Comp. by: BSudhaRevises10000785639 Date:14/7/08 Time:17:04:25 Stage:1st Revises File Path://ppdys1108/Womat3/Production/PRODENV/0000000038/ 0000009008/0000000005/0000785639.3D Proof by: QC by: CHAPTER 21 c0021 Nitrogen Cycling in Coral Reef Environments Judith M. O’Neil and Douglas G. Capone Contents 1. Introduction 937 1.1. New developments 939 2. Nitrogen Cycle Processes 939 2.1. Nitrogen fixation 942 2.2. Nitrification 944 2.3. Dissimilatory nitrate reduction and denitrification 945 2.4. Nitrogen acquisition and uptake 946 2.5. Invertebrate/symbioses 947 2.6. Microbial populations 950 2.7. Ammonification and regeneration 951 3. Nitrogen Perturbations to Reefs 954 3.1. Inorganic N increases 955 3.2. Sea surface warming, coral disease and N dynamics 959 4. Elevated Nutrients on Coral Reefs Experiment (ENCORE) 960 5. Conclusion 962 Acknowledgements 963 References 963 s0010 1. Introduction p0010 Nitrogen cycling on coral reefs is a multifaceted process operating from the micro-scale of prokaryotes to ocean biogeochemistry cycles. Coral reefs are known for their high productivity despite low concentrations of ambient nutrients in the clear, well lit tropical and sub-tropical waters where they exist. Most of the produc- tivity associated with coral reefs is benthic (Crossland, 1983; D’Elia and Wiebe, 1990; Webb et al., 1975) and water column nutrient dynamics over the reef largely reflect net benthic metabolism. Most of the organic matter produced on the reef is recycled and retained in living organisms, or sediments within the reef system (Ayukai, 1995; Suzuki et al., 1995). p0020 Studying the changes in nutrient concentrations in waters before and after they flow over reefs was an approach first utilized to study coral reef nitrogen dynamics Nitrogen in the Marine Environment # 2008 Elsevier Inc. DOI: 10.1016/B978-0-12-372522-6.00021-9 All rights reserved. B978-0-12-372522-6.00021-9, 21 Caponeetal, 978-0-12-372522-6 937
2.3. Dissimilatory nitrate reduction and denitrification 945
2.4. Nitrogen acquisition and uptake 946
2.5. Invertebrate/symbioses 947
2.6. Microbial populations 950
2.7. Ammonification and regeneration 951
3. Nitrogen Perturbations to Reefs 954
3.1. Inorganic N increases 955
3.2. Sea surface warming, coral disease and N dynamics 959
4. Elevated Nutrients on Coral Reefs Experiment (ENCORE) 960
5. Conclusion 962
Acknowledgements 963
References 963
s0010 1. Introduction
p0010 Nitrogen cycling on coral reefs is a multifaceted process operating from themicro-scale of prokaryotes to ocean biogeochemistry cycles. Coral reefs are knownfor their high productivity despite low concentrations of ambient nutrients in theclear, well lit tropical and sub-tropical waters where they exist. Most of the produc-tivity associated with coral reefs is benthic (Crossland, 1983; D’Elia and Wiebe,1990; Webb et al., 1975) and water column nutrient dynamics over the reef largelyreflect net benthic metabolism. Most of the organic matter produced on the reef isrecycled and retained in living organisms, or sediments within the reef system(Ayukai, 1995; Suzuki et al., 1995).
p0020 Studying the changes in nutrient concentrations in waters before and after theyflow over reefs was an approach first utilized to study coral reef nitrogen dynamics
Nitrogen in the Marine Environment # 2008 Elsevier Inc.
DOI: 10.1016/B978-0-12-372522-6.00021-9 All rights reserved.
(Sargent and Austin, 1949). These studies were followed by the landmark work ofOdum and Odum (1955) and subsequently the Symbios project in Eniwetok Atoll,Marshall Islands in the Pacific, (Webb andWiebe, 1975;Webb et al., 1975;Wiebe et al.,1975) which enabled a ‘‘big picture’’ idea of the net fluxes of nutrients cycling on reefs.
p0030 The results of these early experiments framed our view of coral reefs as areas ofvery high gross productivity, but low net productivity, which was hypothesized tobe due to the efficient recycling of nutrients (D’Elia and Wiebe, 1990; Odum andOdum, 1955; Smith and Marsh, 1973). Research in the 1970s showed that reefscould be a source of nitrogen, particularly dissolved organic nitrogen (DON).Sources of nutrients to coral reef environments vary based on factors includingproximity to the coast, ocean topography and latitude, amongst others. Whereasopen ocean reefs can exist in extremely oligotrophic regions, reefs in fact exist alonga gradient of nutrient regimes in coastal and remote regions (Szmant, 2002).Nitrogen sources include upwelling, lateral advective transport, coastal runoff,groundwater seepage, N2 fixation and in situ regeneration (D’Elia, 1988), as wellas atmospheric inputs (Barile and Lapointe, 2005; Szmant, 2002) and localized guanoinputs (Albert et al., 2005; Smith and Johnson, 1995). Wet deposition of inorganicnitrogen in episodic rainfall events is estimated to provide up to 20% of the‘‘new’’ nitrogen to meet the metabolic demands of macroalgae on coral reefs inthe Bahamas (Barile and Lapointe, 2005). Of primary interest in the last few decadesis elucidating the anthropogenic components of groundwater seepage, coastal runoffand atmospheric deposition.
p0040 Understanding nitrogen cycling on coral reefs is paramount to understanding the‘‘paradox of the coral reef ’’: the anomalously high productivity in such low ambientnutrient waters (Szmant, 2002; Webb et al., 1975). Coral reefs have been describedas ‘‘oases’’ in an otherwise oceanic desert (Hoegh-Guldberg, 1999). Another appro-priate metaphor is perhaps that corals act as ‘‘cacti,’’ effectively conserving preciouslimiting resources. The two most important underlying mechanisms to explain thecoral reef paradox are: (1) the recycling of nutrients between algal symbiontsand invertebrate hosts and (2) new nitrogen (Dugdale and Goering, 1967) intro-duced through nitrogen-fixation by cyanobacteria and heterotrophic bacteria. Theclosely coupled nutrient and community dynamics that creates the circumstances for‘‘something from nothing’’ (Hoegh-Guldberg, 1999) reveals a very complex inter-relationship between habitat, hosts and symbionts with a true dependency betweenspecies (obligate mutualism).
p0050 How the species assemblages, and the delicate interchanges and balance amongspecies may react to environmental changes is currently being tested as anthropogenicinfluences increase across the world’s coral reef environments (Bellwood et al., 2004;Brodie, 1995; Hoegh-Guldberg, 1999, 2004a,b; Hughes et al., 2003; Knowlton, 2001;Pandolfi et al., 2003; Gardner 2003;Mora 2008). Increased concern over the fate of theworld’s coral reefs due to pronounced declines in the areal extent of coral reefs, theirhealth and biodiversity, has been a central theme and impetus of much of the coral reefresearch carried out in recent decades (Birkeland, 1997, 2004). In addition to studyingnutrient inputs, research has focused on the effect of other anthropogenic influencesincluding over-fishing, coastal development and global climate change (Pew OceansCommission, 2003).
p0060 Recent research on nitrogen cycling on coral reefs ranges from the further elucida-tion of the structural and functional properties of the reef that increase regenerationof nutrients leading to enhanced retention of nutrients within the reef system(Szmant, 2002), to the finer details underlying cycling of nutrients and the emergingimportance of microbes interacting with the entire coral ‘‘holobiont.’’ In additionto the coral itself, this includes the zooxanthelleae, fungi, endolithic algae and >30species of bacteria as well as the recently discovered coral-associated Archaea (Wegleyet al., 2004). Oceanic Archaea have recently been found to play an important rolein nitrification in the marine N cycle (see Chapter 5 by Ward, this volume).
p0070 Other new developments reveal that heterotrophic bacteria in the coral mucuslayer (and other areas of the coral colony) may be absolutely essential to the health,nutrient cycling and resilience of the coral holobiont (Knowlton and Rohwer, 2003;Rohwer et al., 2002). The importance of both coral mucus (Wild et al., 2004a, 2005,2008) and products from mass spawning (Wild et al., 2004b; Patten et al., 2008) asnutritional sources back into the reef system has also been recognized. The impor-tance to biogeochemical sedimentary cycling and microbial processes, both bacterialand viral have also been recognized (Hewson et al., 2007; Patten et al., 2008). Thesenew insights all underscore the point that we have not teased out all the importantnutrient drivers and interactions in the reef ecosystem.
p9000 The fact that symbiotic associations on reefs are more complex than we haverealized to date, is further demonstrated by work in the Caribbean using del 15Nvalues, which demonstrated that in someMontastrea cavernosa coral colonies nitrogenis obtained by zooxanthellae from cyanobacterial endosymbiotic nitrogenfixers.This ability appears to increase with depth, and dependency on heterotrophy.Greater depth also translates to less photosynthetically active zooxanthellae in thecoral colonies and therefore less oxygen evolution which benefits the oxygensensitive diazotrophic symbionts (Lesser et al., 2007). This raises multiple questionsabout nutrient feed back loops between the coral host, symbiotic dinoflagellates andthe cyanobacteria in terms of what role nitrogen ultimately plays as a “limiting andregulatory element” in this symbiotic associations (Lesser et al., 2007). This is just asmall indication of how much more is yet to be unraveled in terms of the intricatemutualistic relationships involved in coral reef ecosystem functioning. It may provethat the symbiotic relationship between bacteria and corals, as well as other inverte-brate hosts, is just as integral to the coral as a whole, as their relationship withsymbiotic dinoflagellates (zooxanthellae).
p0080 Other new insights gained recently include the potential importance of atmo-spheric deposition, including the role of dust, as bearer of nutrients (Barile andLapointe, 2005), as well as pathogens and metals (Garrison et al., 2003; Prosperoet al., 2005). Another previously under-valued component in nutrient cycling in reefenvironments is the ‘‘secret-garden’’ of benthic microalgae (or microphytobenthos)which have emerged as major primary producers in coral reef systems and majormediators of nutrient flux at the sediment interface (Heil et al., 2004; MacIntyre et al.,1996; Werner et al., 2008). The one theme unifying all recent aspects of work onnutrient cycling on reefs is the incredible complexity of nutrient dynamics in these
systems. It also underscores the need to further elaborate the details of these dynamics,as we bring to bear the tools of molecular biology, remote sensing and geochemistry,as well as other technologies to these questions. By doing so, we may gain a betterunderstanding of the diverse mutualistic and symbiotic relationships that are integralcomponents in the coral reef nitrogen cycle.
