Peggy Fong

EXPERIMENTAL EVIDENCE SUPPORTS THE USE OF δ15N CONTENT OF THE OPPORTUNISTIC GREEN MACROALGA ENTEROMORPHA INTESTINALIS (CHLOROPHYTA) TO DETERMINE NITROGEN SOURCES TO ESTUARIES

One assumption underlying the use of stable nitrogen isotopes (δ15N) for determining nitrogen (N) sources is that the δ15N of primary producers reflects N sources in a predictable manner. To test this assumption, we conducted two experiments. First, we varied δ15N with constant concentration of NO3− or NH4+ to determine whether either nutrient is preferentially selected by the macroalga Enteromorpha intestinalis (L. Link) and if isotopic ratio affected selectivity. Tissue δ15N increased with δ15N supplied for both NO3− and NH4+ but sequestering of 15NH4+ was more rapid than for 15NO3−; in addition, some evidence suggested that high relative abundance of 15N may have decreased NO3− uptake. Second, we held δ15N constant and varied concentrations of either NO3− or NH4+ to determine whether fractionation is concentration dependent. Uptake of N was described by a Michaelis‐Menten equation for both NO3− and NH4+, with higher Vmax and K1/2 for NH4+ than for NO3−. There was no relationship between N concentration and tissue δ15N for either NO3− or NH4+; therefore, no selection for 14N over 15N occurred. This study demonstrated that accumulation of 15N in macroalgal tissue was predictable over a range of water δ15N values and N concentrations, suggesting that E. intestinalis may be used to assess the availability of N sources to estuarine and coastal communities. However, caution must be used when interpreting tissue δ15N depending on the primary inorganic form of N available.

Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral, seagrass, and mangrove habitats

We explored the role of food quality in herbivore preference for macroalgae by comparing consumption of Acanthophora spicifera with and without elevated tissue nitrogen and phosphorus concentrations. Algal enrichment effects on herbivory were examined in coral, seagrass, and mangrove habitats along a sparsely populated Honduran island protected from fishing. Nutrient enrichment led to significantly increased grazing by herbivores across habitats. Consumption of enriched algae increased by 91% compared to controls among the mangrove roots, where herbivory rates were generally lowest. In the heavily grazed seagrass and coral habitats, nutrient enrichment increased consumption by 30 and 20%, respectively, with the effect more spatially variable than among the mangrove roots. We suggest that, at least on the local scale, intact herbivore populations may be able to compensate for effects of increased nutrient supply by locating and consuming nutrient-enriched algae, but that the importance of this mechanism varies both among and within habitats.

Developing an indicator of nutrient enrichment in coastal estuaries and lagoons using tissue nitrogen content of the opportunistic alga, Enteromorpha intestinalis (L. Link)

Abstract We explored the use of an opportunistic green alga, Enteromorpha intestinalis (L. Link), as an indicator of N enrichment in a southern California salt marsh. In conjunction with N additions to cordgrass ( Spartina foliosa , Trin) in April, June and August 1995, mesh bags containing N-starved algal tissue were placed within cordgrass patches, at their edges along islands, and in adjacent channels. After 1 week in the field, recovered algal tissue was used to test detection of two levels of total N supply (one twice as high as the other), as well as no added N (control). Tissue N concentration, calculated as the percentage change in N, was the best of several algal measures at discerning differences in N availability in any month. In both April and June, tissue N declined from the marsh plain to the channels, reflecting declining N supply. Tissue N concentration also reflected differences in the total quantity of N added. Within the channels adjacent to fertilized areas, algal tissue N was similar to control areas, suggesting that N additions to cordgrass are not resulting in eutrophication of open waters. In August, the algae detected N additions on the marsh plain, but survivorship was poor; other algal species may be better indicators of enrichment in late-summer. With further investigation, the technique presented in this paper has the potential to be developed into a useful bioassay for detecting eutrophication of coastal salt marshes and lagoons.

