Mirta Teichberg

Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp.

Receiving coastal waters and estuaries are among the most nutrient-enriched environments on earth, and one of the symptoms of the resulting eutrophication is the proliferation of opportunistic, fast-growing marine seaweeds. Here, we used a widespread macroalga often involved in blooms, Ulva spp., to investigate how supply of nitrogen (N) and phosphorus (P), the two main potential growth-limiting nutrients, influence macroalgal growth in temperate and tropical coastal waters ranging from low- to high-nutrient supplies. We carried out N and P enrichment field experiments on Ulva spp. in seven coastal systems, with one of these systems represented by three different subestuaries, for a total of nine sites. We showed that rate of growth of Ulva spp. was directly correlated to annual dissolved inorganic nitrogen (DIN) concentrations, where growth increased with increasing DIN concentration. Internal N pools of macroalgal fronds were also linked to increased DIN supply, and algal growth rates were tightly coupled to these internal N pools. The increases in DIN appeared to be related to greater inputs of wastewater to these coastal waters as indicated by high δ15N signatures of the algae as DIN increased. N and P enrichment experiments showed that rate of macroalgal growth was controlled by supply of DIN where ambient DIN concentrations were low, and by P where DIN concentrations were higher, regardless of latitude or geographic setting. These results suggest that understanding the basis for macroalgal blooms, and management of these harmful phenomena, will require information as to nutrient sources, and actions to reduce supply of N and P in coastal waters concerned.

Succession patterns in algal turf vegetation on a Caribbean coral reef

Abstract Over the past three decades, Caribbean coral reefs have drastically changed in structure and organization due to anthropogenically driven environmental changes. The prognostic trend indicates a shift from coral- to more algal-dominated reefs coupled with a loss in biodiversity and destabilization of reef structure. This study focuses on the composition of the most common algal growth form, the turf, and investigates turf succession within a fringing Caribbean coral reef. In a field study starting October 2007, we followed succession of turf algal assemblages grown on artificial substrata for periods of 15 up to 333 days at different water depths (5, 15 and 25 m). Species composition and abundance,biodiversity, total cover, and biomass were investigated and compared in uni- and multivariate analyses. Despite the pronounced change in coral reef structure over the past years, we found little difference from primary succession patterns described 30 years earlier. Succession patterns revealed a high diversity, mainly driven by the filamentous brown algal order Ectocarpales, the crustose green alga Pringsheimiella scutata at early stage, and diverse filamentous Cyanobacteria at later stages. Overall, the study provides insight into the early successional stages of coral reef vegetation by identifying the key species and discussing possible factors determining reef development in relation to environmental change.

Nutrient availability affects the response of the calcifying chlorophyte Halimeda opuntia (L.) J.V. Lamouroux to low pH

Atmospheric carbon dioxide emissions cause a decrease in the pH and aragonite saturation state of surface ocean water. As a result, calcifying organisms are expected to suffer under future ocean conditions, but their physiological responses may depend on their nutrient status. Because many coral reefs experience high inorganic nutrient loads or seasonal changes in nutrient availability, reef organisms in localized areas will have to cope with elevated carbon dioxide and changes in inorganic nutrients. Halimeda opuntia is a dominant calcifying primary producer on coral reefs that contributes to coral reef accretion. Therefore, we investigated the carbon and nutrient balance of H.opuntia exposed to elevated carbon dioxide and inorganic nutrients. We measured tissue nitrogen, phosphorus and carbon content as well as the activity of enzymes involved in inorganic carbon uptake and nitrogen assimilation (external carbonic anhydrase and nitrate reductase, respectively). Inorganic carbon content was lower in algae exposed to high CO2, but calcification rates were not significantly affected by CO2 or inorganic nutrients. Organic carbon was positively correlated to external carbonic anhydrase activity, while inorganic carbon showed the opposite correlation. Carbon dioxide had a significant effect on tissue nitrogen and organic carbon content, while inorganic nutrients affected tissue phosphorus and N:P ratios. Nitrate reductase activity was highest in algae grown under elevated CO2 and inorganic nutrient conditions and lowest when phosphate was limiting. In general, we found that enzymatic responses were strongly influenced by nutrient availability, indicating its important role in dictating the local responses of the calcifying primary producer H.opuntia to ocean acidification.

