Marine Foundation Species Research Articles

A facultative mutualistic feedback enhances the stability of tropical intertidal seagrass beds

Marine foundation species such as corals, seagrasses, salt marsh plants, and mangrove trees are increasingly found to engage in mutualistic interactions. Because mutualisms by their very nature generate a positive feedback between the species, subtle environmental impacts on one of the species involved may trigger mutualism breakdown, potentially leading to ecosystem regime shifts. Using an empirically parameterized model, we investigate a facultative mutualism between seagrass and lucinid bivalves with endosymbiotic sulfide-oxidizing gill bacteria in a tropical intertidal ecosystem. Model predictions for our system show that, by alleviating the build-up of toxic sulfide, this mutualism maintains an otherwise intrinsically unstable seagrass ecosystem. However, an increase in seagrass mortality above natural levels, due to e.g. desiccation stress, triggers mutualism breakdown. This pushes the system in collapse-and-recovery dynamics (‘slow-fast cycles’) characterized by long-term persistent states of bare and seagrass-dominated, with rapid transitions in between. Model results were consistent with remote sensing analyses that suggest feedback-mediated state shifts induced by desiccation. Overall, our combined theoretical and empirical results illustrate the potential of mutualistic feedbacks to stabilize ecosystems, but also reveal an important drawback as small environmental changes may trigger shifts. We therefore suggest that mutualisms should be considered for marine conservation and restoration of seagrass beds.

Molecular level responses to chronic versus pulse nutrient loading in the seagrass Posidonia oceanica undergoing herbivore pressure.

Seagrasses are key marine foundation species, currently declining due to the compounded action of global and regional anthropogenic stressors. Eutrophication has been associated with seagrass decline, while grazing has been traditionally considered to be a natural disturbance with a relatively low impact on seagrasses. In the recent years, this assumption has been revisited. Here, by means of a 16-month field-experiment, we investigated the molecular mechanisms driving the long-term response of Posidonia oceanica to the combination of nutrient enrichment, either as a chronic (press) or pulse disturbance, and herbivory. Changes in expression levels of 19 target genes involved in key steps of photosynthesis, nutrient assimilation, chlorophyll metabolism, oxidative-stress response and plant defense were evaluated through reverse transcription-quantitative polymerase chain reaction (RT-qPCR). High herbivore pressure affected the molecular response of P. oceanica more dramatically than did enhanced nutrient levels, altering the expression of genes involved in plant tolerance and resistance traits, such as photosynthesis and defense mechanisms. Genes involved in carbon fixation and N assimilation modulated the response of plants to high nutrient levels. Availability of resources seems to modify P. oceanica response to herbivory, where the upregulation of a nitrate transporter gene was accompanied by the decline in the expression of nitrate reductase in the leaves, suggesting a change in plant-nutrient allocation strategy. Finally, press and pulse fertilizations altered nitrate uptake and reduction-related genes in opposite ways, suggesting that taking into account the temporal regime of nutrient loading is important to assess the physiological response of seagrasses to eutrophication.

Giant kelp, Macrocystis pyrifera, increases faunal diversity through physical engineering.

Foundation species define the ecosystems they live in, but ecologists have often characterized dominant plants as foundational without supporting evidence. Giant kelp has long been considered a marine foundation species due to its complex structure and high productivity; however, there is little quantitative evidence to evaluate this. Here, we apply structural equation modelling to a 15-year time series of reef community data to evaluate how giant kelp affects the reef community. Although species richness was positively associated with giant kelp biomass, most direct paths did not involve giant kelp. Instead, the foundational qualities of giant kelp were driven mostly by indirect effects attributed to its dominant physical structure and associated engineering influence on the ecosystem, rather than by its use as food by invertebrates and fishes. Giant kelp structure has indirect effects because it shades out understorey algae that compete with sessile invertebrates. When released from competition, sessile species in turn increase the diversity of mobile predators. Sea urchin grazing effects could have been misinterpreted as kelp effects, because sea urchins can overgraze giant kelp, understorey algae and sessile invertebrates alike. Our results confirm the high diversity and biomass associated with kelp forests, but highlight how species interactions and habitat attributes can be misconstrued as direct consequences of a foundation species like giant kelp.