s0030 2. Nitrogen Cycle Processes
p0090 Coral reefs are areas of intense nitrogen cycling andmay contribute to the largerbiogeochemical cycling of C and N in the ocean (Capone, 1996a,b; Crossland et al.,1991; see also Carpenter and Capone, Chapter 4, this volume) (Fig. 21.1). Nitrogenfixation appears to satisfy much of the demand for new N in these systems and mayprovide a substantial input to the marine N cycle beyond the immediate reef area.High rates of nitrification also occur and likely contribute to N2O fluxes to theatmosphere, although more research is needed in this area (Capone, 1996b). All themajor features of themarineN-cycle aremediated by biological, rather than chemicalprocesses (Webb, 1981), which is in contrast, for instance, to phosphorus cycling(D’Elia, 1988). In addition to its role as a nutrient, because of its potential to be
transformed among various oxidation states, species of nitrogen can act as a reductantor oxidant in energetic reactions (D’Elia and Wiebe, 1990). Aspects of the majorpathways of nitrogen on coral reefs which include: nitrogen fixation (Fig. 21.1A);ammonification (Fig. 21.1B); nitrification (Fig. 21.1C); denitrification (Fig. 21.1D);uptake and regeneration (Fig. 21.1E and F), have been reviewed previously (D’EliaandWiebe, 1990 and references therein), and are summarized in Fig. 21.1.Coral reefsediments can contain relatively high nitrogen concentrations with values generally10-fold or greater than in the water column (Capone et al., 1992; Corredor andCapone, 1985; Corredor and Morell, 1985; D’Elia and Wiebe, 1990; Hatcher andFrith, 1985; O’Neil and Capone, 1989).
p0100 Nitrogen occurs in a range of forms in the reef environment. Concentrations ofnitrate and ammonium in reef environments vary by an order of magnitude in thewater column ranging from �0.05–0.5 mM. Nitrite is usually below 1 mM. DON isusually the form of nitrogen in highest concentration in the reef water columnranging typically from 5–50 mM (Atkinson and Falter, 2003; Crossland, 1983;Table 21.1). Nitrogen concentrations in porewater can be several orders of magni-tude higher than the water column. Reef porewaters can be anoxic within a matterof cm in many cases and values of nitrate range from 1–6 mM nitrate, withammonium concentrations ranging from 2–80 mM ammonium (Atkinson andFalter, 2003; Capone et al., 1992), although higher values can be seen in alteredsystems (e.g., values up to 300 mM, see Corredor and Morrell, 1985; Entsch et al.,1983; Hines et al., 1992).
p0110 Since nitrogen concentrations in pore water are higher than in the water column,there is often a net flux of nutrients out of the sediments (Williams et al., 1985). Thismay be of particular importance in areas of low flushing and pooling in reef areas(Szmant-Froelich, 1983; Szmant, 2002). However, these processes are also quitevariable in space and time due to various factors including sediment type, hydrody-namics and loading (Corredor and Morrell, 1985).
p0120 In most marine ecosystems, the largest N fluxes occur between inorganic andorganic pools of nitrogen. The net incorporation of inorganic nitrogen into organicnitrogen is generally attributed to photoautotrophs. Regenerative processes, includ-ing the production of NH4
þ, are usually associated with heterotrophic processesalthough depending on the C:N ratio of the organic matter being consumed, hetero-trophs can also account for net N immobilization (Kirchman, 1994). For comparativepurposes, areal rates of net phytoplankton productivity in oligotrophic waters typicallyaccount for 0.3–0.7 mol N m�2 year�1 (Berger et al., 1987; DeVooys, 1979), whereascoral reef net production may account for areal demands of N in excess of 43 molN m�2 year�1 (Capone, 1996a; Smith, 1984).
p0130 Regeneration within the sediments as well as a variety of sites within the coralreef structure itself are all extremely important (Capone, 1996a; DiSalvo, 1971;Szmant-Froelich, 1983). This efficient regeneration of nutrients fuels the intenseproductivity of the coral reef system and results in a tendency to export a smallerpercentage of total production than other marine systems (D’Elia and Wiebe, 1990).Therefore, regeneration of N in coral reefs must meet demands. (Charpy-Roubaudand Larkum, 2005).
p0140 Nitrogen fixation (see also Chapter 4 by Carpenter and Capone, this volume), theprocess by which certain prokaryotes can reduce atmospheric N2 gas to ammoniumvia the nitrogenase enzyme pathways has long been thought to an important linchpinof nitrogen cycling and productivity in coral reef areas (D’Elia and Wiebe, 1999;Larkum et al., 1988) (Fig. 21.1A). The first demonstration of the importance ofnitrogen fixation in reef environments by cyanobacteria (originally hypothesized byOdum and Odum, 1955), was demonstrated in the Symbios project (Crossland andBarnes, 1976; Hanson and Gundersen, 1977; Wiebe et al., 1975). Indeed, it is ‘‘aprominent component of the nitrogen-cycle on coral reefs which may relieve N limitation andmake a globally significant contribution to overall marine N inputs’’ (Capone, 1996a).
t0010 Table 21.1 Nitrogen concentration in tropical coral reef sediments and overlyingwater columns
Nitrogen typeRange ofconc (mM)
Typicalconc (mM) References
NO3� (sed) 1–6 <5 Atkinson and Falter (2003), Capone
et al. (1992)
NO3� (water) 0.05–9.8 0.05–0.5 Crossland and Barnes, (1983),
Crossland and Barnes, (1974), Falter
and Sansone, (2000), Furnas et al.
(1995), Johannes, et al. (1972),
Johannes, et al. (1983), Kinzie, et al.
(2001), Lapointe, (1997), Tribble
et al. (1990), Webb, et al. (1975),
Szmant and Forrester, (1996)
NH4þ (sed) 2.3–300 20–80 O’Neil and Capone, (1989), O’Neil
and Capone, (1996)
80
NH4þ (water) bd-2.4 0.05–0.5 Crossland and Barnes, (1983),
Crossland and Barnes, (1974), Falter
and Sansone, (2000), Furnas et al.
(1995), Johannes et al. (1972),
Johannes et al. (1983), Kinzie et al.
(2001), Lapointe, (1997), Tribble
et al. (1990), Webb et al. (1975),
Szmant and Forrester, (1996)
DON (sed) Na na na
DON (water) bd-22 <5 Crossland and Barnes, (1983), Furnas
et al. (1995), Johannes et al. (1972),
Johannes et al. (1983), Kinzie et al.
(2001), Lapointe, (1997), Webb
et al. (1975), Alongi et al. (1996)
Source: Atkinson and Falter (2003).bd ¼ below detection limits. na ¼ not available.
p0150 Many studies since the 1970s found high rates of nitrogen fixation (see Chapter 4Capone and Carpenter, this volume). In fact, nitrogen fixation on coral reefs has beenreported at rates that at times exceed that of intensive legumous crops (Szmant, 2002;Webb et al., 1975). This energetically demanding process in cyanobacteria is fueled bythe high light flux and recycled phosphorus. Heterotrophic diazotrophic activity issupported by a combination of recycled P and organic matter (D’Elia, 1988).
p0160 In addition to nitrogen fixation associated with the extensive sediments in andaround reef flats (Capone et al., 1992; Corredor and Morrell, 1985; O’Neil andCapone, 1989; Wilkinson et al., 1984; Mayajima et al., 2001; Hewson andFuhrman, 2006; Werner et al., 2008), nitrogen fixation activity has been detectedassociated with live corals (Williams et al., 1987; Lesser et al., 2007), and coral skeletons(Crossland and Barnes, 1976; Larkum, 1988; Shashar et al., 1994a,b; Davey et al., 2008)as well as with epiphytes on macroalgae (Capone et al., 1977; France et al., 1998;O’Neil and Capone, 1996) and by cyanobacterial mats. Nitrogenase activity has alsobeen measured on limestone reef surfaces (Charpy-Roubaud et al., 2001), includingexposed atoll rim areas of various sorts, all attributable to cyanobacteria. In TikehauLagoon, French Polynesia, for instance, nitrogen fixation on these surfaces accountedfor 25–28% of the total nitrogen demand for benthic primary productivity (Charpy-Roubaud et al., 2001; Charpy-Roubaud and Larkum, 2005). Rates of nitrogenfixation in sediments, while lower than rates in localized areas or in mats of cyano-bacteria (Iizumi et al., 1990; Charpy et al., 2000; Bauer et al., 2008), when integratedover the large areal extent of sedimentary environments can make a significantcontribution to the overall coral reef ecosystem (Capone, 1996a; Capone et al.,1992; O’Neil and Capone, 1989). Low d15N signatures noted in reef macrophytesand coral tissue provide further evidence that much of the nitrogen in reef systems isderived from nitrogen fixation (France et al., 1998; Yamamuro et al., 1995).
p0170 Rates of nitrogen fixation in reef environments are variable and can be affectedby the presences of grazers. Grazing by Acanther plancii, the crown of thorns starfishon corals resulted in high rates of nitrogen fixation on the coral skeletons after theoutbreak of this starfish (Larkum, 1988). Similarly, the sea urchin Diadema antillarumwas shown to significantly increase nitrogen fixation when grazing on ‘‘algal turf ’’ inreef environments, as compared to areas where no sea urchins were present. The‘‘diminutive’’ tightly cropped ‘‘algal turf’’ assemblage contained a significant pro-portion of cyanobacteria in addition to benthic diatoms and dinoflagellates (Williamsand Carpenter, 1997). Grazers also aid in nitrogen cycling by excreting nitrogenouswaste which enhances algal turf, while simultaneously cropping it (Williams andCarpenter, 1997) (see below). Fish grazing may also be important in maintainingrates of nitrogen fixation on reefs, by keeping other benthic algae in check. Somediazotrophic cyanobacteria are less palatable than other algae, as they often havechemical deterrents, and also tend to be less nutritionally complete, lacking someessential fatty acids, and hence macroalgae are often preferred by grazers (Capperet al., 2005; O’Neil, 1999). Therefore, cyanobacteria may have less competition forgrowing space and expand into areas where the more palatable species have beenremoved by grazers (Wilkinson and Sammarco, 1983).