The Relative Role of Nutrients, Grazing, and Predation as Controls on Macroalgal Growth in the Waquoit Bay Estuarine System

Understanding whether nutrient availability and grazing by consumers can control macroalgal growth is important to mitigate blooms. To assess the effect of long-term nitrogen loading on macroalgae, we ran a field experiment in which we measured growth of green and red macroalgae in estuaries where loads and eutrophication status differed. The relative abundances of consumers differed among estuaries with more grazers in non-eutrophied estuaries, an important interaction of bottom-up and top-down controls. In the estuary with the lowest nitrogen load, grazers controlled green macroalgal growth, but in higher nitrogen-loaded estuaries, where grazing was lower, growth of green macroalgae overwhelmed potential grazer control. The red macroalga was not controlled by grazers, even in the estuary where grazing pressure was highest. In the low-loaded estuary, invertebrate predators exerted top-down control over grazers, but predation effects did not cascade to macroalgae. Bottom-up mechanisms dominated control of macroalgae through an interaction of direct stimulation of growth and indirect alteration of consumer abundances, and thus, long-term nutrient regimes are likely determining potential for bloom formation in Waquoit Bay.

Non-Random Variability in Functional Composition of Coral Reef Fish Communities along an Environmental Gradient.

Changes in the coral reef complex can affect predator-prey relationships, resource availability and niche utilisation in the associated fish community, which may be reflected in decreased stability of the functional traits present in a community. This is because particular traits may be favoured by a changing environment, or by habitat degradation. Furthermore, other traits can be selected against because degradation can relax the association between fishes and benthic habitat. We characterised six important ecological traits for fish species occurring at seven sites across a disturbed coral reef archipelago in Indonesia, where reefs have been exposed to eutrophication and destructive fishing practices for decades. Functional diversity was assessed using two complementary indices (FRic and RaoQ) and correlated to important environmental factors (live coral cover and rugosity, representing local reef health, and distance from shore, representing a cross-shelf environmental gradient). Indices were examined for both a change in their mean, as well as temporal (short-term; hours) and spatial (cross-shelf) variability, to assess whether fish-habitat association became relaxed along with habitat degradation. Furthermore, variability in individual traits was examined to identify the traits that are most affected by habitat change. Increases in the general reef health indicators, live coral cover and rugosity (correlated with distance from the mainland), were associated with decreases in the variability of functional diversity and with community-level changes in the abundance of several traits (notably home range size, maximum length, microalgae, detritus and small invertebrate feeding and reproductive turnover). A decrease in coral cover increased variability of RaoQ while rugosity and distance both inversely affected variability of FRic; however, averages for these indices did not reveal patterns associated with the environment. These results suggest that increased degradation of coral reefs is associated with increased variability in fish community functional composition resulting from selective impacts on specific traits, thereby affecting the functional response of these communities to increasing perturbations.

Relative Influence of Grazing and Nutrient Supply on Growth of the Green Macroalga Ulva lactuca in Estuaries of Waquoit Bay, Massachusetts

