Kelp carbon sink potential decreases with warming due to accelerating decomposition.

Cycling of organic carbon in the ocean has the potential to mitigate or exacerbate global climate change, but major questions remain about the environmental controls on organic carbon flux in the coastal zone. Here, we used a field experiment distributed across 28° of latitude, and the entire range of 2 dominant kelp species in the northern hemisphere, to measure decomposition rates of kelp detritus on the seafloor in relation to local environmental factors. Detritus decomposition in both species were strongly related to ocean temperature and initial carbon content, with higher rates of biomass loss at lower latitudes with warmer temperatures. Our experiment showed slow overall decomposition and turnover of kelp detritus and modeling of coastal residence times at our study sites revealed that a significant portion of this production can remain intact long enough to reach deep marine sinks. The results suggest that decomposition of these kelp species could accelerate with ocean warming and that low-latitude kelp forests could experience the greatest increase in remineralization with a 9% to 42% reduced potential for transport to long-term ocean sinks under short-term (RCP4.5) and long-term (RCP8.5) warming scenarios. However, slow decomposition at high latitudes, where kelp abundance is predicted to expand, indicates potential for increasing kelp-carbon sinks in cooler (northern) regions. Our findings reveal an important latitudinal gradient in coastal ecosystem function that provides an improved capacity to predict the implications of ocean warming on carbon cycling. Broad-scale patterns in organic carbon decomposition revealed here can be used to identify hotspots of carbon sequestration potential and resolve relationships between carbon cycling processes and ocean climate at a global scale.

The microbiome of the habitat-forming brown alga Fucus vesiculosus (Phaeophyceae) has similar cross-Atlantic structure that reflects past and present drivers1.

Latitudinal diversity gradients have provided many insights into species differentiation and community processes. In the well-studied intertidal zone, however, little is known about latitudinal diversity in microbiomes associated with habitat-forming hosts. We investigated microbiomes of Fucus vesiculosus because of deep understanding of this model system and its latitudinally large, cross-Atlantic range. Given multiple effects of photoperiod, we predicted that cross-Atlantic microbiomes of the Fucus microbiome would be similar at similar latitudes and correlate with environmental factors. We found that community structure and individual amplicon sequencing variants (ASVs) showed distinctive latitudinal distributions, but alpha diversity did not. Latitudinal differentiation was mostly driven by ASVs that were more abundant in cold temperate to subarctic (e.g., Granulosicoccus_t3260, Burkholderia/Caballeronia/Paraburkholderia_t8371) or warm temperate (Pleurocapsa_t10392) latitudes. Their latitudinal distributions correlated with different humidity, tidal heights, and air/sea temperatures, but rarely with irradiance or photoperiod. Many ASVs in potentially symbiotic genera displayed novel phylogenetic biodiversity with differential distributions among tissues and regions, including closely related ASVs with differing north-south distributions that correlated with Fucus phylogeography. An apparent southern range contraction of F. vesiculosus in the NW Atlantic on the North Carolina coast mimics that recently observed in the NE Atlantic. We suggest cross-Atlantic microbial structure of F. vesiculosus is related to a combination of past (glacial-cycle) and contemporary environmental drivers.

Consistency in a marine algal-grazer interaction over multiple scales.

Coralline algae are conspicuous members of many marine assemblages, especially those characterized by intense grazing pressure. We explored whether articulated species, especially Corallina vancouveriensis, depend on grazing invertebrates to both establish and flourish in an exposed rocky intertidal setting, and whether this plant-grazer relationship varied over more than three orders of magnitude (≈100->300,000 µm). Three experimental manipulations, supplemented by observations on recruitment, demonstrated that (i) C. vancouveriensis failed to recover rapidly from disturbed areas when grazers were experimentally excluded; (ii) recruitment occurred in the presence of grazers; (iii) increasing surface texture of molded surfaces enhanced coralline recruitment more when grazers were present; and (iv) settlement occurred predominately in microtopographical low areas of a molded surface, whereas a competitively superior fleshy red alga tended to recruit to high areas. These results confirm that coralline algal establishment and persistence are enhanced by grazers and reveal that this relationship is consistent over a range of biologically relevant scales.

Patterns and scales of connectivity: temporal stability and variation within a marine metapopulation.