p0180 A major fraction of total benthic nitrogen fixation on a global scale may comefrom shallow coral reef environments (Capone, 1983). However, whereas rates of
pelagic nitrogen fixation have been steadily refined by surveys of the filamentouscyanobacterium Trichodesmium (Capone et al., 2005), novel geochemical approaches(Mahaffey, 2005), and the potential importance of unicellular nitrogen fixersrevealed (Montoya et al., 2004), nitrogen fixation in coral reef environments remainsunder-sampled and underestimated. Nitrogen fixation by benthic or symbioticcyanobacteria (Charpy et al., 2007; Lesser et al., 2007; Bauer et al., 2008; Daveyet al., 2008) as well as heterotrophic bacteria including those epiphytic on macro-algae and coral surfaces (Davey et al., 2008), have yet to be fully elucidated (Koopet al., 2001; O’Neil and Capone, 1989, 1996; Hewson et al., 2007; Werner et al.,2008). The diazotrophic community may in fact be changing as a consequence ofcoastal eutrophication. Nitrogen fixation could either decrease due to nitrogenloading, or increase in response to inputs of limiting factors such as phosphorus ormicronutrients such as Fe, decreases in N:P loading ratios, or as a result of organicloadings and stimulation of heterotrophic N2 fixation directly through provision oforganic substrates or the increase in local anoxic zones.
p0190 Black band disease (BBD), which is caused by a consortium of cyanobacteria andmicrobes may be diazotrophic (Frias-Lopez et al., 2002, 2003). This hypothesis wasrecently suggested by a molecular study of bacterial communities associated withBBD which yielded a 16sRNA sequence 97% homologous with the nitrogen fixingpelagic cyanobacterium Trichodesmium tenue. This led the authors to speculate thatnitrogen fixation might be carried out in the oxygen depleted microzones of theBBD assemblage (Frias-Lopez et al., 2002). More work is needed to test thishypothesis in a rigorous manner as subsequent work on isolated Phormidium corally-ticum (formerly Oscillatoria corallinae) from Florida corals with BBD tested negativefor nitrogen fixation (acetylene reduction) activity (Richardson and Kuta, 2003).
p0200 Invertebrate diazotrophic symbioses have been reported from reef systemsincluding reef sponges that acquire fixed nitrogen via associated cyanobacteria(Wilkinson and Fay, 1979). Symbiotic cyanobacteria and bacteria are found inalmost all marine sponges (Mohamed et al., 2006; Thacker, 2005) and may formmutualistic associations with hosts especially if the symbiont provides fixed C or N.The cyanobacterium Oscillatoria spongieliae has been found within several species ofsponges including the reef spongeDysidea herbacea on the Great Barrier Reef (GBR)(Flowers et al., 1998; Ridley et al., 2005). Synechococcus has also been described fromseveral species of sponge, which are genetically distinct from free living planktonicspecies of Synechococcus (Thacker, 2005). In some instances metabolic products (e.g.,fixed carbon) are translocated from symbiont to host (Arillo et al., 1993). However,in most cases the relationship between host and symbiont are not well defined(Ridley et al., 2005).
p0210 Potential translocation of N from nitrogen fixers to hosts has also been investi-gated. Nitrogenase activity was reportedly associated with an intact Procholoron-Ascidian association (Lissoclinum sp.) (Paerl, 1984), although activity could not bedirectly detected from the isolated symbiont (Odintsov, 1991). It was subsequentlydetermined that at least a portion of the cellular N was derived (directly or indirectly)from N2 fixation, based on the low isotopic ratio of 15N/14N in Lissoclinum sp.associations (Kline and Lewin, 1999). Diazotrophs have also been found associatedwith corals (Frias-Lopez et al., 2002; Rohwer et al., 2001, 2002; Shashar et al., 1994a,b)
with nitrogen fixation measured in some live corals (Shashar et al., 1994a,b;Williams et al., 1987). More recently the presence of a diazotrophic coccoidcyanobacteria has also been reported in the tissues of certain species of the coralMontastrea (Lesser et al., 2004). Interestingly it has been further demonstrated throughdel N analyes that the zooxanthellae from Caribbean colonies ofMontastraea cavernosacolonies which contain the endosymbiotic cyanobacteria acquire N from the nitrogenfixing cyanobacteria rather than the coral host (Lesser et al., 2007).
s0050 2.2. Nitrification
p0220 Nitrification has been conventionally viewed as the two step process by whichcertain groups of chemoautotrophic bacteria oxidize ammonium to nitrite andsubsequently, another group of chemoautotrophic bacteria, oxidize nitrite to nitrate(Fig. 21.1C) (see Chapter 5 by Ward, this volume). Nitrification generally occurs inaerobic zones throughout the marine environment, and can occur at high rates incoral reef ecosystems (Capone et al., 1992; Corredor and Capone, 1985; Corredoret al., 1988; Johnstone et al., 1990; Wafar et al., 1990; Webb et al., 1975). Nitrifica-tion in reef lagoons can oxidize ammonium recently released from nitrogen fixationor regenerative processes (Webb and Wiebe, 1975). Nitrification is also thought tobe a major source of N2O in marine systems, and may contribute to the overall weakmarine N2O flux to the atmosphere (Capone, 1996b) (see also Chapter 2 by Bange,this volume).
p0230 Nitrification on coral reefs was first noted when net nitrate production wasmeasured at Eniwetok Atoll. This, in conjunction with the isolation of a species ofnitrifying bacteria, Nitrobacter agilis, was taken as strong evidence for nitrification as asignificant process in the reef system (Webb andWiebe, 1975). Ammonium oxidationand nitrite oxidationwere presumed to be closely coupled as therewas not a build up ofthe intermediary product nitrite (D’Elia and Wiebe, 1990). Coral reef sediments inPuerto Rico showed nitrification rates that were highest in the upper few centimetersof sediment, with a second peak �20 cm (Corredor and Capone, 1985). Nitrifyingbacteria have also been identified as sponge symbionts on reefs in the Caribbean(Corredor et al., 1988). Later studies investigating the relationship between four spongespecies including the Caribbean coral reef species Chondrilla nucla found that highestrates of nitrate release were associated with sponges that had cyanobacterial endosym-bionts (Diaz and Ward, 1997) suggesting that sponge-mediated nitrification may bevery common in tropical benthic communities and may constitute a large input ofoxidized nitrogen in these systems (see Chapter 27, Foster andO’Mullin, this volume).However, further research is needed to elucidate the details of these pathways.
p0240 Recently research has revealed that nitrification is not exclusively associatedwith chemoautotrophic bacteria of the b and g proteobacteria, but occurs in manyCrenarcheaota as well (Francis et al., 2005; Konneke et al., 2005; Wuchter et al.,2006) and in fact may dominate this process in seawater (Wuchter et al., 2006)(see Chapter 5 by Ward, this volume). The extent that archael nitrificationoccurs in coral reef habitats remains to be determined. Ammonium oxidationhas also been shown to occur anoxically in some marine sediments at the expenseof NO2
� (Thamdrup and Dalsgaard, 2002) (see Chapter 6, Devol, this volume).
This process is termed ‘‘Anammox’’ for ‘‘anaerobic ammonium oxidation’’ and iscatalyzed by a specialized group of planctomycetes first discovered in sewagereactors (Strous and Jetten, 2004). Again, the importance of Anammox in coralreef environments has not yet been considered.
s0060 2.3. Dissimilatory nitrate reduction and denitrification
p0250 There are two pathways of dissimilatory nitrate reduction, generally thought to bemediated by anaerobic, or facultatively anaerobic bacteria, using NO3
� as a terminalelectron acceptor in respiration (Fig. 21.1D and F) (see Chapter 6, Devol, thisvolume). One pathway leads to production of ammonium, and may act as aninternal cycling loop within the system (D’Elia and Wiebe, 1990). The otherpathway, denitrification, ends in production of N2O gas and N2 gas, which canthen be lost from the system to the atmosphere.
p0260 Denitrification has been measured in a number of reef environments with highlyvariable rates obtained (Capone et al., 1992; Corredor and Capone, 1985; Johnstoneet al., 1990; Koop et al., 2001; O’Neil and Capone, 1996; Seitzinger and D’Elia,1985; Smith, 1984; Williams et al., 1985). This may be related to differences insubstrate availability as well as differences in sediment organic and nutrient content(Koop et al., 2001; O’Neil and Capone, 1996).
p0270 Denitrification was originally dismissed as an important process on reefs as itwas thought that anaerobic processes would not occur in a seemingly aerobicenvironment and additionally, high amounts of nitrate exportation had been obser-ved (D’Elia and Wiebe, 1990; Wiebe, 1976). Denitrification does indeed occur,however its extent within reef sediments and the reef matrix after the deposition ofparticulate organic matter is a large unknown (Furnas, 2003).
p0280 Additionally, the anammox reaction mentioned earlier results in the reduction ofNO2
�with the production of N2 gas. Recent direct tracer evidence from both marinesediments (Thamdrup and Dalsgaard, 2002) (see Chapter 6, Devol, this volume) andseveral anoxic water column systems (Hamersley et al., 2007; Kuypers et al., 2005) hasshown that the anammox pathway, rather than conventional denitrification, can be asignificant and, at times, predominant source of N2 production. Future studies ofcombined N loss from reefal environments should also consider this pathway.
s0070 2.4. Nitrogen acquisition and uptake
p0290 Uptake of combinedN by organisms for growth is an aspect of the nitrogen cycle thathas been relatively well studied for the coral/algal symbiosis (D’Elia andWebb, 1977;Webb and Wiebe, 1978; Blythell, 1990a,b). Other organisms in the reef environ-ment, including macroalgae, benthic microalgae and phytoplankton as well as manyheterotrophic prokaryotes have the capacity to take up combined nitrogen.
p0300 Oxidized forms of nitrogen such as nitrate, need to first be reduced to ammo-nium before their incorporation into biomass. Nitrate is reduced by the enzymeassimilatory nitrate reductase. Assimilatory nitrite reduction is essentially an inter-mediary step in the reduction of nitrate to ammonium (D’Elia and Webb, 1977)(Fig. 21.1E) (see Chapter 7, Mulholland and Lomas, this volume).