Nitrogen supply is a major control on growth of coastal macroalgae (1, 2, 3). Top-down effects in which grazing signifi cantly affects macroalgae (4, 5), and nutrient-grazer interactions (3) have also been described. In this paper we describe an experiment in which we measured net growth of a common macroalga, Ulva lactuca, in treatments that allowed different numbers of grazers to access fronds as well as incubation of fronds in estuaries with demonstrably different nutrient supplies. These treatments were intended to assess the relative infl uence of grazer and nitrogen supply on net growth rates of a coastal producer. To examine the effect of grazing on growth of U. lactuca, we constructed acrylic plastic cages with sides of 1-mm, 4-mm, or 18-mm mesh. The different mesh openings were intended to allow entry to different numbers of grazers, which we took as a proxy for grazing pressure. The cage design also allowed for light penetration and horizontal water fl ow. The 18-mm mesh permitted larger size classes and a greater number of grazers to enter the cages, while the 1-mm mesh excluded larger size classes and allowed fewer grazers. The 4-mm mesh was intended to furnish an intermediate grazer treatment. To evaluate the effect of nitrogen supply and grazing on algal growth, cages with the three mesh sides were placed in three estuaries in Waquoit Bay, Massachusetts. These three estuaries experience different nitrogen loads—Sage Lot Pond, 14 kg ha 1 y 1 ; Quashnet River, 350 kg ha 1 y 1 ; and Childs River, 601 kg ha 1 y 1 —from their watershed (6). These nitrogen loads led to different mean nitrate concentrations measured in the estuaries during July 2002, one year prior to the time of our experiments: 0.04, 6.1, and 11.75 M for Sage Lot Pond, Quashnet River, and Childs River, respectively (G. Tomasky, Boston University Marine Program, unpubl. data). To minimize effects of differences between estuaries other than our treatments, we chose sites similar in salinity, depth, and algal composition. In each estuary we placed four replicates of each of the three grazing pressure treatments, for a total of 36 cages. Three fronds of U. lactuca, each approximately 300 mg (blotted wet weight), were suspended inside each cage. To measure the effect of top-down versus bottom-up factors, we measured net growth as the dependent variable. Net growth was the growth achieved by the fronds minus the biomass consumed by grazers. To determine net growth, the U. lactuca fronds were weighed initially (blotted wet weight) and again after 10 days of fi eld incubation. First, we assess the successed of the treatments. To roughly measure the grazing pressure, we sorted and counted the potential grazers found in the cages for two replicates of each treatment at the end of the incubation. The grazers were sorted into four groups, amphipods, shrimp, crabs, and isopods. The total number of grazers in the 1-mm mesh cages was signifi cantly lower in all three estuaries than the number in the 4-mm cages (Fig. 1a; ANOVA F 31.0, P 0.0014). The number of grazers found in the 18-mm mesh cages was also signifi cantly different, although they contained lower grazer abundances than the 1-mm and 4-mm mesh cages (Fig. 1a). Predatory fi sh and large shrimp entered the cages with 18 mm mesh and likely fed on the smaller grazers, thus decreasing grazer abundances. This possible effect of predators on grazers suggests that there might be important top-down cascade effects in this system waiting to be studied. The difference in nitrogen load in the three estuaries provided quantitatively different nutrient supplies, as evident in the nitrate concentrations cited above. Bottom-up effects from these different nitrogen supplies on net growth of U. lactuca were dominant factors. Rates of net growth were higher in estuaries receiving

Differences in urbanization and degree of marine influence are reflected in δ13C and δ15N of producers and consumers in seagrass habitats of Puerto Rico

Couplings between land use and marine food webs in tropical systems are poorly understood. We compared land-sea coupling in seven sites around Puerto Rico, differing in the degree of precipitation and urbanization, by measuring delta(13)C and delta(15)N in producers and consumers. delta(15)N values were influenced by human activity: the food web from sites near urbanized centers was on average 1 per thousand heavier in delta(15)N compared to undeveloped sites. This is most likely due to wastewater inputs from septic systems relatively near the shoreline. Changes in delta(13)C were best explained by differences in the degree of marine influence. Where terrestrial inputs from a major river dominated, delta(13)C values were lighter, whereas sites further from land and in locations exposed to oceanic currents had heavier delta(13)C values, characteristic of a marine source of dissolved organic carbon. We found no significant effect of precipitation on connectivity in spite of a twofold difference in annual average rainfall between the north and south coast. The results suggest there is some connectivity between land and sea in Puerto Rico, despite high rates of evaporation relative to precipitation.