Form–function relationships in a marine foundation species depend on scale: a shoot to global perspective from a distributed ecological experiment

Form–function relationships in plants underlie their ecosystem roles in supporting higher trophic levels through primary production, detrital pathways, and habitat provision. For widespread, phenotypically‐variable plants, productivity may differ not only across abiotic conditions, but also from distinct morphological or demographic traits. A single foundation species, eelgrass Zostera marina, typically dominates north temperate seagrass meadows, which we studied across 14 sites spanning 32–61°N latitude and two ocean basins. Body size varied by nearly two orders of magnitude through this range, and was largest at mid‐latitudes and in the Pacific Ocean. At the global scale, neither latitude, site‐level environmental conditions, nor body size helped predict productivity (relative growth rate 1–2% day‐1 at most sites), suggesting a remarkable capacity of Z. marina to achieve similar productivity in summer. Furthermore, among a suite of stressors applied within sites, only ambient leaf damage reduced productivity; grazer reduction and nutrient addition had no effect on eelgrass size or growth. Scale‐dependence was evident in different allometric relationships within and across sites for productivity and for modules (leaf count) relative to size. Zostera marina provides a range of ecosystem functions related to both body size (habitat provision, water flow) and growth rates (food, carbon dynamics). Our observed decoupling of body size and maximum production suggests that geographic variation in these ecosystem functions may be independent, with a future need to resolve how local adaptation or plasticity of body size might actually enable more consistent peak productivity across disparate environmental conditions.

Eelgrass Leaf Surface Microbiomes Are Locally Variable and Highly Correlated with Epibiotic Eukaryotes

Eelgrass (Zostera marina) is a marine foundation species essential for coastal ecosystem services around the northern hemisphere. Like all macroscopic organisms, it possesses a microbiome (here defined as an associated prokaryotic community) which may play critical roles in modulating the interaction of eelgrass with its environment. For example, its leaf surface microbiome could inhibit or attract eukaryotic epibionts which may overgrow the eelgrass leading to reduced primary productivity and subsequent eelgrass meadow decline. We used amplicon sequencing of the 16S and 18S rRNA genes of prokaryotes and eukaryotes to assess the leaf surface microbiome (prokaryotes) as well as eukaryotic epibionts in- and outside lagoons on the German Baltic Sea coast. Prokaryote microbiomes varied substantially both between sites inside lagoons and between open coastal and lagoon sites. Water depth, leaf area and biofilm chlorophyll a concentration explained a large amount of variation in both prokaryotic and eukaryotic community composition. The prokaryotic microbiome and eukaryotic epibiont communities were highly correlated, and network analysis revealed disproportionate co-occurrence between a limited number of eukaryotic taxa and several bacterial taxa. This suggests that eelgrass leaf surfaces are home to a mosaic of microbiomes of several epibiotic eukaryotes, in addition to the microbiome of the eelgrass itself. Our findings thereby underline that eukaryotic diversity should be taken into account in order to explain prokaryotic microbiome assembly and dynamics in aquatic environments.

The ‘golden kelp’ Laminaria ochroleuca under global change: Integrating multiple eco‐physiological responses with species distribution models