Because many marine invertebrates have a dispersive planktonic phase, the spatial scale of demographic, connectivity among local populations remains a key, but elusive, parameter driving population and metapopulation dynamics. However, temporal variation in the scale of connectivity remains largely undocumented, despite its recognized importance for predicting population responses to environmental changes. To assess the temporal stability of metapopulation connectivity, we conducted a large-scale survey of a blue mussel (Mytilus spp.) metapopulation for five years along a 100-km section of coastline of the Gaspé Peninsula, Québec, Canada. For each year, we estimated the scale of demographic coupling among 27-29 sites within our study region, using the spatial cross-covariance between adult abundance and recruit density across sites. Despite large interannual variability in overall recruit abundance, our analysis revealed stationary spatial distributions of adult and recruit abundance. More importantly, our analysis revealed a consistent demographic coupling among populations at a distance ranging from 12 to 24 km in all but one of the five years studied. The scale of connectivity in this system is thus temporally stable, but can occasionally show irregular fluctuations, and our results provide evidence in support of the integration of time-varying connectivity to marine metapopulation and reserve network theories.

Drift Algal Accumulation in Ice Scour Pits Provides an Underestimated Ecological Subsidy in a Novel Antarctic Soft-Sediment Habitat.

Ice scouring is one of the strongest agents of disturbance in nearshore environments at high latitudes. In depths, less than 20 m, grounding icebergs reshape the soft-sediment seabed by gouging furrows called ice pits. Large amounts of drift algae (up to 5.6 kg/m2) that would otherwise be transported to deeper water accumulate inside these features, representing an underestimated subsidy. Our work documents the distribution and dimensions of ice pits in Fildes Bay, Antarctica, and evaluates their relationship to the biomass and species composition of algae found within them. It also assesses the rates of deposition and advective loss of algae in the pits. The 17 ice pits found in the study area covered only 4.2% of the seabed but contained 98% of drift algal biomass, i.e., 60 times the density (kg/m2) of the surrounding seabed. Larger ice pits had larger and denser algal accumulations than small pits and had different species compositions. The accumulations were stable over time: experimentally cleared pits regained initial biomass levels after one year, and advective loss was less than 15% annually. Further research is needed to understand the impacts of ice scouring and subsequent algal retention on ecosystem functioning in this rapidly changing polar environment.

Detecting the impacts of notorious invaders: experiments versus observations in the invasion of eelgrass meadows by the green seaweed Codium fragile.

Biological invasions can vary in the extent of their effects on indigenous communities but predicting impacts for particular systems remains difficult. In coastal marine ecosystems, the green seaweed Codium fragile ssp. fragile is a notorious invader with its reputation based on studies conducted largely on rocky shores. The green seaweed has recently invaded soft-bottom eelgrass communities by attaching epiphytically to eelgrass (Zostera marina) rhizomes, thereby creating the potential for disruption of these coastal habitats through competition or disturbance. We investigated the effect of this invader on various aspects of eelgrass performance (shoot density and length, shoot growth, above- and below-ground biomass, carbohydrate storage) using both small-scale manipulative and large-scale observational experiments. Manipulative experiments that varied Codium abundance demonstrated clear negative effects over a 4-month period on shoot density and carbohydrate reserves, but only for high, but realistic, Codium biomass levels. Light levels were much lower under canopies for high and medium density Codium treatments relative to low and control Codium cover treatments, suggesting that shading may influence eelgrass growing under the algal cover. In contrast, these effects were either not detectable or very weak when examined correlatively with field surveys conducted at larger spatial scales, even for sites that had been invaded for over 4 years. It is premature to extend generalizations of Codium's impact derived from studies in other systems to eelgrass communities; further efforts are required to assess the long-term threats that the alga poses to this ecosystem. This study demonstrates the need to investigate impacts of invasions over multiple scales, especially those that incorporate the temporal and spatial heterogeneity of the invader's abundance.

Historical invasions of the intertidal zone of Atlantic North America associated with distinctive patterns of trade and emigration.

Early invasions of the North American shore occurred mainly via deposition of ballast rock, which effectively transported pieces of the intertidal zone across the Atlantic. From 1773-1861, >880 European ships entered Pictou Harbor, Nova Scotia, as a result of emigration and trade from Europe. The rockweed Fucus serratus (1868) and the snail Littorina littorea ( approximately 1840) were found in Pictou during this same period. With shipping records (a proxy for propagule pressure) to guide sampling, we used F. serratus as a model to examine the introductions because of its relatively low genetic diversity and dispersal capability. Microsatellite markers and assignment tests revealed 2 introductions of the rockweed into Nova Scotia: 1 from Galway (Ireland) to Pictou and the other from Greenock (Scotland) to western Cape Breton Island. To examine whether a high-diversity, high-dispersing species might have similar pathways of introduction, we analyzed L. littorea, using cytochrome b haplotypes. Eight of the 9 Pictou haplotypes were found in snails collected from Ireland and Scotland. Our results contribute to a broader understanding of marine communities, because these 2 conspicuous species are likely to be the tip of an "invasion iceberg" to the NW Atlantic from Great Britain and Ireland in the 19th Century.

