The effects of nitrogen and phosphorus enrichment on algal community development: Artificial mini-reefs on the Belize Barrier Reef sedimentary lagoon
Introduction
The productivity of benthic macroalgae is often nutrient-limited in tropical coral-reef ecosystems (Lapointe, 1987, Lapointe et al., 1987). Excessive water-column nutrient inputs to tropical reefs increase harmful algal interference with coral colonies, decreasing irradiance, reducing gas and nutrient exchanges, lowering productivity and ultimately causing die-offs. Nutrient/herbivory models, similar to the relative dominance model (RDM) for coral reefs (Littler and Littler, 2007), are receiving considerable attention [compare Fig. 7 in Littler and Littler, 1984 with the very similar Fig. 2a in Bellwood et al., 2004]. Understanding the effects of herbivore inclusion/exclusion-cage experiments (e.g., Lapointe et al., 2004, Bellwood et al., 2006) and feeding-preference studies (top-down control), in addition to much-needed data from nutrient-enrichment manipulations (bottom-up control), on lagoonal and coral-reef ecosystems is central to the elucidation of mechanisms that determine relative dominances, phase shifts and stable states.
Within healthy sedimentary lagoon environments, water-column nutrient concentrations become slightly elevated, herbivory is minimal and most of the available space is occupied by a restricted diversity of plant life (Macintyre et al., 1987). Water-column dissolved nutrients in combination with ample current flow are generally sufficient to allow substantial productivity of epilithic, epiphytic and other non-rhizomatous algal species within these habitats. However, the extreme nutrient constraints typically observed in the healthy coral-reef ecosystems upstream (Littler et al., 2006a, Littler et al., 2006b) are not as common in sedimentary lagoonal habitats, which are characterized by greatly elevated pore-water nutrient availability. For example, organic detritus rarely develops to high levels on coral-dominated reefs because of intense herbivory and export; whereas, sedimentary back-reef environments contain decomposing organic materials within extensive sediment layers that substantially elevate pore-water nutrient concentrations. These pore-water nutrients can leach or be biologically pumped upward to enrich the overlying water column where they are then accessible to nearby macroalgae (Larned, 1998). Because nutrient uptake kinetics in algae are mostly concentration dependent (Lapointe, 1997), growth rates of epilithic algal communities on lagoon rubble should be less nutrient limited than those on upstream coral reefs.
It is generally known and accepted that low-nutrient levels can saturate growth rates of macroalgae (see Lapointe, 1997, Lapointe, 1999). However, controversy has arisen (e.g., Hughes et al., 1999) as to the efficacy of universal threshold concentration values for DIN (1.0 μM dissolved inorganic nitrogen) and SRP (0.1 μM soluble reactive phosphorus) releasing macroalgal nutrient limitation for potential deleterious overgrowth of coral reefs, as well as the relative importance of each in regulating algal growth in tropical waters (Smith, 1984, Howarth, 1988). These very low-nutrient thresholds were originally hypothesized (Bell, 1992, Lapointe et al., 1997, Bell et al., 2007) regarding the lowered resiliencies for transitions from coral domination toward fleshy algal states. Such low-nutrient threshold concentrations are correlated with (Lapointe et al., 1993) harmful macroalgal overgrowth of seagrass and coral-reef communities along natural nutrient gradients on the Belize Barrier Reef, as well as being corroborated by in situ experimental nutrient-enrichment studies (e.g., Larkum and Koop, 1997, Thacker et al., 2001, Belliveau and Paul, 2002) on other coral reefs and associated lagoonal patch reefs (McClanahan et al., 2002, McClanahan et al., 2003). The above in situ experiments, carried out in geographically separated areas characterized by nutrient levels only marginally above 0.1 μM SRP and 1.0 μM DIN and documenting minimal algal stimulation following nutrient enrichment alone, serve to emphasize the low-nutrient concentrations involved (Littler and Littler, 2007).