Abstract The loss of marine foundation species, in particular kelps at temperate latitudes, has been linked to climatic drivers and co‐occurring human perturbations. Ocean temperature and nutrients typically covary over local and regional scales and play a crucial role on kelp dynamics. Examining their independent and interactive effects on kelp physiological performance is essential to understand and predict patterns of kelp distribution, particularly under scenarios of global change. Crossed combinations of ocean temperatures and availability of nutrients were experimentally tested on juveniles of the ‘golden kelp’, Laminaria ochroleuca, from the northwestern Iberian Peninsula. Eco‐physiological responses included: survival, growth and total N content. Results were embedded into a Species Distribution Model (SDM), which relates presence records and climatic and non‐climatic data to forecast distribution patterns of L. ochroleuca under different climate change scenarios. Temperatures above 24.6°C were lethal irrespective of nutrients. Optimal growth of juvenile sporophytes occurred between 12 and 18°C and no nutrient limitation. The SDM, where ocean temperature was the main predictor of kelp distribution in line with temperature thresholds given by eco‐physiological responses, suggests a future expansion towards northern latitudes and a retreat from the southern limit/boundary of the current distribution. Synthesis. Range‐shifting of the golden kelp can have severe ecological impacts at regional and local scales. The expansion or retraction of the species along the European coast seems to be modulated mainly by temperature, but nutrient availability would be a key to maintain optimal physiological performance. Our work highlights that the combination of empirical and modelling approaches is accessible to researchers and crucial to building more robust predictions of ecological and biogeographic responses of habitat‐forming species to forecasted environmental change.

The effects of elevated temperature and dissolved ρCO2 on a marine foundation species.

Understanding how climate change and other environmental stressors will affect species is a fundamental concern of modern ecology. Indeed, numerous studies have documented how climate stressors affect species distributions and population persistence. However, relatively few studies have investigated how multiple climate stressors might affect species. In this study, we investigate the impacts of how two climate change factors affect an important foundation species. Specifically, we tested how ocean acidification from dissolution of CO 2 and increased sea surface temperatures affect multiple characteristics of juvenile eastern oysters (Crassostrea virginica). We found strong impacts of each stressor, but no interaction between the two. Simulated warming to mimic heat stressed summers reduced oyster growth, survival, and filtration rates. Additionally, we found that CO 2‐induced acidification reduced strength of oyster shells, which could potentially facilitate crab predation. As past studies have detected few impacts of these stressors on adult oysters, these results indicate that early life stages of calcareous marine organisms may be more susceptible to effects of ocean acidification and global warming. Overall, these data show that predicted changes in temperature and CO 2 can differentially influence direct effects on individual species, which could have important implications for the nature of their trophic interactions.

Fluctuations in population fecundity drive variation in demographic connectivity and metapopulation dynamics.

Demographic connectivity is vital to sustaining metapopulations yet often changes dramatically through time due to variation in the production and dispersal of offspring. However, the relative importance of variation in fecundity and dispersal in determining the connectivity and dynamics of metapopulations is poorly understood due to the paucity of comprehensive spatio-temporal data on these processes for most species. We quantified connectivity in metapopulations of a marine foundation species (giant kelp Macrocystis pyrifera) across 11 years and approximately 900 km of coastline by estimating population fecundity with satellite imagery and propagule dispersal using a high-resolution ocean circulation model. By varying the temporal complexity of different connectivity measures and comparing their ability to explain observed extinction-colonization dynamics, we discovered that fluctuations in population fecundity, rather than fluctuations in dispersal, are the dominant driver of variation in connectivity and contribute substantially to metapopulation recovery and persistence. Thus, for species with high variability in reproductive output and modest variability in dispersal (most plants, many animals), connectivity measures ignoring fluctuations in fecundity may overestimate connectivity and likelihoods of persistence, limiting their value for understanding and conserving metapopulations. However, we demonstrate how connectivity measures can be simplified while retaining utility, validating a practical solution for data-limited systems.

Long-term acclimation to reciprocal light conditions suggests depth-related selection in the marine foundation species Posidonia oceanica.