Seascapes and foraging success: Movement and resource discovery by a benthic marine herbivore.

Spatially concentrated resources result in patch-based foraging, wherein the detection and choice of patches as well as the process of locating and exploiting resource patches involve moving through an explicit landscape composed of both resources and barriers to movement. An understanding of behavioral responses to resources and barriers is key to interpreting observed ecological patterns. We examined the process of resource discovery in the context of a heterogeneous seascape using sea urchins and drift kelp in urchin barrens as a model system. Under field conditions, we manipulated both the presence of a highly valuable resource (drift kelp) and a barrier to movement (sandy substratum) to test the interacting influence of these two factors on the process of resource discovery in barren grounds by urchins. We removed all foraging urchins (Strongylocentrotus droebachiensis) from replicate areas and monitored urchin recolonization and kelp consumption. We tested two hypotheses: (1) unstable substratum is a barrier to urchin movement and (2) the movement behavior of sea urchins is modified by the presence of drift kelp. Very few urchins were found on sand, sand was a permeable barrier to urchin movement, and the permeability of this barrier varied between sites. In general, partial recolonization occurred strikingly rapidly, but sand slowed the consumption of drift kelp by limiting the number of urchins. Differences in the permeability of sand barriers between sites could be driven by differences in the size structure of urchin populations, indicating size-specific environmental effects on foraging behavior. We demonstrate the influence of patchy seascapes in modulating grazing intensity in barren grounds through modifications of foraging behavior. Behavioral processes modified by environmental barriers play an important role in determining grazing pressure, the existence of refuges for new algal recruits, and ultimately the dynamics of urchin-algal interactions in barren grounds.

Effects of sediment on spore performance as a potential constraint on kelp distribution.

Kelp habitats contribute to marine productivity and diversity, making understanding the constraints on their distribution important. In the Gulf of St. Lawrence, Alaria esculenta occupies a subset of Saccharina latissima's range. Since tolerance to sedimentation by early life stages was suggested to cause this contrasting distribution, we tested the influence of sediment levels on spore attachment and development. For both species, the proportion of attached spores that developed decreased with increasing sediment. However, spore attachment and gametophyte density increased with sediment concentration but only for Saccharina. At the maximum sediment level examined, spore attachment and gametophyte densities of the two species were similar, contrary to the idea that sediment effects on early life stages explain differences in adult distribution. Further investigation, particularly with higher sediment loads, is required to confirm this conclusion. As turbidity is increasing globally, understanding the mechanisms underpinning changes in seaweed distribution will facilitate appropriate local-scale management.

Bacterial Communities Show Algal Host (Fucus spp.)/Zone Differentiation Across the Stress Gradient of the Intertidal Zone.

The intertidal zone often has varying levels of environmental stresses (desiccation, temperature, light) that result in highly stress-tolerant macrobiota occupying the upper zone while less tolerant species occupy the lower zone, but little comparative information is available for intertidal bacteria. Here we describe natural (unmanipulated) bacterial communities of three Fucus congeners (F. spiralis, high zone; F. vesiculosus, mid zone; F. distichus, low zone) as well as those of F. vesiculosus transplanted to the high zone (Dry and Watered treatments) and to the mid zone (Procedural Control) during summer in Maine (United States). We predicted that bacterial communities would be different among the differently zoned natural congeners, and that higher levels of desiccation stress in the high zone would cause bacterial communities of Dry transplants to become similar to F. spiralis, whereas relieving desiccation stress on Watered transplants would maintain the mid-zone F. vesiculosus bacterial community. Bacteria were identified as amplicon sequence variants (ASVs) after sequencing the V4 hypervariable region of the 16S rRNA gene. Microbiome composition and structure were significantly different between the differently zoned congeners at each tissue type (holdfasts, receptacles, vegetative tips). ASVs significantly associated with the mid-zone congener were frequently also present on the high-zone or low-zone congener, whereas overlap in ASVs between the high-zone and low-zone congeners was rare. Only 7 of 6,320 total ASVs were shared among tissues over all congeners and transplant treatments. Holdfast bacterial community composition of Dry transplants was not significantly different from that of F. spiralis, but Watered holdfast communities were significantly different from those of F. spiralis and not significantly different from those of procedural controls. Additional stressor(s) appeared important, because bacterial communities of Dry and Watered transplants were only marginally different from each other (p = 0.059). The relative abundance of Rhodobacteraceae associated with holdfasts generally correlated with environmental stress with highest abundance associated with F. spiralis and the two high-zone transplant treatments. These findings suggest that the abiotic stressors that shape distributional patterns of host species also affect their bacterial communities.