Macroalgal bloom dynamics in a highly eutrophic southern California estuary

A 16-mo long monitoring study was carried out in Upper Newport Bay estuary (UNB), Orange County, California, to quantify the macroalgal community of a southern California estuary. Quarterly sampling began December 1996 at 8 stations along the main channel and tidal creeks ranging from the head to the lower end of UNB. At each station, two strata (one at high and one at low elevation) were surveyed. Macroalgal species abundance (% cover and biomass) and algal tissue nitrogen (N) and phosphorus (P) were measured. The algal community changed from sparse macroalgal cover during winter 1996 to larger patches dominated byEnteromorpha intestinalis in spring 1997. The community was characterized by a thick cover of macroalgae comprised ofE. intestinalis andUlva expansa in summer 1997 andU. expansa andCeramium spp. in fall 1997. UNB returned to sparse macroalgal cover by spring 1998. In summer and fall 1997, biomass ofE. intestinalis andCeramium reached over 1,000 g wet wt m−2 each, andU. expansa biomass exceeded 700 g wet wt m−2. Tissue N was high inE. intestinalis andU. expansa collected from UNB (≈3% dry wt) and higher inCeramium (≈3.5% dry wt). Tissue P in all three algae ranged from 0.24–0.28% dry wt. Tissue N∶P (molar) ratios inE. intestinalis andU. expansa ranged from 16.4 to 30.0 and inCeramium from 21.8 to 40.1. A field experiment was conducted in whichE. intestinalis was used as a bioassay of N and P availability. Algal tissue was cultured under known conditions and samples were deployed throughout the estuary and left for 24 h. Tissue N of algae from these bags showed a nominal increase in N with proximity to the primary nutrient input to the system, San Diego Creek (p=0.0251; r2=0.200). Our data indicate that UNB is already a highly eutrophic estuary, but macroalgal blooms in UNB may increase if more N is added to the system.

DRAMATIC DECLINES IN MUSSEL BED COMMUNITY DIVERSITY: RESPONSE TO CLIMATE CHANGE?

Mussel beds along the wave-exposed coast of the eastern North Pacific Ocean serve as an important habitat, harboring a high diversity of species. A comparison of California mussel bed community diversity in 2002 to historical data (1960s to 1970s) revealed large declines (mean loss 58.9%), including some declines >141 species (approximately 80% loss). Concurrent work revealed inconsistent changes in mussel populations (biomass and bed thickness) along the California coast, suggesting that diversity declines may be related to large-scale processes rather than local habitat destruction. Potential factors causing declines in mussel community diversity are discussed, with regional climate change associated with the Pacific Decadal Oscillation and climate change induced alterations of ecological interactions and biological processes suggested as likely causes. Although extensive literature has predicted the potential effects of climate change on global diversity, this study is one of the few examples of declines attributed to climate change.

Coral Reef Algae

Benthic macroalgae, or “seaweeds,” are key members of coral reef communities that provide vital ecological functions such as stabilization of reef structure, production of tropical sands, nutrient retention and recycling, primary production, and trophic support. Macroalgae of an astonishing range of diversity, abundance, and morphological form provide these equally diverse ecological functions. Marine macroalgae are a functional rather than phylogenetic group comprised of members from two Kingdoms and at least four major Phyla. Structurally, coral reef macroalgae range from simple chains of prokaryotic cells to upright vine-like rockweeds with complex internal structures analogous to vascular plants. There is abundant evidence that the historical state of coral reef algal communities was dominance by encrusting and turf-forming macroalgae, yet over the last few decades upright and more fleshy macroalgae have proliferated across all areas and zones of reefs with increasing frequency and abundance. Ecological processes that sustain these shifts from coral- to algal-dominated tropical reefs include increases in open suitable substrate due to coral mortality, anthropogenic increases in nutrient supply, reductions in herbivory due to disease and overfishing, and the proliferation of algae with chemical defenses against herbivory. These shifts are likely to be accelerated and the algal state stabilized by the impacts of invasive species and climate change. Thus, algal-dominated tropical reefs may represent alternative stable states that are resistant to shifts back to coral domination due to the strength and persistence of ecological processes that stabilize the algal state.

Salinity stress, nitrogen competition, and facilitation: what controls seasonal succession of two opportunistic green macroalgae?

Differential tolerance of low salinity, competition for nitrogen (N), and facilitation by altering N supply all may act to determine the pattern of seasonal succession of Enteromorpha intestinalis (L.) Link and Ulva expansa (Setch) S. and G. in estuaries and lagoons of southern California. Low salinity negatively affected both of these algae. However, when N was in sufficient supply, salinities of 15 ppt favored E. intestinalis while oceanic salinity (35 ppt) favored U. expansa; neither alga had a clear advantage at 25 ppt. When starved of N, E. intestinalis and U. expansa competed directly for nutrients. When grown alone, they had similar N uptake and growth rates; when grown together, E. intestinalis was the superior competitor, negatively affecting growth of U. expansa. In addition, U. expansa facilitated the growth of E. intestinalis when N was in short supply; when grown together, there was a positive effect of U. expansa on E. intestinalis. The mechanism of this effect may have been the release or ‘leaking’ of DON when U. expansa no longer had sufficient tissue N to grow. Thus, E. intestinalis would be favored immediately after a rain, but would be replaced by U. expansa when N is available and tidal action reestablishes oceanic salinity. However, at the end of the rainy season when N becomes scarce, E. intestinalis would outcompete U. expansa. We hypothesize that U. expansa may facilitate the dominance of E. intestinalis by leaking N that can be assimilated by E. intestinalis.