Phenotypic differences among populations of the same species reflect selective responses to ecological gradients produced by variations in abiotic and biotic factors. Moreover, they can also originate from genetic differences among populations, due to a reduced gene flow. In this study, we examined the extent of differences in photo‐acclimative traits of Posidonia oceanica (L.) Delile clones collected above and below the summer thermocline (i.e., −5 and −25 m) in a continuous population extending along the water depth gradient. During a reciprocal light exposure and subsequent recovery in mesocosms, we assessed degree of phenotypic plasticity and local adaptation of plants collected at different depths, by measuring changes in several traits, such as gene expression of target genes, photo‐physiological features, and other fitness‐related traits (i.e., plant morphology, growth, and mortality rates). Samples were also genotyped, using microsatellite markers, in order to evaluate the genetic divergence among plants of the two depths. Measures collected during the study have shown a various degree of phenotypic changes among traits and experimental groups, the amount of phenotypic changes observed was also dependent on the type of light environments considered. Overall plants collected at different depths seem to be able to acclimate to reciprocal light conditions in the experimental time frame, through morphological changes and phenotypic buffering, supported by the plastic regulation of a reduced number of genes. Multivariate analyses indicated that plants cluster better on the base of their depth origin rather than the experimental light conditions applied. The two groups were genetically distinct, but the patterns of phenotypic divergence observed during the experiment support the hypothesis that ecological selection can play a role in the adaptive divergence of P. oceanica clones along the depth gradient.

Temporal stability in patterns of genetic diversity and structure of a marine foundation species (Zostera marina).

Genetic diversity and population structure reflect complex interactions among a diverse set of processes that may vary temporally, limiting their potential to predict ecological and evolutionary outcomes. Yet, the stability of these patterns is rarely tested. We resampled eelgrass (Zostera marina) meadows from published studies to determine variability in genetic diversity and structure within and between meadows over 5-12 years. The meadows sampled (San Francisco, Tomales and Bodega Bays in California and the Virginia coastal bays) represent a range of life histories (annual vs perennial), age (well-established vs restored) and environments (rural vs urbanized). In all of these systems, neither diversity nor differentiation (FST) changed over time. Differences among tidal heights within Bodega Bay were also remarkably consistent, with the high intertidal being more diverse than the subtidal, and tidal height differentiation being modest but significant at both time points. Historical studies used only a few microsatellite loci; therefore, our temporal comparisons were based on 4-5 loci. However, analysis of the current data using a set of 12 loci show that 4-5 loci are sufficient to describe diversity and differentiation patterns in this system. This temporal consistency was not because of the resampling of large clones, underscoring the feasibility and relevance of understanding drivers of the differences. Because seagrasses are declining at rapid rates, restoration and conservation are increasingly a coastal management priority. Our results argue that surveys of eelgrass genetic structure and diversity at decadal scales can provide accurate depictions of populations, increasing the utility of published genetic data for restoration and designing networks of reserves.

Edge effects reverse facilitation by a widespread foundation species.

Dense aggregations of foundation species often mitigate environmental stresses for organisms living among them. Considerable work documents such benefits by comparing conditions inside versus outside these biogenic habitats. However, environmental gradients commonly arise across the extent of even single patches of habitat-forming species, including cases where stresses diverge between habitat interiors and edges. We ask here whether such edge effects could alter how habitat-forming species influence residents, potentially changing the strength or direction of interactions (i.e., from stress amelioration to exacerbation). We take as a model system the classic marine foundation species, Mytilus californianus, the California mussel. Results demonstrate that mussel beds both increase and decrease thermal stresses. Over a distance of 6 to 10 cm from the bed interior to its upper surface, peak temperatures climb from as much as 20 °C below to 5 °C above those of adjacent bedrock. This directional shift in temperature modification affects interactions with juvenile mussels, such that thermal stresses and associated mortality risk are higher at the bed surface, but substantially reduced deeper within the adult matrix. These findings provide a case example of how stress gradients generated across biogenic habitats can markedly alter ecological interactions even within a single habitat patch.