First mussel settlement observed in Antarctica reveals the potential for future invasions.

Global biodiversity is both declining and being redistributed in response to multiple drivers characterizing the Anthropocene, including synergies between biological invasions and climate change. The Antarctic marine benthos may constitute the last biogeographic realm where barriers (oceanographic currents, climatic gradients) have not yet been broken. Here we report the successful settlement of a cohort of Mytilus cf. platensis in a shallow subtidal habitat of the South Shetland Islands in 2019, which demonstrates the ability of this species to complete its early life stages in this extreme environment. Genetic analyses and shipping records show that this observation is consistent with the dominant vectors and pathways linking southern Patagonia with the Antarctic Peninsula and demonstrates the potential for impending invasions of Antarctic ecosystems.

Dynamics of recruitment and establishment of the invasive seaweed Codium fragile within an eelgrass habitat.

Knowledge of the potential distribution (i.e. abundance and spatial extent) of an invasive species is important to estimating its potential impacts on recipient communities. Most previous studies have focused on the potential spatial extent of invasive species populations at regional scales, but little is known on how species successfully recruit and establish at more local scales. In this study, we examined how recruitment of the green alga Codium fragile ssp. fragile (hereafter Codium) can vary spatially and the environmental factors associated with Codium establishment in eelgrass (Zostera marina) beds. Standardized recruitment blocks (65 blocks in a 720 × 240 m2 grid) were used to monitor the number of Codium recruits, juveniles and adults over 2 years. Environmental factors (depth, relative water flow, light and temperature) and attributes of the surrounding macrophyte assemblage (eelgrass density, eelgrass length, Codium biomass) were also measured. Recruitment occurred on all blocks or nearby artificial structures (i.e. buoys) and mainly originated from button stages (i.e. female gametes or utricles). Contrary to other studies, the abundance of Codium (recruits, juveniles and adults) was best predicted by the density of the native canopy-forming species, Z. marina, which highlights a positive interaction between native and non-native canopy-forming species. Seasonal variation in recruitment was observed; it was lower during the summer. Recruitment did not show any distinct spatial pattern (e.g. gradient or patch), but the same spatial pattern of recruitment was observed every sampling date, suggesting that there are "hotspots" for recruitment. In general, the total number of Codium fronds observed on a block at the end of the experiment was positively correlated with the cumulative number of recruits. However, recruitment occurred on some blocks but recruits never grew, suggesting that some environmental factors limit Codium distribution and abundance in eelgrass beds. Overall, the assessment of Codium recruitment over 2 years showed that the colonization of suitable locations by Codium within seagrass beds may take several years and that some factors may not only limit, but also inhibit Codium expansion within eelgrass beds.

Dispersal and recruitment of a canopy-forming intertidal alga: the relative roles of propagule availability and post-settlement processes.

The daily settlement of eggs and zygotes of the monoecious brown alga Pelvetia compressa (J. Agardh) De Toni was measured on artificial substrata in areas inside and outside patches of adults in the high intertidal zone of central California. Settlement was generally 1-2 orders of magnitude higher under the adult canopy. This pattern seems to be due to the synchronous release of gametes during the daytime low tide. The release of gametes also appears periodic over longer time scales (e.g., 3- and 14-day cycles). In spite of the high availability of propagules under the adult canopy, juveniles were most abundant outside patches, where propagule availability was lower. In both areas, juveniles were disproportionately associated with patches of a red algal turf [primarily Endocladia muricata (Postels & Ruprecht) J. Agardh and Masticarpus papillata (C. Agardh) Kützing]. The turf, which is less common under the P. compressa canopy, may offer protection from dislodgment, grazing, and/or desiccation and thus facilitate recruitment at this site. Overall, post-settlement processes appear more important in determining population structure than does the availability of propagules in areas in and around patches of adults. However, the apparent small range of dispersal of P. compressa may make propagule availability an important limitation to the establishment of new populations and may restrict gene flow between populations.

