow upscaling of restoration in many ecosystems that depend on self-facilitation for persistence, by constraining biological material requirements and implementation costs.

Nutrient availability induces community shifts in seagrass meadows grazed by turtles.

In the Caribbean, green turtles graze seagrass meadows dominated by Thalassia testudinum through rotational grazing, resulting in the creation of grazed and recovering (abandoned) patches surrounded by ungrazed seagrasses. We evaluated the seagrass community and its environment along a turtle grazing gradient; with the duration of (simulated) grazing as a proxy for the level of grazing pressure. The grazing levels consisted of Short-term (4 months clipping), Medium-term (8 months clipping), Long-term grazing (8 months of clipping in previously grazed areas), 8-months recovery of previously grazed patches, and ungrazed or unclipped patches as controls. We measured biomass and density of the seagrasses and rhizophytic algae, and changes in sediment parameters. Medium- and Long-term grazing promoted a shift in community species composition. At increasing grazing pressure, the total biomass of T. testudinum declined, whereas that of early-successional increased. Ammonium concentrations were highest in the patches of Medium-term (9.2 + 0.8 µM) and Long-term grazing levels (11.0 + 2.2 µM) and were lowest in the control areas (4.6 + 1.5 µM). T. testudinum is a late-successional species that maintains sediment nutrient concentrations at levels below the requirements of early-successional species when dominant. When the abundance of this species declines due to grazing, these resources become available, likely driving a shift in community composition toward a higher abundance of early-successional species.

Range-wide population genetic structure of the Caribbean marine angiosperm Thalassia testudinum.

Many marine species have widespread geographic ranges derived from their evolutionary and ecological history particularly their modes of dispersal. Seagrass (marine angiosperm) species have ranges that are unusually widespread, which is not unexpected following recent reviews of reproductive strategies demonstrating the potential for long-distance dispersal combined with longevity through clonality. An exemplar of these dual biological features is turtle grass (Thalassia testudinum) which is an ecologically important species throughout the tropical Atlantic region. Turtle grass has been documented to have long-distance dispersal via floating fruits and also extreme clonality and longevity. We hypothesize that across its range, Thalassia testudinum will have very limited regional population structure due to these characteristics and under typical models of population structure would expect to detect high levels of genetic connectivity. There are very few studies of range-wide genetic connectivity documented for seagrasses or other sessile marine species. This study presents a population genetic dataset that represents a geographic area exceeding 14,000 km2. Population genetic diversity was evaluated from 32 Thalassia testudinum populations sampled across the Caribbean and Gulf of Mexico. Genotypes were based on nine microsatellites, and haplotypes were based on chloroplast DNA sequences. Very limited phylogeographic signal from cpDNA reduced the potential comparative analyses possible. Multiple analytical clustering approaches on population genetic data revealed two significant genetic partitions: (a) the Caribbean and (b) the Gulf of Mexico. Genetic diversity was high (H E = 0.641), and isolation by distance was significant; gene flow and migration estimates across the entire range were however modest, we suggest that the frequency of successful recruitment across the range is uncommon. Thalassia testudinum maintains genetic diversity across its entire distribution range. The genetic split may be explained by genetic drift during recolonization from refugia following relatively recent reduction in available habitat such as the last glacial maxima.

Severe impacts of brown tides caused by Sargassum spp. on near-shore Caribbean seagrass communities.

From mid-2014 until the end of 2015, the Mexican Caribbean coast experienced a massive influx of drifting Sargassum spp. that accumulated on the shores, resulting in build-up of decaying beach-cast material and near-shore murky brown waters (Sargassum-brown-tides, Sbt). The effects of Sbt on four near-shore waters included reduction in light, oxygen (hypoxia or anoxia) and pH. The monthly influx of nitrogen, and phosphorus by drifting Sargassum spp. was estimated at 6150 and 61kgkm-1 respectively, resulting in eutrophication. Near-shore seagrass meadows dominated by Thalassia testudinum were replaced by a community dominated by calcareous rhizophytic algae and drifting algae and/or epiphytes, resulting in 61.6-99.5% loss of below-ground biomass. Near-shore corals suffered total or partial mortality. Recovery of affected seagrass meadows may take years or even decades, or changes could be permanent if massive influxes of Sargassum spp. recur.