USING OPPORTUNISTIC GREEN MACROALGAE AS INDICATORS OF NITROGEN SUPPLY AND SOURCES TO ESTUARIES

Nutrient inputs to estuaries are increasing worldwide, and anthropogenic contributions are increasingly complex and difficult to distinguish. Measurement of integrated effects of salinity and nutrient changes simultaneously can help ascertain whether N sources of similar magnitude and stable isotope (sigma15N) signatures are river dominated. We used Enteromorpha spp., an opportunistic macroalga, to obtain integrated measures of salinity, nutrient supply, and nutrient source in estuaries. We outplanted cultured algae in the field along spatial gradients within three southern California estuaries for 24 hours in wet and dry seasons. Tissue was analyzed for potassium (K+) to measure osmoregulatory changes, total nitrogen to examine changes in nutrient supply, and sigma15N to assess nutrient sources. Discrete measures of water salinity correlated with tissue K+ content; however, there was significant variability in the relationship, suggesting that the algae were subject to considerable variation in salinity over a tidal cycle. Tissue total N was not always related to snapshot measures of water column dissolved inorganic nitrogen (DIN), suggesting that integrated measures may be better at capturing the temporal and spatial complexity of nutrient availability. The combination of tissue K+, total N, and sigma15N measures revealed that inflowing rivers delivered N from watershed sources to Mugu Lagoon and Carpinteria Salt Marsh, while both the inflowing river and a mid estuary source were important sources of high sigma15N N in Upper Newport Bay. These experiments revealed complex patterns of supply and sources of N and demonstrate the usefulness of macroalgal indicators over water sampling to detect these patterns.

SALICORNIA VIRGINICA IN A SOUTHERN CALIFORNIA SALT MARSH: SEASONAL PATTERNS AND A NUTRIENT-ENRICHMENT EXPERIMENT

Salicornia virginica (common pickleweed) is the dominant vascular plant of many saline marshes of the US west coast, yet little is known about seasonal patterns or abiotic factors controlling it. In a southern California salt marsh, quarterly sampling revealed strong seasonal trends, with 2x greater S. virginica biomass in summer than in winter. Tissue nitrogen (N) and phosphorus (P) concentrations were highest in winter and lower in spring and summer, suggesting a dilution of nutrients as plants accumulated biomass during the growing season. Despite high sediment nutrient levels in this marsh, an experiment examining N and P effects still found strong S. virginica responses to N applied biweekly for > 1 year. Increases in succulent tissue biomass after N addition were first seen in April 1998 (after fertilization for 11 months); two-fold increases in biomass and the number of branches resulted by the end of the experiment in August 1998. Addition of N increased N concentration in the woody tissues when sampled in August. The N:P ratio increased with N addition beginning in winter (7 months after fertilization began) and continuing through the remainder of the experiment. Effects of P addition were less marked, as adding P did not result in biomass responses; however, it did influence tissue nutrient levels. These amendments increased P concentrations in the woody tissue in August 1998. In contrast to N amendments, which did not affect root nutrient concentrations, P addition led to increases in P content of root tissues in the latter portion of the growing season. These data suggest that increases in nutrients (especially N, but also P) can lead to large changes in S. virginica characteristics even in estuaries with high sediment nutrient levels.

Upward cascading effects of nutrients: shifts in a benthic microalgal community and a negative herbivore response

We evaluated the effects of nutrient addition on interactions between the benthic microalgal community and a dominant herbivorous gastropod, Cerithidea californica (California horn snail), on tidal flats in Mugu Lagoon, southern California, USA. We crossed snail and nutrient (N and P) addition treatments in enclosures on two tidal flats varying from 71 to 92% sand content in a temporally replicated experiment (summer 2000, fall 2000, spring 2001). Diatom biomass increased slightly (~30%) in response to nutrient treatments but was not affected by snails. Blooms of cyanobacteria (up to 200%) and purple sulfur bacteria (up to 400%) occurred in response to nutrient enrichment, particularly in the sandier site, but only cyanobacterial biomass decreased in response to snail grazing. Snail mortality was 2–5 times higher in response to nutrient addition, especially in the sandier site, corresponding to a relative increase in cyanobacterial biomass. Nutrient-related snail mortality occurred only in the spring and summer, when the snails were most actively feeding on the microalgal community. Inactive snails in the fall showed no response to nutrient-induced cyanobacterial growths. This study demonstrated strongly negative upward cascading effects of nutrient enrichment through the food chain. The strength of this upward cascade was closely linked to sediment type and microalgal community composition.