Comparative studies contrasting nutrient limitation in back-reef sedimentary environments vs. coral reefs are few. Moreover, whether DIN or SRP are the most limiting to algal colonization and growth has been experimentally addressed only rarely (e.g., McClanahan et al., 2003). Historically, DIN is considered to be the main nutrient limiting productivity in tropical waters (Parsons et al., 1977). However, geochemical models (Smith, 1984) and in situ macroalgal bioassays (Lapointe, 1985, Lapointe, 1987, Littler et al., 1991, Lapointe et al., 1992) suggest that SRP, rather than DIN, is often the primary growth-limiting nutrient in carbonate-rich systems, such as the site studied here. In well-oxygenated tropical reef systems, SRP is often low due to its reaction with carbonate fluoroapatite (Gulbrandsen and Robertson, 1973). Conversely, in siliciclastic environments (Hanisak, 1990, Lapointe et al., 1992), DIN is most often the limiting nutrient.
The present study was designed to address the comparative ecological effects, in respect to DIN and/or SRP additions, regarding algal community development on artificial mini-reefs within a tropical back-reef sedimentary lagoon. The 12-mo study included in situ nutrient-enrichment recruitment/colonization experiments on mini-reef diffusers, as well as standing stock measurements, current assessments, seawater nutrient/tissue analyses and herbivory assays.
Section snippets
Study area
The 2.0 m deep study site (N16°48′11″, W88°04′50″) west of the Belize Barrier Reef back-reef flat is located on the back-reef sedimentary lagoon behind Carrie Bow Cay (Fig. 1) — not far (∼230 m west) from upstream oligotrophic coral-reef sites that were studied earlier (Lewis, 1986, Littler et al., 2006a, Littler et al., 2006b, Littler and Littler, 2007). Proximity to shelter has long been recognized (Randall, 1965, Ogden et al., 1973) as an important factor determining herbivore foraging ranges.
Water-column nutrient levels
The ambient DIN and SRP concentrations next to the bases of the non-enriched control diffusers were consistently above the 1.0 μM DIN and at the 0.1 μM SRP tipping-point levels for release of macroalgal growth (means = 2.06 μM DIN and 0.12 μM SRP; Fig. 2, Fig. 3), indicating that strictly oligotrophic conditions do not prevail on this sedimentary back-reef lagoon system. Both the DIN and the DIN + SRP nutrient diffusers filled with slow-release fertilizers produced the desired results (Fig. 2, Fig. 3),
Discussion
Nutrient manipulative studies have used window-screen baggies (Thacker et al., 2001), plastic pipes with holes (Flothmann and Werner, 1992, Furman and Heck, 2008), internally inoculated plastic bags (Lapointe, 1985, Lapointe, 1987, Miller and Hay, 1996), drilled hollow concrete blocks (Miller et al., 1999) and broadcast spreading (McClanahan et al., 2002; 1.0 kg of Scott's slow-release high-P fertilizer per 0.36 m2 plot) to disperse various chemical nutrients. We selected porous terra-cotta clay
Conclusions
While many coral-reef scientists agree that both nutrients and herbivory are important, and the details of their relative roles depend on the situation (see Lapointe, 1999, Bellwood et al., 2004), the coral-reef research community still needs a broader biological perspective to further the recognition of the role played by chronic nutrient enrichment in the coral-reef health/resilience paradigm. The problem is that bottom-up experimental research is logistically difficult and requires more
Acknowledgements
Support for this study came from the Smithsonian Institution Scholarly Studies Program, Caribbean Coral Reef Ecosystems Program (CCRE Contribution No. 869), the Smithsonian Marine Station at Ft. Pierce (SMSFP Contribution No. 808) and the National Museum of Natural History.[SS]
References (82)
- et al.
Sleeping functional group drives coral reef recovery
Curr. Biol.
(2006) - et al.
An experimental analysis of factors controlling the standing crop of the epilithic algal community on a coral reef
J. Exp. Mar. Biol. Ecol.
(1983) Spatial patterns of grazing intensity on a Caribbean barrier reef: herbivory and algal distribution
Aq. Bot.
(1981)Pollution and the degradation of coral reef communities
Strategies for pulsed nutrient supply to Gracilaria cultures in the Florida Keys: interactions between concentration and frequency of nutrient pulses
J. Exp. Mar. Biol. Ecol.
(1985)Phosphorus-rich waters at Glovers Reef Belize?
Mar. Pollut. Bull.
(2004)- et al.