p0310 In most marine ecosystems primary productivity is concentrated in water columnphytoplankton, but the bulk of coral reef productivity occurs in the benthos and canbe attributed to coral zooxanthellae, turf algae and benthic micro and macroalgae(Larkum, 1983; Taylor, 1983a,b). Benthic microalgae (also called microphyto-benthos, Macintyre et al., 1996) are a diverse assemblage of diatoms, dinoflagellates,and cyanobacteria with poorly understood with regard to the influence of theirproductivity and abundance to nutrient dynamics relative to some of the othernutrient processes on coral reefs (Heil et al., 2004). Benthic microalgae are ubiqui-tous and abundant in the clear well lit environments of many coral reefs, and canhave chlorophyll values 100� that of the integrated water column above them.Areal rates of photosynthesis by these turfs rival terrestrial systems and implysubstantial N demand (Heil et al., 2004; Werner et al., 2008).
p0320 Benthic microalgae in and on reef sediments may derive some of their nutrientsfrom the sediments as appreciable ammonium levels have been reported (Caponeet al., 1992; Heil et al., 2004; Johnstone et al., 1990). Increases in benthicmicroalgae with nutrient enrichment suggest that these populations can also accessnutrients in the water column, which result from regenerative processes within thewater column. Benthic microalgae are also net O2 producers which may influencenutrient dynamics, particularly nitrification and denitrification by changing redoxprofiles as well as the nutrient exchange across the sediment water interface.
s0080 2.5. Invertebrate/symbioses
p0330 Perhaps the most significant evolutionary adaptation for sustained high productivityin oligotrophic seas is the symbiotic relationships that lead to efficient retention andrecycling of nutrients in these systems (Hoegh-Guldberg, 1999; Miller andYellowlees, 1989). The multitude of algal-invertebrate symbioses that have evolvedin reef environments to efficiently recycle nutrients is a testament to this strategy(Muscatine and Porter, 1977). Nitrogen transformations are the centerpieces of theseassociations (Taylor, 1983a); with the symbiotic dinoflagellates (zooxanthellae)providing C for translocation from photosynthesis to coral animal host, and thetransfer of N from animal waste to the symbiotic algae (Taylor, 1983b; Wilkersonand Trench, 1986) (Fig. 21.2). Other, diverse but less well characterized symbiosesoccur in coral reef environments including microbes associated with sponges (e.g.,Garson et al., 1998; Mohamed and Hill, 2006; Thacker, 2005; Wilkerson and Fay,1979; also Chapter 27, Foster and O’Mullin this volume), giant clams (e.g.,Ambariyanto and Hoegh-Guldberg, 1999; Fitt et al., 1995; Summons et al., 1986;Wilkerson and Trench, 1986), anemones (e.g., Cook et al., 1988, 1992; Wang andDouglas, 1997); scyphozoan jellyfish (e.g., Wilkerson and Kremer, 1992), andAscidians (see Chapter 4 by Carpenter and Capone, and Chapter 27, Foster andO’Mullins, this volume) as well as N transfer from endosymbiotic, diazotrophiccyanobacteria to symbiotic dinoflagellates within a coral (Lesser, 2007). Aspects ofeach of these symbiotic associations revolve around interactions with nitrogen.
p0340 Animals in general are not able to take up inorganic nitrogen directly (Muscatineet al., 1979), and usually excrete reduced nitrogenouswastes into the surroundingwater(Rahav et al., 1989). Algal-invertebrate symbioses of coral reefs are an exception to this
generalization (Cook et al., 1987, 1988; Cook et al., 1992; Miller and Yellowlees,1989). In particular, the algal-anthozoan symbioses have been termed the ‘‘physiologi-cal chimera between alga and animal’’ (Furla et al., 2005). Corals can take up bothdissolved inorganic (e.g., Badgley et al., 2006; Crossland and Barnes, 1977; Groveret al., 2003a,b; Tanaka et al., 2006) and organic nitrogen (e.g., Hoegh-Guldberg andWilliamson, 1999; Grover et al., 2006), as well as ingesting particulate nitrogen (e.g.,Anthony, 2000; Lawn and McFarlane, 1991; Mills et al., 2004; Ribes et al., 2003).
p0350 The amount of nitrogen available to corals is a function of both particulate hostfeeding as well as inorganic N uptake which can be effected by nutritional history(Piniak and Lipshultz, 2004). Corals and other sessile organisms can acquire neces-sary nutrients by harvesting zooplankton, microbes and detritus from the watercolumn directly (Erez, 1990; Lawn and McFarlane, 1991; Porter, 1974, 1978)through mucus-netting strategies, or indirectly by capture of protozoa that grazeon bacteria. These trapping processes are so efficient it has been termed ‘‘the wall ofmouths’’ (Yonge, 1930) and are one of the matrix of factors that permit coral reefs tosupport high biomass concentrations in oligotrophic waters. Corals can gain up to70% of their nitrogen budget from particulate sources and microbes which accountfor 30–45% of the incorporated particulate matter (Bak et al., 1998).
p0360 A second pathway is by the uptake up dissolved inorganic nitrogen (DIN) by thesymbiont. The inorganic nitrogen may itself derive from recycling of animal wasteswhich are then retained by the symbionts in exchange for photosynthate releasedback to the host (Muscatine et al., 1989; Piniak and Lipschultz, 2004; Wang and
Low nutrient conditions
result in low rates of symbiont
growth but high release of
organic matter , resulting in
high rates of coral growth
and reproduction
High nutrient conditions
result in high symbiont
growth but low release of
organic matter , resulting in
low rates of coral growth
and reproduction
N+P
N+P
N+P
CaCO3CaCO3
CaCO3 CaCO3
CO2
CO2 CO2
CO2
org org
N+P
f0020 Figure 21.2 Nutrient availability changes the relationship between microalgal symbionts andcoral hosts (adapted from Dubinsky and Stambler,1996; Furnas, 2003). Under low nutrient condi-tions zooxanthellae translocate photosynthate to corals for growth, calcification and reproduc-tion. Under higher nutrients, zooxanthellae increase in abundance and keep more of thephotosynthate for themselves; translocating less to host coral formetabolic needs.
Douglas, 1998, see below). Alternatively, the symbiont may obtain inorganicnitrogen either in reduced (e.g., ammonium) or oxidized forms (e.g., nitrate)directly from seawater (Bythell, 1990a,b; Ferrier-Pages et al., 2001; Marubini andDavies, 1996; Wilkerson and Trench, 1986). The latter is often a light dependentprocess (Grover et al., 2003a,b). It has further been demonstrated that both intactcorals (D’Elia and Web, 1977), as well as isolated zooxanthellae, can take up bothnitrate and ammonium (Bythell, 1988; Grover et al., 2003a,b). This net uptake canaccount for approximately 30% of the daily nitrogen requirement for tissue growth,gamete production and DON production (Bythell, 1988, 1990a,b).
p0370 Summons and Osmond (1981) first demonstrated light dependent uptake of 15Nlabeled nitrate, ammonium and urea by zooxanthellae which they attributed to theglutamine synthetase–glutamate synthase (GS-GOGAT) pathway. Anderson andBurris (1987) directly confirmed GS activity in symbionts isolated from corals andin pure culture (see also Miller and Yellowlees, 1989). In contrast, in giant clamsYellowlees et al. (1994) reported ammonium assimilation in zooxanthellae wascatalyzed by the glutamate dehydrogenase enzyme (GDH). Exactly how this mech-anism works has not been fully elucidated as both the symbionts and host appear tocontain the enzyme GDH (Wilkerson andMuscatine, 1984; Yellowlees et al., 1994).The model proposed by D’Elia et al. (1983) suggested a ‘‘depletion-diffusion’’ modelfor ammonium uptake, where the symbiont takes up ammonium at a rate thatdepletes the concentration in the tissue and allows for diffusion of nutrient throughthe animal tissues. In sea anemones with zooxanthellae there is evidence of uptakeand translocation of ammonium derived nitrogen using 15N tracers (Lipschultz andCook, 2002).
p0380 The symbiotic dinoflagellates (zooxanthellae) are responsible for the uptake ofthe inorganic nitrogen, subsequently synthesizing organic compounds that are trans-located to the host (Wang andDouglas, 1999).Whereas early workers focused on therelease of glycerol by the dinoflagellate symbionts, Muscatine first showed thatalanine was also an important metabolite (Muscatine, 1980). The symbionts thusallow coral systems to retain and incorporate inorganic nitrogen at micromolar, anddown to nanomolar, concentrations (Muscatine and D’Elia, 1978; Grover et al.,2002). Translocation of the amino acid aspartate from symbiotic dinoflagellates totheir anemone hosts can occur (Swanson and Hoegh-Guldberg, 1998). Other studiesrevealed the incorporation of aspartate into proteins that are deposited rapidly asskeletal organic matrix (Allemand et al., 1998). This may be indicative of pathways ofprotein synthesis that are unique for the skeletal matrix and different from the generalcoral protein metabolism, or due to endolithic algal communities within the coralskeleton (Hoegh-Guldberg, 2004a,b).
p0390 Experiments with nitrogen additions have given some insight into the role ofnitrogen in the algal-coral symbiosis relationship. Additions of ammonium andammoniumþ phosphate increased both zooxanthellae density; their protein synthe-sis rates (Muscatine et al., 1989); as well as the amount of chlorophyll and nitrogen persymbiont (Snidvongs and Kinzie, 1994). More recently, Tanaka et al. (2006) demon-strated that 50% of 15NO3
� and 13C delivered to the coral Acropora pulchra was takenup and appear in the host in organic forms; demonstrating translocation from thezooxanthellae. The C:N ratio of the translocated organic matter appeared to change
based on the N availability for the zooxanthellae. The incorporated organic 15Nseems to be recycled within the coral-algal symbiotic system, with high C:N com-pound such as lipids and carbohydrates being more rapidly utilized than lower C:Ncompounds such as proteins and nucleic acids (Tanaka et al., 2006).