Sublethal stress in the intertidal zone: tidal emersion inhibits photosynthesis and retards development in embryos of the brown alga Pelvetia fastigiata.

The effect of tidal emersion on survivorship, photosynthesis and embryonic development was studied in 8 h old zygotes and 7 d old embryos of the intertidal brown alga Pelvetia fastigiata (J. Ag.) DeToni. Zygotes and embryos were outplanted for single low tides in the intertidal zone on the central coast of California (U.S.A.) during June, 1990. Both zygotes and embryos exhibited close to 100% survival when outplanted beneath the canopy of adult P. fastigiata. Embryos (7 d old) also exhibited high survival when outplanted in a red algal turf, the microhabitat where most successful recruitment occurs. However, zygotes (8 h old) experienced high mortality (65-90%) when outplanted in the turf microhabitat. Embryos and zygotes that survived emersion experienced sub-lethal stress that temporarily impaired light-saturated photosynthesis when plants were reimmersed in seawater. The effects of sub-lethal stress were more pronounced in 8 h old zygotes than 7 d embryos, and more severe in the turf microhabitat than beneath the adult Pelvetia canopy. Zygotes outplanted in the red algal turf did not re-establish net photosynthesis until at least 6 h after re-immersion. Photosynthesis was less inhibited in 8 h old zygotes outplanted beneath the adult Pelvetia canopy, and recovered to control (non-emersed) levels within 3 h of re-immersion. Embryos (7 d old) were able to achieve positive net photosynthesis immediately on re-immersion after emersion in the turf or canopy microhabitats. Emersion also retarded the rate of embryonic development in 8 h old zygotes, delaying the formation of primary rhizoids, which help to attach the plant to the substrate. For example, at 19 h post-fertilization, 75% of control (non-emersed) zygotes had developed rhizoids, compared to 3% and 30% for zygotes outplanted in the turf and canopy microhabitats. The different emersion responses of 8 h old zygotes and 7 d old embryos appeared to be related to their ability to tolerate cellular dehydration. Overall, our data suggest that the effects of sub-lethal stresses may have been underestimated in studies of intertidal ecology.

Optimizing early detection of non-indigenous species: estimating the scale of dispersal of a nascent population of the invasive tunicate Ciona intestinalis (L.).

Knowledge of dispersal and establishment during the early stages of invasion is essential for allocating monitoring effort, detecting nascent populations and predicting spread. The scarcity of these data, however, provides little guidance for monitoring programs. Here we present data on the adult distribution and the subsequent pattern of larval recruitment from a nascent population of the invasive tunicate Ciona intestinalis in Prince Edward Island, Canada. Existing niche models indicate the entire study site is suitable for recruitment, suggesting an equal probability of detection throughout the site. In contrast, we found a heterogeneous pattern of larval recruitment, including areas of zero recruitment. By fitting a dispersal kernel, we show Ciona is not capable of naturally dispersing between bays, restricting further spread, and provide guidance for future monitoring. Our results also highlight how large-scale models, although important, lack the small-scale patterns essential for monitoring and early detection of invasive species.

Forecasting the expansion of zebra mussels in the United States.

Because zebra mussels spread rapidly throughout the eastern United States in the late 1980s and early 1990s, their spread to the western United States has been expected. Overland dispersal into inland lakes and reservoirs, however, has occurred at a much slower rate than earlier spread via connected, navigable waterways. We forecasted the potential western spread of zebra mussels by predicting the overland movement of recreational boaters with a production-constrained gravity model. We also predicted the potential abundance of zebra mussels in two western reservoirs by comparing their water chemistry characteristics with those of water bodies with known abundances of zebra mussels. Most boats coming from waters infested with zebra mussels were taken to areas that already had zebra mussels, but a small proportion of such boats did travel west of the 100th meridian. If zebra mussels do establish in western U.S. water bodies, we predict that population densities could achieve similar levels to those in the Midwestern United States, where zebra mussels have caused considerable economic and ecological impacts. Our analyses suggest that the dispersal of zebra mussels to the western United States is an event of low probability but potentially high impact on native biodiversity and human infrastructure. Combining these results with economic analyses could help determine appropriate investment levels in prevention and control strategies.