A comparison of nutrient-limited productivity in macroalgae from a Caribbean barrier reef and from a mangrove ecosystem
Aq. Bot.
(1987) - et al.
The relative importance of nutrient enrichment and herbivory on macroalgal communities near Norman's Pond Cay, Exumas Cays, Bahamas: a “natural” enrichment experiment
J. Exp. Mar. Biol. Ecol.
(2004) - et al.
Macroalgal blooms on southeast Florida coral reefs: I. Nutrient stoichiometry of the invasive green alga Codium isthmocladum in the wider Caribbean indicates nutrient enrichment
Harmful Algae
(2005) - et al.
Macroalgal blooms on southeast Florida coral reefs: II. Cross-shelf discrimination of nitrogen sources indicates widespread assimilation of sewage nitrogen
Harmful Algae
(2005)
Herbivore abundance and grazing intensity on a Caribbean coral reef
J. Exp. Mar. Biol. Ecol.
The population and community structure of Hawaiian fringing-reef crustose Corallinaceae (Rhodophyta Cryptonemiales)
J. Exp. Mar. Biol. Ecol.
Animal-plant defense associations: effects on the distribution and abundance of tropical reef macrophytes
J. Exp. Mar. Biol. Ecol.
Harmful algae on tropical coral reefs: bottom-up eutrophication and top-down herbivory
Harmful Algae
Nutrient manipulation methods for coral reef studies: a critical review and experimental field data
J. Exp. Mar. Biol. Ecol.
Algal growth and species composition under experimental control of herbivory, phosphorus abundance in Glovers Reef, Belize
Mar. Poll. Bull.
An experimental analysis of the effects of herbivory and nutrient enrichment on benthic community dynamics on a Hawaiian reef
Coral Reefs
Kaneohe Bay, Hawaii: urban pollution and a coral reef ecosystem
Eutrophication and coral reefs: some examples in the Great Barrier Reef Lagoon
Water Res.
Reevaluation of ENCORE: support for the eutrophication threshold model for coral reefs
AMBIO
Effects of herbivory and nutrients on the early colonization of crustose coralline and fleshy algae
Mar. Ecol. Prog. Ser.
Confronting the coral reef crisis
Nature
Reconnaissance study of the geomorphology and benthic communities of the outer barrier reef platform, Belize
Herbivore vs. nutrient control of marine primary producers; context-dependent effects
Ecology
Mass mortality of a Caribbean sea urchin: immediate effects on community metabolism and other herbivores
Proc. Natl. Acad. Sci. U.S.A.
Seasonal growth in Laminaria longicruris: relations with dissolved inorganic nutrients and internal reserves of nitrogen
Mar. Biol.
Experimental eutrophication of an intertidal sand flat: effects on microphytobenthos, meio- and macrofauna
Epiphytic Cyanobacteria maintain shifts to macroalgal dominance on coral reefs following ENSO disturbance
Ecology
Effects of nutrient enrichment and grazers on coral reefs: an experimental assessment
Mar. Ecol. Prog. Ser.
Inorganic phosphorus in seawater
The use of Gracilaria tikvahiae as a model system to understand the nitrogen nutrition of cultivated seaweeds
Hydrobiologia
Nutrient limitation of net primary production in marine ecosystems
Annu. Rev. Ecol. Syst.
Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef
Science
Algal blooms on coral reefs: What are the causes?
Limnol. Oceanogr.
Pseudoreplication and the design of ecological field experiments
Ecol. Monog.
Historical over-fishing and the recent collapse of coastal ecosystems
Science
Facies and fabric specificity of early subsea cements in shallow Belize (British Honduras) reefs
J. Sediment. Petrol.
Effects of nitrate, phosphate and iron on the growth of macroalgae and benthic Cyanobacteria from Cocos Lagoon, Guam
Mar. Ecol. Prog. Ser.
Phosphorus-and nitrogen-limited photosynthesis and growth of Gracilaria tikvahiae (Rhodophyceae) in the Florida Keys: an experimental field study
Mar. Biol.
Nutrient thresholds for bottom-up control of macroalgal blooms on coral reefs in Jamaica and southeast Florida
Limnol. Oceanogr.
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