p0400 Yet other pathways of nitrogen acquisition may exist. Symbionts are able to takeup dissolved free amino acids (DFAA) (Ferrier, 1991; Hoegh-Guldberg andWilliamson, 1999). In the coral Pocillopora damicornis, DFAA uptake from seawatercan account for �11% of the nitrogen demands in the coral. Uptake of DFAA hasalso been shown by the giant clam Tridacna maxima (Ambariyanto and Hoegh-Guldberg, 1999). This may be an important episodic source of nitrogen for coralsduring times of local fish migrations and the activity of other grazers that result inalgal cell breakage or exudation which increase DON concentration on the reef(Hoegh-Guldberg and Willamson, 1999). More recently, concentration dependentuptake of 15N-urea was demonstrated in the coral Stylophora pistillata (Grover et al.,2006). Uptake kinetics suggested adaptation of the corals to low seawater concen-trations of urea and, when compared to uptake rates of ambient ammonium andnitrate concentrations, urea was preferred to nitrate. Urea therefore may also be animportant episodic source of nitrogen as well.
p0410 Zooxanthellae provide much of the coral’s energy; transferring up to 95% of thesymbiotic algae’s photosynthate to the host (Fine and Loya, 2002; Muscatine, 1990).In the absence of zooxanthellae (e.g., in cases of coral bleaching and the loss of algalsymbionts due to stress, Hoegh-Guldberg, 1999), translocation of photosyntheticcarbon can also take place between algae living in the coral skeleton (endoltihicalgae), and the coral host (Fine and Loya, 2002; Schlichter and Kerisch, 1995). Thus,endolithic organisms (e.g., bacteria, fungi and algae) living within the coral skeletonmay also be potential nutrient sources (Fine and Loya, 2002; Le Campion-Alsumardet al., 1995; Kushmaro and Kramarsky-Winter, 2004). Ferrer and Szmant (1998)estimated that 55–60% of the nitrogen required by the coral can be satisfied by thesesources. Recent work indicates that these symbiotic and mutualistic relationships areeven more varied, complex and dynamic than previously thought (Fine and Loya,2002; Furnas, 2003).
p0420 Reef sponges (Wilkinson and Fay, 1979) and some corals may acquire fixednitrogen from associated diazotrophic cyanobacteria (Frias-Lopez et al., 2002;Lesser et al., 2004; Rohwer et al., 2001, 2002; Shashar et al., 1994a,b, see Chapter4, Capone and Carpenter, this volume). The nutritional significance of these alter-native pathways remains to be fully evaluated.
s0090 2.6. Microbial populations
p0430 Recent research has shown the diversity and potential significance of microbialcommunities living in and on coral reefs (Kushmaro and Kramarsky-Winter,2004; Rohwer et al., 2002) with an implicit role in nitrogen uptake, packagingand regeneration Bacterial productivity within cavities in the reef framework ishigher than that in open water surrounding the reef (Scheffers et al., 2005) (seeChapter 8, Bronk and Steinberg, this volume), and the ecological role of bacterialiving in coral mucus and skeletons is just now being elucidated. Cyanobacteria have
also been detected in the mucus layer of corals (Ritchie and Smith, 2004; Rohweret al., 2001) and specialized bacteria may also protect the coral animal from oppor-tunistic pathogens by having antibacterial or toxic properties. However, the role ofthe microbial populations of the coral surface mucopolysaccharide layer (SML) interms of nitrogen dynamics has not yet been fully studied. One might hypothesizepossible roles involving N immobilization, regeneration, nitrification and nitrogenfixation, amongst others.
p0440 Microbial populations in reef ecosystems may serve directly as nutrient sourcesfor higher organisms. They are known to have a low C:N ratio in general and theuse of the SML bacterial community in particular as a food source has beendemonstrated (Ritchie and Smith, 2004; Sorokin, 1973). With respect to nutrientacquisition, microbes are effective in sequestering nutrients due to their high affinitytransport systems and large surface to volume ratios. In nutrient poor waters,prokaryotes scavenge nutrients at much lower concentrations than eukaryotes, andassimilate most of the limiting nutrients thereby restricting primary productivity(Kirchman, 2000; Rohwer and Kelly, 2004). Coral associated microbes mayalso be in direct competition with their host for water column nutrients (Rohweret al., 2002). Given ability of prokaryotes for nutrient uptake, corals may usemicrobes to ‘‘fish’’ for nutrients i.e. cultivation gardening for certain beneficialmicrobes by excreting organic matter in the form of mucus (Ducklow, 1990;Saffo, 1992).
p0450 Microbes may in some cases also act as pathogens causing harm to corals. Recentwork has shown that reefs that are more eutrophied, often have denser stands ofmacro- and micro-algae (see below). The algae produces carbon substrates, which inturn then enhance the proliferation of bacteria on live coral surfaces which can causethe corals to die, enabling more substrate for algal growth (Smith et al., 2006).
s0100 2.7. Ammonification and regeneration
p0460 Given the high gross productivity of reefs, the majority of this production must besupported by the retention and internal recycling of nitrogen (Szmant-Froelich,1983 Fig. 21.3). The pathway of ammonium production from organic matter isoften referred to as ammonification (Fig. 21.1B). Ammonium is released throughgrazing processes in which fish, echinoderms, zooplankton, filter feeders (includingsponges) as well as detritivores (such as worms), and bacteria recycle organicnitrogen and excrete it (D’Elia and Wiebe, 1990; D’Elia, 1988; Szmant-Froelich,1983). Coral reef fish have excretory products very high in nitrogen (N:P ¼ 48),with ammonium as the most important source of DIN and excretory products thatare enriched in P (N:P ¼ 8). Coral growth is higher in the presence of reef fish,particularly resting fish such as grunts, which forage and then return to the reef torest in large aggregations (Meyer and Schultz, 1985).
p0470 Regeneration of organic nitrogen may occur in various components of the reefincluding within the diverse symbiotic associations (see Section 2.1). In addition tothe surrounding sediments (DiSalvo, 1969; Entsch et al., 1983; Rasheed et al.,2002), structures on the reef proper may be important sources of regeneration ofnutrients, including ‘‘porewater’’ within the coral skeletons themselves (Risk and
Muller, 1983) that have important ‘‘biocatalytic’’ function in terms of regenerationof organic matter and release of nutrients to the coral reef (Rasheed et al., 2002).Up to 70% of reef volume can be attributed to the myriad of nooks and cranniesthat trap sediments, fecal pellet and decaying organic matter (Ginsburg, 1983;Szmant-Froelich, 1983; Szmant, 2002). Regenerated inorganic species can then
Low ambient dissolved organic nitrogen water upstream of reef becoming high dissolved organic water downstream
Nitrogen cycling within reef interstitial waters which exchange with surface waters
Limestone/soft calcium carbonate sediment
Nitrogen fixation by sediment bacteria and cyanobacteria in algal turfs
Leaching of dissolved organic nitrogen
Filter feeding sponges absorb microplankton and nutrients
Invertebrates and herbivorous fish grazing
Predatory fish
Excretion (dissolved nitrogen) and fecal production (particulate nitrogen)
Cnidarian with symbiotic zooxanthellae capturing zooplankton and dissolved organic and inorganic nitrogen and excreting mucus
DON
DON DON
DON
N
N
N2
DNPN
DNPN
PN PN
DONDIN
DON
DONDONDONDIN
PN
DON
f0030 Figure 21.3 Generalized nutrient pathways and means of trophic cycling and regeneration onreefs (adapted from Szmant-Froelich, 1983); showing the importance of nitrogen cycling andregenerationwithin the interstices of the coral structure and fromgrazers.
percolate through the porous structures. Elevated nutrients have indeed beenmeasured in reef cavities and interstices (DiSalvo, 1971; Andrews and Muller,1983; Szmant-Froehlich, 1983, 2002), which can be introduced to the reefthrough ‘‘burps’’ (Szmant-Froelich, 1983) of nutrient-enriched water throughholes and fissures that provide reef organisms with pulses of nutrients(Fig. 21.3). Cavities within the reef structure are areas of high bacterial activityand hence nutrient regeneration (Scheffers et al., 2004, 2005). In a study inCuracao, open water bacterial productivity was limited by both N and P, whereasreef crevice bacteria were only limited by P (Scheffers et al., 2005). N limitationappears to be circumvented in these interstices through remineralization processeswhich can, in turn, increase inorganic N concentrations in the overlying reefwaters through exchange with the ambient water (Scheffers et al., 2005).
p0480 Rasheed et al. (2002) determined that nutrient concentrations in these regenera-tive spaces within the reef framework were 1–3 times higher than surrounding watercolumn values, corresponding to fluxes of 14.5 mmol m�2 day�1 for ammonium;7.7 mmol m�2 day�1 for nitrate and 0.9 mmol m�2 day�1 for nitrite. Nutrientswithin the sediments were 15–80 times higher than the water column values, cor-responding to a diffusive flux of 0.06 mmol m�2 day�1 for ammonium;0.03 mmol m�2 day�1; for nitrate and 0.01 mmol m�2 day�1 for nitrite; under-scoring the importance of these sites in trapping organic matter and regeneratingnutrients (Rasheed et al., 2002).
p0490 Recycling of nutrients between coral hosts and symbiotic dinoflagellates (zoox-anthellae) is a key reef process (see Section II above). Zooxanthellae take up theammonium excreted by the coral animal, therefore this waste N is not released to thewider system (Muscatine and D’Elia, 1978; Wilkerson and Trench, 1986). Recy-cling of N by the coral host could satisfy all the nitrogen needs of the symbiotic algae(Crossland and Barnes, 1974, 1977).
p0500 Transfer of ammonium and other nitrogenous waste may aid in the process ofcoral calcification. Enhanced calcification was noted in experiments when ammo-nium and urea were added to corals (Crossland and Barnes, 1974). The authorssuggested that excretory ammonia may combine with protons released whenbicarbonate is converted to carbonate. Their model suggested that at the site ofcalcification, the hydrolysis of urea formed by the breakdown of allantoins yieldsCO2 and NH3. The CO2 could provide a carbonate source for calcificationand the NH3 would then neutralize and remove protons from the calcifyingmilieu. However, Taylor (1983a,b) re-analyzing their study suggested it wasmore reasonable to attribute the enhancement of calcification by ammoniumand urea to the stimulation of symbiont photosynthesis. Kinsey and Davies(1979) showed a decrease in coral calcification with the addition of nitrogen andphosphorus, but suggested this was more probably attributable to P effects ratherthan N (see Elevated Nutrients on Coral Reefs Experiment (ENCORE) casestudy below).