Molecular physiology reveals ammonium uptake and related gene expression in the seagrass Zostera muelleri

Seagrasses are important marine foundation species, which are presently threatened by coastal development and global change worldwide. The molecular mechanisms that drive seagrass responses to anthropogenic stresses, including elevated levels of nutrients such as ammonium, remains poorly understood. Despite the evidence that seagrasses can assimilate ammonium by using glutamine synthetase (GS)/glutamate synthase (glutamine-oxoglutarate amidotransferase or GOGAT) cycle, the regulation of this fundamental metabolic pathway has never been studied at the gene expression level in seagrasses so far. Here, we combine (i) reverse transcription quantitative real-time PCR (RT-qPCR) to measure expression of key genes involved in the GS/GOGAT cycle, and (ii) stable isotope labelling and mass spectrometry to investigate 15N-ammonium assimilation in the widespread Australian species Zostera muelleri subsp. capricorni (Z. muelleri). We demonstrate that exposure to a pulse of ammonium in seawater can induce changes in GS gene expression of Z. muelleri, and further correlate these changes in gene expression with 15N-ammonium uptake rate in above- and below-ground tissue.

Genetic signatures of Bassian glacial refugia and contemporary connectivity in a marine foundation species

AbstractAimTo examine the population genetic structure in Posidonia australis meadows, a marine foundation species capable of long distance dispersal (LDD), and the role of historical versus contemporary processes in shaping post Last Glacial Maximum (LGM) re‐colonization.LocationSoutheastern Australia including the Bass Strait Islands.MethodsWe generated multilocus genotypes and assessed spatial patterns of genetic diversity. Relationships among meadows were assessed in terms of historical sea level changes, oceanic boundary currents and contemporary seed dispersal based on a hydrodynamic model.ResultsThere was strong regional spatial genetic structuring among P. australis meadows in south‐eastern Australia, which was congruent with three recognized marine biogeographical provinces [Peronian (eastern), Flindersian (western and southern), and Maugean (south‐eastern)]. The genetic data suggest Maugean meadows persisted in isolation during the LGM, with evidence for admixture and contemporary gene flow. Simulated dispersal events identified high rates of local and regional demographic connectivity, with evidence for occasional LDD events.Main conclusionsThe strong regional differentiation is consistent with long‐term barriers to dispersal persisting in the marine environment through many sea level fluctuations. Bass Strait Island meadows all have strong signals of genetic admixture. A weak but significant isolation by distance relationship is consistent with a historical signal and contemporary seed dispersal mostly within the Bass Strait.

Trophic versus structural effects of a marine foundation species, giant kelp (Macrocystis pyrifera).

Foundation species create milieus in which ecosystems evolve, altering species abundances and distribution often to a dramatic degree. Although much descriptive work supports their importance, there remains little definitive information on the mechanisms by which foundation species alter their environment. These mechanisms fall into two basic categories: provision of food or other materials, and modification of the physical environment. Here, we manipulated the abundance of a marine foundation species, the giant kelp Macrocystis pyrifera, in 40×40-m plots at Mohawk Reef off Santa Barbara, California and found that its biomass had a strong positive effect on the abundance of bottom-dwelling sessile invertebrates. We examined the carbon (C) stable isotope values of seven species of sessile invertebrates in the treatment plots to test the hypothesis that this positive effect resulted from a nutritional supplement of small suspended particles of kelp detritus, as many studies have posited. We found no evidence from stable isotope analyses to support the hypothesis that kelp detritus is an important food source for sessile suspension-feeding invertebrates. The isotope composition of invertebrates varied with species and season, but was not affected by kelp biomass, with the exception of two species: the tunicate Styela montereyensis, which exhibited a slight enrichment in C stable isotope composition with increasing kelp biomass, and the hydroid Aglaophenia sp., which showed the opposite effect. These results suggest that modification of the physical habitat, rather than nutritional subsidy by kelp detritus, likely accounts for increased abundance of sessile invertebrates within giant kelp forests.

Biodiversity mediates top-down control in eelgrass ecosystems: a global comparative-experimental approach.

