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Dissolved Organic Matter in Coral Reefs: Distribution, Production, and Bacterial Consumption

  • Yasuaki Tanaka
  • Ryota Nakajima
Chapter
Part of the Coral Reefs of the World book series (CORW, volume 13)

Abstract

Dissolved organic matter (DOM) constitutes the largest organic matter pool in coral reef waters and is released and utilized by various coral reef organisms. In this chapter, we review the distribution and fluctuation of DOM concentrations in coral reefs around the world, with a special focus on Shiraho Reef, Ishigaki Island, Okinawa, Japan, where DOM fluxes have been studied most intensively since the late 1990s. Then, we review the DOM production rates from specific reef organisms and DOM consumption rates by bacteria. Previous studies have shown that both dissolved organic carbon and nitrogen (DOC and DON, respectively) generally have a higher concentration in most coral reefs than in the surrounding ocean. At Shiraho Reef, the average ratio of the net DOC production to the net primary production on the reef flat was 18%, and the C:N ratio of DOM that was produced on the reef flat was estimated to be 9.3. The abundance of heterotrophic bacteria was also higher in most coral reefs than offshore, which indicates that bacterial growth was enhanced by reef-derived DOM. Some of the DOC that was produced in coral reefs was persistent to bacterial decomposition in the long term, which suggests that coral reef ecosystems export some reef-derived DOM to the ambient ocean, irrespective of the water residence time in the reef.

Keywords

DOM C:N ratio Biogeochemical cycles Nutrients Coral Benthic algae Phytoplankton Primary production Decomposition Refractory organic matter 

2.1 Introduction

Dissolved organic matter (DOM) in the oceans is one of the largest pools of organic matter on the Earth’s surface (Hedges 1992). The amount of carbon (C) in oceanic DOM is estimated to be 700 Gt (Ogawa and Tanoue 2003), which is equivalent to that of atmospheric carbon dioxide (CO2). Although most oceanic DOM is refractory organic matter with a turnover time of 1000–6000 years (Williams and Druffel 1987; Bauer et al. 1992), fresh DOM is continuously produced from various biological and chemical processes (Carlson 2002; Mostofa et al. 2013). In particular, photic zones have a higher DOM concentration in the vertical profile (Ogawa et al. 1999; Carlson 2002), which indicates that primary producers such as phytoplankton are generally major DOM producers in marine ecosystems (Meyers-Schulte and Hedges 1986; Opsahl and Benner 1997).

Marine DOM is usually defined as the organic matter that passes through glass fiber filters (Whatman GF/F, a nominal pore size 0.7 μm), which are the most widely used for filtration (Ogawa and Tanoue 2003). The organic matter that is collected on these filters is referred to as particulate organic matter (POM). The definitions of DOM and POM are based on its practical size; therefore, DOM does not exactly mean the chemically dissolved phases of organic matter. For example, 22–38% of marine bacteria are not retained on GF/F filters and are counted as DOM (Lee et al. 1995). POM includes a complex mixture of living and nonliving organic matter with a broad size range (Volkman and Tanoue 2002). For example, phytoplankton, zooplankton, large detritus, and some bacteria are included in POM (Blanchot et al. 1989).

In general oceanic surface waters, the concentration of dissolved organic carbon (DOC) ranges from 50 to 100 μmol L−1 (μM) (Carlson 2002; Ogawa and Tanoue 2003), which is one order of magnitude higher than that of particulate organic carbon (POC). Approximately 40 μM of DOC consists of refractory compounds, which are ubiquitously distributed in the global oceans and turn over on time scales of centuries to millennia (Williams and Druffel 1987; Bauer et al. 1992), so the remaining 10–60 μM is considered to be a relatively degradable fraction. This degradable fraction can be further categorized into labile and semi-labile fractions, which turn over on time scales of minutes to days and months to years, respectively (Carlson 2002). Labile and semi-labile DOM can be utilized by heterotrophic bacteria (hereafter bacteria), and the energy is transferred to higher trophic levels, such as heterotrophic protists, through microbial food web s (Pomeroy 1974; Azam et al. 1983; Sherr and Sherr 1987). The energy transfer through microbial food webs is a particularly important process in understanding material recycling in aquatic ecosystems (Cho and Azam 1988; Fuhrman et al. 1989; Pavés and González 2008; Dinsdale and Rohwer 2011).