p0510 Much of the regenerated nitrogen on the reef ultimately is derived from nitrogenintroduced to the system through grazing. Grazer interactions also help recyclenutrients with fish and invertebrates grazing benthic microalgae. Benthic microalgaecan act as a nutrient trap for regenerated nutrients including N, and have been
shown to increase with increasing levels of ammonium (Uthicke, 2001; Uthicke andKlumpp, 1997). Benthic microalgae have been observed to increase in the presenceof holothurian grazers (Uthicke, 2001), due to ammonium release. This constitutesan important component of a benthic retention mechanism akin to the pelagicmicrobial loop (Uthicke, 2001).
p0520 Recently there has been a growing awareness of the importance of coral mucusto the overall productivity and retention of nutrients in the reef system (Wild et al.,2004a). Up to 50% of the carbon assimilated by zooxanthellae may be exuded asmucus, which protects the coral colony against fouling, dessication and sedimenta-tion. A previously unrecognized aspect of mucus within these systems is that itefficiently traps organic particulate matter from the water column, including bacteriaknown to fix both N and C; thereby increasing the nutritional quality in coralassociated communities. In a study in Australia, Wild et al. (2004a) found that coralmucus could increase both its N and C content up to 3 orders of magnitude in 2 h.Bacteria are much better than corals at assimilating nutrients at low concentrations(Knowlton and Rower, 2003) and coral associated bacteria may scavenge limitingnutrients, including iron and vitamins, which are then harvested by the coralsthemselves. This is supported by the observation that some corals eat their ownmucus (Coles and Strathmann, 1973). These enriched mucus-particle aggregatessubsequently provided 10–20% of the total organic carbon supply to the sediments,maintaining nutrients for heterotrophs and remineralization processes within thecoral reef system (Wild et al., 2004a). Coral mucus and organic flux from massspawning events back to the benthos from the overlying water column may affectsediment biogeochemistry in reef environments by enhancing the organic contentof sediments and affecting microbial processes and nutrient processing (Wild et al.,2004a,b,c; 2005, 2008).
s0110 3. Nitrogen Perturbations to Reefs
p0530 The rapid decline in coral reefs over the last few decades clearly has resultedfrom multiple stressors from various sources including exposure to excess nitrogenwhich can have direct effects on corals and their symbionts (Stambler et al., 1991;Dubinsky and Stambler, 1996; Furnas, 2003; Mora, 2008) (Fig. 21.2). Nutrients canhave direct physiological effects on corals by reducing growth or reproduction rates.Nutrients can affect corals indirectly by: increasing susceptibility to bleaching anddisease; affecting the coral-zooxanthellae symbiosis (Bruno et al., 2003); or by causingphase shifts in community structure (Knowlton, 2001; Szmant, 2002). Food webs incoral reef systems can become highly altered with the removal of predators providing‘‘top-down’’ control and increases in nutrients providing ‘‘bottom up’’ control.(Hughes et al., 1999, 2007; Lapointe, 1997, 1999, 2004a,b; Szmant, 2002). Withincreased nutrients, coral reefs change from symbiosis-dominated systems with tightrecycling of nutrients to regions with a higher proportion of macroalgae; withsubsequent succession to heterotrophic filter feeders (Fabricius, 2005).
p0540 Coral reefs are not stable, static communities living in benign environments, butrather are very dynamic ecosystems which are subject to frequent natural physicaldisturbance on times scales which vary from minutes to years (Furnas, 2003; Furnas
et al., 2005). Despite their inherent resilience, coral reefs are nonetheless threatenedworld wide, with an estimated 140,000 km2 lost in the last few decades and more thanhalf of the world’s coral reefs listed at high or medium risk with more than 80% of thereefs in SE Asia under medium to high threat from activities such as over-developmentand over-exploitation (Brown, 1987; Bryant et al., 1998; Dubinsky and Stambler,1996; Hoegh-Guldberg, 1999, Hughes et al., 2003). The resilience of the systembecomes weaker with more accumulated impacts (McClanahan et al., 2002).
p0550 Impacts of overfishing, global climate change and the increase in coral disease(including coral-bleaching) (Bellwood et al., 2006; Hoegh-Guldberg, 1999; Hugheset al., 1999, 2003, 2007; Jackson et al., 2001; Pandolfi et al., 2003; Smith andBuddenmeier, 1992; Wilkinson and Buddemeier, 1994; Mora, 2008) are emergentareas of interest in coral reef research. There has been much debate in the literatureover which factors (e.g., nutrients, loss of grazers, terrestrial runoff and sedimenta-tion; climate change etc.) are the most deleterious. These factors may have synergis-tic or antagonistic effects, which may vary in differing regions and reefs (e.g.,Aronson et al., 2003; Boesch et al., 2001; Fabricius, 2005; Hughes et al., 1999,2003; Jackson et al., 2001; Lapointe, 1997, 1999, 2004a,b; Pandolfi et al., 2003;Szmant, 2001, 2002). These problems may be further exacerbated by increasingurbanization and other changing land usages which can subsequently result inamplified runoff of nutrients, fertilizers contaminants and increased sediment loading(Furnas, 2003; Hutchins et al., 2005) resulting in general coastal eutrophication (Bell,1992; Costa et al., 2000; Fabricius, 2005; Furnas and Brodie, 1996; Koop et al.,2001).
p0560 Threats to reefs can be either acute or chronic (Edinger et al., 1998). Acute beingdefined as ‘‘dramatic damage in a short period of time,’’ which includes: destructivefishing practices; anchor damage; ship groundings; cyclones or hurricanes; or diseaseor predation (e.g., Acanthaster outbreaks) (Brodie et al., 2005). Chronic threats alterthe physical or biological environment on a long term basis, and cause long termdamage to coral reefs. Nutrient inputs including sewage; increased sedimentation(particulate nutrients), resulting in nearshore eutrophication (Tomascik et al., 1993)can manifest themselves in both modes. Chronic stresses may be more detrimentalto the long term health of coral reef ecosystem than acute stresses (Kuntz et al.,2005). Combinations of stressors are associated with threshold responses, as well as‘‘ecological surprises’’ which can include disease and pathogen breakouts (Brodieet al., 2005; Bruno et al., 2003; Knowlton, 2001).
p0570 Whether reefs will have the resilience to recover from multiple anthropogenicstresses (Hughes and Connell, 1999) is a major issue of concern to scientists andresource managers. Recent studies have highlighted the serious decline in waterquality in coastal environments, including coral reef areas (Fabricius, 2005; Hutchinset al., 2005; Kuntz et al., 2005; Wilkinson, 2002; Barile, 2004).
s0120 3.1. Inorganic N increases
s0130 3.1.1. Effects on coral colonies and life cycle
p0580 Elevated nutrients (ammonium, nitrate and phosphate) may derive from multiplesources (see above) and can directly affect both adult coral colonies as well asreproduction and recruitment of larvae in a number of ways (Fabricius, 2005).
Nutrient induced perturbations include changes in: biochemical composition of thecorals (Marubini and Atkinson, 1996; Stambler et al., 1991); skeletal growth (bothpositive and negative) (Ferrier-Pages et al., 2000); calcification (Marubini andAtkinson, 1999); reproductive potential (Tomascik, 1991), and density of algalsymbionts (Dubinsky and Stambler, 1996) (Fig. 21.2). When corals are in lownutrient environment, zooxanthellae produce photosynthate in excess of theircapacity to take up nutrients. This excess organic carbon is then available to thehost for growth, calcification and reproduction (Fig. 21.2. left panel). Under highnutrient conditions the zooxanthellae preferentially keep the organic carbon fortheir own growth, increasing symbiont number, but decreasing the transfer to thecoral host, which decreases the coral’s calicifiation and reproduction (Furnas, 2003).The long term ecological implications of these often subtle changes in symbiont andhost interaction and translocation of organic matter and energy away from coralgrowth and reproduction, have not been fully elucidated (Furnas, 2003). Directeffects of DIN on both corals reproduction and coral adults has recently beensummarized by Fabricius et al. (2005, and references therein).
s0140 3.1.2. Algal increases and grazer decreases
p0590 One manifestation of excess nutrients, and specifically N, on reefs is algal over-growth (Barile, 2004; Lapointe, 1997; McCook, 1999, 2001; Reaka-Kudla et al.,1997; Scheffers et al., 2005; Szmant 2002). Excess nitrogen may also enable, or actsynergistically, with other stressors to increase and expedite, the spread of diseasewithin coral communities (Rosenberg and Loya, 2004, refs therein; Kuntz et al.,2005). The determination of factors that lead to algal overgrowth on reefs has beenan important, and at times controversial issue, as to whether increased nutrients(including N), or loss of grazers has given rise to the problem. In a special issue onthe topic, Szmant (2001) summarizes the problem: ‘‘It is clear from the studies in thisissue that several factors are conspiring to change the dynamics of coral reef algal communitiesfrom those we observed (but did not study very well) in the early and middle decades of the pastcentury, to those present now. These factors appear to differ in degree among localities.’’
p0600 In the same special issue, McCook et al. (2001) provide an extensive review ofcoral—algal interactions which may be characterized as positive, neutral or negative.Positive effects include symbiotic algal-coral interactions; neutral interactionsinclude situations where grazing and algal growth are balanced and negative effectsof algae on corals which include both direct or indirect influences. Direct negativeaffects often involve competition or the direct overgrowth and/or invasion of coralby algae. An example of this is the algae Coralliophila hurysmansii which causes tissueswelling on the coral. Indirect affects include interactions such as those with thealgae Antrichium tenue which has a mucus layer that traps sediments (and possiblymicrobes); increasing microbial processes which help turn the algal-coral relation-ship from a neutral relationship to a negative one, thereby taking on the character-istics of disease, with increased nutrients as the trigger (Willis et al., 2004). Someother indirect affects include reduction in physical space, for coral growth andrecruitment of coral larvae due to algal coverage and allelopathic activity (Kuffnerand Paul, 2004; McCook et al., 2001). Recent research suggests that overgrowth ofalgae can cause mortality of corals from enhanced microbial activity on coral
surfaces. This may in turn be a result of algal exudates, which then allows more freesurface area for algal growth (Smith et al., 2006). Other evidence indicates that algalexudates can also suppress fecundity, recruitment and survival (Hughes et al., 2007).