Spatio-Temporal Patterns in Coral Reef Communities of the Spermonde Archipelago, 2012–2014, I: Comprehensive Reef Monitoring of Water and Benthic Indicators Reflect Changes in Reef Health

Pollution, fishing, and outbreaks of predators can heavily impact coastal coral reef ecosystems, leading to decreased water quality and benthic community shifts. To determine the main environmental drivers of coral reef status in the Spermonde Archipelago, Indonesia, we monitored environmental variables and coral reef benthic community structure along an on-to-offshore gradient annually from 2012-2014. Findings revealed that concentrations of phosphate, chlorophyll a-like fluorescence, suspended particulate matter, and light attenuation significantly decreased from on-to-offshore, while concentrations of dissolved O2 and values of water pH significantly increased on-to-offshore. Nitrogen stable isotope signatures of sediment and an exemplary common brown alga were significantly enriched nearshore, identifying wastewater input as a primary N source from the city of Makassar. In contrast to the high temporal variability in water quality, coral reef benthic community cover did not show strong temporal, but rather, spatial patterns. Turf algae was the dominant group next to live coral, and was negatively correlated to live coral, crustose coralline algae (CCA), rubble and hard substrate. Variation in benthic cover along the gradient was explained by water quality variables linked to trophic status and physico-chemical variables. As an integrated measure of reef status and structural complexity, the benthic index, based on the ratio of relative cover of live coral and CCA to other coral reef organisms, and reef rugosity were determined. The benthic index was consistently low nearshore and increased offshore, with high variability in the midshelf sites across years. Reef rugosity was also lowest nearshore and increased further offshore. Both indices dropped in 2013, increasing again in 2014, indicating a period of acute disturbance and recovery within the study and suggesting that the mid-shelf reefs are more resilient to disturbance than nearshore reefs. We thus recommend using these two indices with a selected number of environmental variables as an integral part of future reef monitoring.

CO2 and inorganic nutrient enrichment affect the performance of a calcifying green alga and its noncalcifying epiphyte

Ocean acidification studies in the past decade have greatly improved our knowledge of how calcifying organisms respond to increased surface ocean CO2 levels. It has become evident that, for many organisms, nutrient availability is an important factor that influences their physiological responses and competitive interactions with other species. Therefore, we tested how simulated ocean acidification and eutrophication (nitrate and phosphate enrichment) interact to affect the physiology and ecology of a calcifying chlorophyte macroalga (Halimeda opuntia (L.) J.V. Lamouroux) and its common noncalcifying epiphyte (Dictyota sp.) in a 4-week fully crossed multifactorial experiment. Inorganic nutrient enrichment (+NP) had a strong influence on all responses measured with the exception of net calcification. Elevated CO2 alone significantly decreased electron transport rates of the photosynthetic apparatus and resulted in phosphorus limitation in both species, but had no effect on oxygen production or respiration. The combination of CO2 and +NP significantly increased electron transport rates in both species. While +NP alone stimulated H. opuntia growth rates, Dictyota growth was significantly stimulated by nutrient enrichment only at elevated CO2, which led to the highest biomass ratios of Dictyota to Halimeda. Our results suggest that inorganic nutrient enrichment alone stimulates several aspects of H. opuntia physiology, but nutrient enrichment at a CO2 concentration predicted for the end of the century benefits Dictyota sp. and hinders its calcifying basibiont H. opuntia.

Bottom-Up Versus Top-Down Control of Macroalgal Blooms

Macroalgal blooms have increased worldwide due to anthropogenic activities. Coastal eutrophication and overfishing are two of the main influences that have led to macroalgal blooms. However, the relative roles of nutrient supply and grazing pressure in macroalgal bloom formation are still unresolved. This chapter provides an overview of occurrences of macroalgal blooms and their ecological consequences and discusses the role of bottom-up and top-down controls of macroalgal growth in shallow estuaries, coral reefs, and intertidal or subtidal rocky shores, in order to understand how different systems may compare in response to these controls. We conclude with a future outlook on how eutrophication and overfishing in combination with other environmental factors may influence macroalgal bloom occurrences.