Nutrient pollution and reduced grazing each can stimulate algal blooms as shown by numerous experiments. But because experiments rarely incorporate natural variation in environmental factors and biodiversity, conditions determining the relative strength of bottom-up and top-down forcing remain unresolved. We factorially added nutrients and reduced grazing at 15 sites across the range of the marine foundation species eelgrass (Zostera marina) to quantify how top-down and bottom-up control interact with natural gradients in biodiversity and environmental forcing. Experiments confirmed modest top-down control of algae, whereas fertilisation had no general effect. Unexpectedly, grazer and algal biomass were better predicted by cross-site variation in grazer and eelgrass diversity than by global environmental gradients. Moreover, these large-scale patterns corresponded strikingly with prior small-scale experiments. Our results link global and local evidence that biodiversity and top-down control strongly influence functioning of threatened seagrass ecosystems, and suggest that biodiversity is comparably important to global change stressors.

Canopy facilitates seaweed recruitment on subtidal temperate reefs

Summary Facilitation through physical stress amelioration has been largely overlooked in subtidal marine ecosystems, where abiotic gradients are perceived to be benign. However, seemingly subtle changes in marine environmental conditions can alter community structure across vast areas, and therefore, the type of interactions and any refuge provided by marine foundation species. This could have substantial implications for community organization. We measured net recruitment rates of subtidal seaweeds under experimentally modified canopy densities, across 1000 km of coastline, to examine the nature of interactions between seaweed canopies and recruits. Contrary to expectations, facilitation, as evidenced by higher recruitment under canopies, was observed throughout all conditions for Scytothalia dorycarpa and under partial canopies at three of four locations for Sargassum spp., whilst competitive interactions remained prevalent for Sargassum under closed canopies. Supply side dynamics were also of major importance to recruitment success for Scytothalia. For Sargassum, the interaction strength between recruits and the canopy became increasingly positive towards lower latitudes, suggesting the canopy environment was mitigating stress across the latitudinal climate gradient. Synthesis. Positive interactions and stress amelioration play an important and previously unrecognized role in determining the recruitment success and viability of seaweeds in subtidal marine ecosystems. These results challenge long held paradigms about the general importance of canopy competition and force a rethink of how seaweed interactions affect habitat resilience to disturbances in subtidal ecosystems.

Morphological and physiological variation among seagrass (Zostera marina) genotypes

Intraspecific variation in habitat-forming species can have important ecological consequences at the population, community, and ecosystem level. However, the contribution of genetic variation among individuals to these effects is seldom documented. We quantified morphological and physiological variation among genotypes of a marine foundation species, the seagrass Zostera marina. We grew replicate shoots of eight genetically distinct Zostera individuals collected from Bodega Bay, California, in a common garden environment and then quantified shoot production and morphology, nutrient uptake, and key photosynthetic parameters. We found that genotypes differed in shoot production, biomass, and both root and shoot nutrient uptake rates, even when corrected for genotype-specific biomass differences. In addition, the rank order of uptake ability differed for ammonium and nitrate, indicating that genotypes may exhibit resource partitioning of different forms of nutrients. Our results suggest that both niche complementarity among genotypes and the sampling/selection effect could contribute to previously observed positive effects of seagrass clonal diversity on resource utilization and biomass production. Further, they highlight that genotypic variation in key traits of habitat-forming species could have measurable effects on community structure and function.

Associations of concern: declining seagrasses and threatened dependent species

Seagrasses are important marine foundation species that are reported to be declining worldwide, with almost 15% of species considered threatened. Seagrasses are highly productive plants that reconfigure water flow and influence nutrient cycling, as well as provide critical habitat for a wide array of fish and invertebrate species. Yet, many of these seagrass‐dependent species, including economically important fishes and invertebrates, are themselves in danger of overexploitation or extinction. In fact, there is on average more than one threatened associated species for every seagrass species across the globe. Links between threatened seagrasses and their dependent communities illustrate the importance of an ecosystem‐based management approach that incorporates interdependencies and facilitation among species.