The fundamental role of ecological feedback mechanisms for the adaptive management of seagrass ecosystems - a review.

Seagrass meadows are vital ecosystems in coastal zones worldwide, but are also under global threat. One of the major hurdles restricting the success of seagrass conservation and restoration is our limited understanding of ecological feedback mechanisms. In these ecosystems, multiple, self-reinforcing feedbacks can undermine conservation efforts by masking environmental impacts until the decline is precipitous, or alternatively they can inhibit seagrass recovery in spite of restoration efforts. However, no clear framework yet exists for identifying or dealing with feedbacks to improve the management of seagrass ecosystems. Here we review the causes and consequences of multiple feedbacks between seagrass and biotic and/or abiotic processes. We demonstrate how feedbacks have the potential to impose or reinforce regimes of either seagrass dominance or unvegetated substrate, and how the strength and importance of these feedbacks vary across environmental gradients. Although a myriad of feedbacks have now been identified, the co-occurrence and likely interaction among feedbacks has largely been overlooked to date due to difficulties in analysis and detection. Here we take a fundamental step forward by modelling the interactions among two distinct above- and belowground feedbacks to demonstrate that interacting feedbacks are likely to be important for ecosystem resilience. On this basis, we propose a five-step adaptive management plan to address feedback dynamics for effective conservation and restoration strategies. The management plan provides guidance to aid in the identification and prioritisation of likely feedbacks in different seagrass ecosystems.

Experimental evidence of pollination in marine flowers by invertebrate fauna.

Pollen transport by water-flow (hydrophily) is a typical, and almost exclusive, adaptation of plants to life in the marine environment. It is thought that, unlike terrestrial environments, animals are not involved in pollination in the sea. The male flowers of the tropical marine angiosperm Thalassia testudinum open-up and release pollen in mucilage at night when invertebrate fauna is active. Here we present experimental evidence that, in the absence of water-flow, these invertebrates visit the flowers, carry and transfer mucilage mass with embedded pollen from the male flowers to the stigmas of the female flowers. Pollen tubes are formed on the stigmas, indicating that pollination is successful. Thus, T. testudinum has mixed abiotic-biotic pollination. We propose a zoobenthophilous pollination syndrome (pollen transfer in the benthic zone by invertebrate animals) which shares many characteristics with hydrophily, but flowers are expected to open-up during the night.

Caribbean-wide, long-term study of seagrass beds reveals local variations, shifts in community structure and occasional collapse.

The CARICOMP monitoring network gathered standardized data from 52 seagrass sampling stations at 22 sites (mostly Thalassia testudinum-dominated beds in reef systems) across the Wider Caribbean twice a year over the period 1993 to 2007 (and in some cases up to 2012). Wide variations in community total biomass (285 to >2000 g dry m(-2)) and annual foliar productivity of the dominant seagrass T. testudinum (<200 and >2000 g dry m(-2)) were found among sites. Solar-cycle related intra-annual variations in T. testudinum leaf productivity were detected at latitudes > 16°N. Hurricanes had little to no long-term effects on these well-developed seagrass communities, except for 1 station, where the vegetation was lost by burial below ∼1 m sand. At two sites (5 stations), the seagrass beds collapsed due to excessive grazing by turtles or sea-urchins (the latter in combination with human impact and storms). The low-cost methods of this regional-scale monitoring program were sufficient to detect long-term shifts in the communities, and fifteen (43%) out of 35 long-term monitoring stations (at 17 sites) showed trends in seagrass communities consistent with expected changes under environmental deterioration.