p0610 Nutrient stimulation of algal growth may often only be visible in the absence ofgrazers (Hughes, 1994; Furnas, 2003). Concomitant with nutrient increase, reefs areexperiencing a major reduction in grazers that help keep the system in balance.(Hughes, 1994; Jackson et al., 2001; Pandolfi et al., 2003). In some instances this maypromote a phase shift from corals to macroalgae, and a resultant loss of resilience inrecovery to other perturbations such as storms and climate change and diseases(Bellwood et al., 2004). For instance, Caribbean reef decline was preceded by adwindling of fish stocks, along with simultaneous increases in nutrients and sedimentrunoff from the land (Hughes, 1994; Jackson et al., 2001). Similarly, on the GBR,inputs of sediment and nutrients have increased by four times that of pre-Europeansettlement (McCulloch et al., 2003;Williams, 2002) and macro grazer populations ofsea-turtles and dugong have decreased dramatically along with larger predator fishpopulations (Bellwood et al., 2004). Additionally, some effects of nutrients anddisease may be exacerbated by sea surface warming which can also lead to coralbleaching. What effect this will have on long term coral reef health is presentlyunknown (Buddemeier and Fauntin, 1993; Koop et al., 2001; Smith andBuddenmeier, 1992; Szmant, 2002).
s0150 3.1.3. Effects of runoff and sedimentation
p0620 Although coral reef environments are generally characterized as low nutrient envir-onments, there are some areas in which intermittent sources of nutrients are addedby seasonal runoff reaching reef environments ( Furnas, 2003; Gabric and Bell, 1993;Kinsey, 1991; Marsh, 1977). In the GBR region for instance, coastal river inputs ofsediments and nutrients has increased fourfold over the last�150 years (Brodie et al.,2003) and the dissolved nitrogen fraction of this runoff is widely dispersed in theGBR system (Devlin and Brodie, 2005). Land development including increases inimpervious surfaces as well as processes that lead to increased erosion such asagricultural grazing can increase runoff of sediments during rain events such asobserved on Molokai, a high relief, heavily ranched portion of Hawaii that is anarea of local concern and study currently (Chaston, 2006).
p0630 Terrestrial runoff is a major concern for areas with coral reefs. Nutrient enrich-ment, sedimentation, and turbidity can all degrade reefs at local scales (Fabricius,2005). While there are some coastal coral reefs that can flourish in relatively highnutrient and high levels of particulate matter, they tend to be restricted in depth to�10 m; whereas in clearer offshore reefal systems they may extend to >40 m(Fabricius, 2005). Some corals can use the particulate matter for nutrition. However,there is a fine line, between increased nutrient availability for the coral for ingestionand the tipping point at which the corals are unable to cope with sedimentation andsilting affects. (Anthony, 2000; Anthony and Fabricius, 2000; Fabricius and Wolanski,2000; Mills and Sebens, 2004; Mills et al., 2004).
p0640 Other anthropogenic, terrestrial sources of nitrogen to reefs include groundwater(D’Elia et al., 1981; Littler et al., 2006), and sewage (Hanson and Gundersen, 1976;Lapointe et al., 2005a,b; Risk and Erdmann, 2000; Szmant Froelich, 2002). Since
1960, the use of nitrogen fertilizer globally on an annual basis has increased by afactor of six (Fabricius, 2005; Matson et al., 1997). Fertilizer loss off the land is amajor source of anthropogenic nutrients to coral reefs in many regions (Mitchellet al., 2005). In some areas, roosting seabirds can be a major episodic contributor ofguano and nitrogen input (Albert et al., 2005; Furnas et al., 2005; Smith and Johnson,1995). Some of the effects of terrestrial runoff including sediment and nutrientenrichment on coral reefs have recently been summarized by Fabricius (2005).
p0650 Gradients of reef health, community structure, biodiversity, and ecological functionin near-shore coral reef systems are often associated with environmental gradientsinfluenced by terrestrial runoff (Fabricius, 2005; Fabricius and De’ath, 2004,Fabricius et al., 2005). However, the exact cause of runoff related effects are controver-sial (e.g., nutrients vs. sediments vs. toxicants vs. fresh-water input) (Szmant, 2002).
p0660 Although coral growth itself may be positive in polluted reefs, increased nutrientscan cause net reef erosion. Therefore the paradoxical combination of normal coralgrowth and net reef erosion need to both be taken into consideration for any wholereef perspective approach to coral reef health (Edinger et al., 2000).
p0670 In terms of nitrogen inputs, the effects of terrestrial run-off to marine systems maybe better understood in a biogeochemical context and the gradients in microbialprocessing of nutrients (Alongi andMcKinnon, 2005). For instance, denitrification inthe coastal zone may help reduce the amount of N that is transported to the offshorereefs (Seitzinger, 1988) and coastal habitats such asmangrove and intertidal zonesmayprovide significant protection buffers for offshore coral reefs by trapping, transform-ing and storing sediments and organic matter. While intact coastlines may be able tomitigate some of the runoff effects, these vital areas are under increasing developmentpressure worldwide with large scale clearing of mangrove and coastal vegetation aswell as the steady increase in impervious surfaces. These synergistic effects maytherefore increase the effective load of nutrients reaching coral reef environments(Furnas et al., 2005).
s0160 3.1.4. Sewage
p0680 Sewage pollution remains a concern in many coral reef regions, particularly indeveloping nations, and is widely considered as one of the major causes of thedemise of coral reef health (Smith et al., 1981; Brown and Howard, 1985; Edingeret al., 1998, Furnas et al., 2005; Ginsburg and Glynn, 1994; Hatcher and Frith, 1985;Johannes, 1975; Wilkinson, 1993). It is not only a concern from an environmentalhealth perspective but for human health as well (Colwell, 2004).
p0690 Documented effects of sewage impacts on reefs include: increased particulate andsediment load resulting in smothering of corals, lower photosynthetic rate by corals,increased bioerosion, hypoxia, algal overgrowth (see above) as well as changes incommunity structure and shifts towards filter-feeding heterotrophic organisms (Riskand Erdmann, 2000). In Indonesia, Edinger et al. (1998) found that reefs subjected toland based pollution (sewage, sedimentation and or industrial pollution) had areduction in diversity of 30–50% at 3 m and a 40–60% reduction of diversity at10 m, relative to unpolluted reefs.
p0700 Wastewater nutrients and animal wastes are generally enriched in 15N, the heavystable isotope of nitrogen (Sammarco et al., 1999; Heikoop et al., 2000).
15N-signatures have been used as a tracer of fertilizer input to corals reefs in Bali(Marion et al., 2005). New methods of tracking sewage plumes through using 15
N/14N or d15N-signatures in bioindicator organisms such as stomatopods, macro-algae, mangroves, and corals (Heikoop et al., 2001; Risk and Erdmann, 2000; Riskand Heikoop, 1997; Mendes et al., 1997) have recently been implemented in somereef areas thereby providing a measure of integrated water quality over longer timescales rather than the snapshot of water quality obtained with chemical measure-ments of nutrients (Costanzo et al., 2001, 2005; Hoegh-Guldberg et al., 2004;Muscatine et al., 2005; Udy et al., 2005). For instance, coral tissue d15N from Poriteslobata was significantly higher in sewage affected reefs than reference sites in 70% ofimpacted reef sites in Indonesia (Heikoop et al., 2001). Excess nitrogen can lead toincreased zooxanthellae density and ultimately decreases in translocation of carbonand nitrogen to the coral host as the coral loses control of the symbiotic relationship,with the symbionts increasing in number and holding onto their photosynthate fortheir own growth (Fig. 21.2) (Heikoop et al., 2001); this suggests that sewagederived nitrogen can disrupt normal coral-zooxanthellae physiology.
p0710 One very clear cut case where nutrient input, and in particular nitrogen, has hada serious and demonstrable deleterious effect on coral reefs is Kaneohe Bay, Hawaii(Smith et al., 1981; Hanson and Gundersen, 1976; Szmant, 2002). A sewage outfallcaused a major overgrowth of the green ‘‘bubble’’ algae Valoniawhich overgrew thecorals which then died. The sewage outfall was moved and some improvement inthe system was seen. However the fragile balance had been disrupted, and thesediments contained a long memory of nutrients. Subsequently non-point sourcesbecame a problem at Kaneohe Bay as well and it is still not back to its originalcondition, partly due to organic matter accumulation, which is being observed inmany reef systems (D’Elia and Wiebe, 1990; Furnas, 2003) as inputs of nutrients,particularly N, are exceeding losses. This impaired system was further damaged, dueto loss of herbivores, and the introduction of the invasive algae Dictyoshpaeriacavernosa (Stimson et al., 2001).
p0720 Increased nitrogen can also increase phytoplankton in the water column as wellas macroalgal abundance, particularly in areas where over-fishing has occurred(Hughes et al., 2003; McCook, 2001; McCook et al., 2001; Szmant, 2002). Theincrease in BBD also appears to be increasing in prevalence which may also beassociated with elevated nutrients input and or sewage outflows (Antonius, 1988;Bruckner et al., 1997; Taylor, 1983a,b). Kuta and Richardson (2002) found apositive relationship between elevated nitrite and BBD incidence, but no positivecorrelation with nitrate, ammonium, or phosphate. BBD is, however, routinelyobserved on pristine reefs far from acute nutrient perturbations. Therefore, the exactrelationship between BBD and water quality remains elusive.
s0170 3.2. Sea surface warming, coral disease and N dynamics
p0730 Global climate change is a major threat to coral reefs (Phinney et al., 2006 andreferences therein), with reefs already exhibiting climate warming effects in termsof coral bleaching due to zooxanthellae expulsion (Brown, 1997; Hughes et al.,2003). Thermal sensitivity of reef-building corals may prove to be the ‘‘Achilles
heel’’ in terms of reef ecosystem resilience (Graham et al., 2006). Climate changemay further exacerbate population phase shifts in degraded reefs with bleachingcoral mortality providing more space for macroalgae, and filamentous cyanobac-teria and less space for coral recruitment to help recovery on over-fished and/oreutrophied reefs (Hughes et al., 2007; Kuffner and Paul, 2004).
p0740 What direct effects climate change will have on various aspects of nitrogencycling on reefs including coral bleaching events and zooxanthellae expulsion,remains to be seen. The subsequent consequences for N conservation and Nacquisition of the corals and other symbioses, on the reef will undoubtedly beaffected as the balance between symbionts and host interaction is very sensitive toenvironmental conditions (Knowlton, 2001).
p0750 Rising average sea surface temperatures resulting from global climate change mayincrease the amount of nitrogen fixed globally (Karl et al., 2002) and in reefenvironments specifically (Paul et al., 2005) due to both increased physiologicalrates of nitrogen fixation as well as increasing cyanobacterial populations (Paerl andHusiman, 2008). Recent research has also demonstrated an increased rate of nitro-gen fixation on coral skeletons that have been subjected to bleaching events, whichmay increase the availability of nitrogen in these systems for an extended periodbeyond the initial bleaching event. The scales events are predicted to become moreprevalent, this may increase suitable substrate for diazotrophy as a result of climatechange (Davey et al., 2008). Similarly, increases in macroalgal populations (Lapointeet al., 2005a,b; McCook et al., 2001) may also increase the surface area available forboth diazotrophic heterotrophic bacteria and cyanobacteria.
p0760 Warming conditions could also lead to the increase in the prevalence of harmfulcyanobacterial assemblages such as the toxin producing genus Lyngbya (e.g., Albertet al., 2005; Paul et al., 2005), as well as species that have been linked with BBD incorals including Phormidium and others (e.g., Oscillatoria submembranaceae; Beggiatoa;Desulfovibrio; Phormidium corallyticum) (Rosenberg and Loya, 2004 and referencestherein). The prevalence of BBD in the Caribbean increases during the warmestmonths of the year when temperatures are above 30� (Richardson, 2004).
s0180 4. Elevated Nutrients on Coral Reefs Experiment
(ENCORE)
p0770 A replicated in situ fertilization experiment was conducted on the GBR at OneTree Reef Lagoon, Australia during 1993–1996 (Larkum and Koop, 1997). Thisexperiment (ENCORE) was specifically designed to address nutrient effects in situbased on previous smaller scale fertilization studies in micro-atolls in One TreeIsland lagoon (Kinsey and Davies, 1979; Kinsey and Domm, 1974). Laboratoryresults, and small scale mesocosm experiments had to that point indicated thatnutrients additions could perturb the natural physiology of corals and some otherinvertebrate reef organisms (Belda et al., 1993; Ferrier-Pages et al., 1998; Hoegh-Guldberg and Smith, 1989; Jokiel et al., 1994; Muller-Parker et al., 1994; Muscatineet al., 1989), but evidence directly from the field and simultaneous assessment of
different reef organisms and processes were largely lacking (Hoegh-Guldberg,2004a,b; Koop et al., 2001).
p0780 While increasing nutrient loads were perceived as deleterious, what the preciseresponses that different reef organisms would have was unknown. Therefore, part ofthe aim of the ENCORE study was to identify organisms or community responsefactors which could be used as indicators of ecosystem degradation (Steven andLarkum, 1993). Twelve micro-atolls, or patch reefs were fertilized with N (ammo-nium chloride), P (sodium phosphate) and Nþ P over the course of 3 years. Dosingwith nutrients occurred to the internal ‘‘lagoons’’ of each micro-atoll during the�4–5 h of each low tide when they were physically isolated from the larger lagoon.During the first � year of the experiment the atolls were dosed at N levels that wereapproximately 2 times ambient (average �0.7–11 mM). During the second year thedosage was increased to approximately 6 times ambient (�0.7–36 mM) (Steven andAtkinson, 2003).
p0790 The results of these experiments are summarized in Fig. 21.4. Overall theparameters that were most responsive to nutrient enrichment were coral fertiliza-tion, benthic microbial processes, stomatopod recruitment and symbiont numbers(Koop et al., 2001). In terms of direct effects to nitrogen cycling, nitrogen fixationincreased in P fertilized plots and decreased in the N treatments, whereas denitrifi-cation increased in the N and N þ P treatments and macroalgae showed rapiduptake of N (Koop et al., 2001; O’Neil and Capone, 1996). Other effects that wereseen in the þN treatments included reduced fecundity, fertilization and settlementin corals as well as reduced lipid content in the corals (Harrison and Ward, 2001;Koop et al., 2001; Ward and Harrison, 2000). Increased number of zooxanthellae incorals and the giant clam Tridacna were also observed; as well as increased N:P andreduced NH4
þ uptake capacity in the giant clams. In the þP treatments; coralreproduction was affected with reduced settlement of larvae and smaller eggs, as wellas increased mortality in adult corals. Corals also had increased linear extension, butwere more fragile. Some species of coral had more zooxanthellae and increased lipidcontent. Tridacna had decreased N:P. Macroalgae showed reduced alkaline phos-phatase activity. In the þNþP treatments, there was a mixed result, with coralreproduction again affected in terms of reduced fecundity, and settlement as well asincreased mortality. Corals had increased linear extension but were more fragile;zooxthanthellae numbers stayed the same, but corals showed a reduction in lipids.There was rapid uptake by macroalgae of both N and P and reduced alkalinephosphatase activity. There was reduced stomatopod recruitment. Tridacna had nochange in N:P but increased zooxanethellae (Fig. 21.4).
p0800 What was not observed, however, was a massive overgrowth of algae. Over-growth of algae in response to nutrients may in fact only be detectable in the absenceof grazers in over-fished areas (McCook et al., 2001). As a protected research areawithin the Great Barrier Marine Park, One Tree Island has an abundant fishpopulation; therefore underscoring the probable importance of top-down controlwith a healthy grazing fish population for the health and resilience of a system undernutrient stress (Hughes et al., 2007). The increased þN and P inputs increaseddenitrification in the sediments, while P inputs increased sedimentary nitrogenfixation. Increased denitrification with P enrichment may have been due to
concomitant increases in N2-fixation providing substrates for denitrification(Fig. 21.4). This suggests a very dynamic feed-back capacity of the reef systemwhich allows it to respond to changes in nutrients (Capone, 1996a). While thepotential for denitrification on reefs has been demonstrated (Johnstone et al., 1990;O’Neil and Capone, 1996), the information on its quantitative significance is poorlyconstrained (Capone, 1996a). Part of the missing picture in the ENCORE study wasthat changes in the sedimentary benthic microalgal (BMA) community, and nutrient
ENCORE results
Windmixing
Increasing sensitivity
Unresponsive to elevated nutrients
Fertilization
Settlement
Coralreproduction
Intense grazing
Responsive
Calcification >Bioerosion
Fecundity
Coral polyp
Brown coral
Red macroalgae
Giant clam
Stomatopod
Green macroalgae
Soft coral
Epilithic algal community
Rhodolith
N2
Sand
Den
itrifi
catio
n
N F
ixat
ion
NH4+
PO4−3
+NH4+PO4
−3+PO4−3
Org N
P addition N+P additionN addition
Hig
her
deni
trifi
catio
n
N2
Reducedfecundity
+NH+4
Rapid uptake
More zoox
anthellae
increase
d N:P
Reduced N
H 4 uptake
capacit
y
More zooxanthellae (in some spp.)Stunted
Reducedlipids
Org N
N F
ixat
ion
Reduced fertilization
Reducedsettlement
CoralReproduction
Reduced fertilization
Settlementaffected
CoralReproduction
N2
More smalleggs
Increase
d
mortality
Reduced
phosphatase
Same zoox
anthellae
decrease
d N=P
More tissue
Increasedlinear
extension
More fragile
More zooxanthellae (in some spp.)
Increased lipids
Org N
Den
itrifi
catio
n
Hig
her
N F
ixat
ion
Hig
her
deni
trifi
catio
n
N2
Reducedfecundity
Increase
d
morta
lity
More zoox
anthellae
no N:P
change
Same zooxanthellae
Reducedlipids
Org N
N F
ixat
ion
Increasedlinear
extension
More fragile
Reduced
recruitm
entRapid uptake
reduced phosp
hatase
Reduced fertilization
Reducedsettlement
CoralReproduction
f0040 Figure 21.4 Summary of the major effects of elevated nitrogen on coral reef processes from theENCOREproject, showing a gradation in responsiveness to nutrient additions; aswell as the indi-vidual effects ofþN;þPaswell as combined effects ofþNþP.
uptake by this important component of the benthic community were not fullyquantified (Koop et al., 2001).
p0810 d15N isotope signatures in two species of corals from þN treatments providedevidence that 50–100% of the overall nitrogen budget of enriched corals could comefrom ammonium suggesting that dissolved nutrients can have a significant effect onnitrogen uptake and dominated both the d15N signature of both the symbiont andthe host. It also suggested that the nutrient history of the reef may be recordedwithin the organic components of the symbiotic dinoflagellates, as well as the coralsand the skeletal associates which may therefore possibly be used as indicators of thechronology of nutrient concentrations surrounding a coral during its lifetime(Hoegh-Guldberg, 2004a,b; Marion et al., 2005).
s0190 5. Conclusion
p0820 The nitrogen cycle is key to high productivity and healthy ecosystem func-tioning on coral reefs. By trying to unravel the complex interaction and specific rolesof each component of the reef ecosystem and coral holobiont with regard to theuptake, exchange and transformation of nitrogen, insight may be gained into ‘‘howcorals have come to dominate tropical near-shore systems and how they may be ableto adapt to changing environmental conditions’’ (Rohwer and Kelley, 2004).
p0830 As threats to coral reefs world wide have grown, the urgency to better under-stand the basic natural functioning in these systems has also grown, to be better ableto assess these impacts on reefs. All aspects of nutrient cycling are undergoing changewith increases in anthropogenic nutrification, and multiple perturbations includingincreased sedimentation, runoff and levels of pollutants. Therefore it is important tocontinue to gain more insight into nitrogen cycling in coral reefs ecosystems as theability of coral reefs to ‘‘adapt to these perturbations in the past is no guarantee ofresilience in the future’’ (Hughes, 1994). We must, as Bellwood et al. (2004) suggest,confront our global coral reef crisis worldwide and reassess our current managementpractices (Hughes et al., 2003; Phinney et al., 2006 and references therein).
ac0100ACKNOWLEDGEMENTS
p0840 The authors thank the GBRMPA and ENCORE project participants fortopical discussion. The UMCES Integration and Application Network (IAN) staffmembers W.C. Dennison; T. Carruthers, J. Thomas and Diana Kliene (MarineBotany University of Queensland) for help with graphics. DGC thanks NSF OceanSciences for sustained support.
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