Coral reef ecosystems develop in shallow sea areas of tropical and subtropical climate zones. The surface oceanic seawater in tropical and subtropical zones is generally deficient in nutrients , and this oligotrophic seawater continuously flows in and out of coral reefs. Thus, the growth of phytoplankton in coral reef waters is usually limited by the availability of nutrients (Furnas et al. 2005; Rochelle-Newall et al. 2008). On the other hand, the primary production rates per unit surface area of coral reefs (e.g., 190–640 mmol C m−2 day−1; Atkinson 2011) have been reported to be the highest among marine ecosystems (Duarte and Cebrián 1996), although most of the primary production of coral reefs is consumed by respiration in the ecosystem (Crossland et al. 1991; Gattuso et al. 1996, 1998; Atkinson and Falter 2003). This high rate of gross primary production in coral reefs is largely attributed to benthic primary producers, the biomass of which is usually much higher than that of the planktonic primary producers in shallow coral reefs (Atkinson and Falter 2003; Atkinson 2011). Therefore, fluctuations in seawater parameters such as DOM are strongly related to benthic biological activities. For example, reef-building corals (Tanaka et al. 2009; Nakajima et al. 2010; Levas et al. 2015) and benthic algae (Haas et al. 2010a, b; Mueller et al. 2014) release DOM into the ambient seawater; conversely, sponges absorb DOM from seawater (Yahel et al. 2003; de Goeij et al. 2008, 2013; Rix et al. 2016). The produced DOM is consumed by bacteria in the reef water and sediment (Ferrier-Pagès et al. 2000; Wild et al. 2004a, b; Tanaka et al. 2011a; Nakajima et al. 2015). Because of the oligotrophic environments of most coral reefs, dissolved organic nitrogen (DON) can be an essential nitrogen (N) source for microorganisms (Seitzinger and Sanders 1999). The fluxes of DOC and DON reflect these benthic and planktonic processes and thus can be used as an important parameter to understand biogeochemical cycles in coral reefs (Wild et al. 2004a; Mari et al. 2007; Miyajima et al. 2007a; Tanaka et al. 2011a, b).

Measuring precise DOC and DON concentrations in seawater had been a challenging task for a long time and has been improved since the late 1990s (Sharp et al. 2002a, b, 2004). However, determining accurate DOC and DON concentrations is still difficult; therefore, detecting small changes in their concentrations is particularly difficult in oligotrophic seawaters, such as those near coral reefs. Among the three major geographical structures of coral reefs (fringing reefs, barrier reefs, and atolls), fringing reefs develop along shorelines and often have a shallow backreef zone called a reef flat (Iryu et al. 1995; Kennedy and Woodroffe 2002). Because the DOM concentration fluctuates to a relatively large extent on a shallow reef flat, fringing reefs are considered to be most suitable for detecting changes in DOM concentrations and studying their fluxes in the reef ecosystem (Hata et al. 2002; Miyajima et al. 2007a; Tanaka et al. 2011a, b; Wyatt et al. 2012; Thibodeau et al. 2013). Other seawater parameters such as dissolved inorganic carbon (DIC) have also been studied to evaluate their fluxes in fringing coral reefs (Kayanne et al. 1995, 2005 Gattuso et al. 1996; Wyatt et al. 2010, 2013; Watanabe et al. 2013).

2.1.1 Shiraho Reef

Fringing reefs are commonly seen in the Ryukyu Islands, which are located in the southwestern part of Japan (Iryu et al. 1995). Shiraho Reef, Ishigaki Island, Okinawa, Japan, is a typical fringing reef in which the biogeochemical cycles of DOM have been intensively studied (Hata et al. 2002; Miyajima et al. 2007a; Tanaka et al. 2011a, b). This reef has a well-developed reef flat that extends several hundred meters offshore from the shoreline (Fig. 2.1). On the reef flat of Shiraho Reef, seagrass beds extend from the shoreline to 200–400 m offshore. Many reef-building coral communities are found from approximately 500 to 800 m, and the dominant coral species are Acropora spp., Porites spp., and Montipora spp. (Nakamura and Nakamori 2009). The gap zone between seagrass and corals is mainly covered with bare carbonate sands. The depth of the Shiraho reef flat is approximately 1–3 m and becomes shallower on the reef crest, which forms almost parallel to the shoreline (Fig. 2.1). The reef crest emerges above the sea surface during low tide and thus separates the seawater on the reef flat from the offshore oceanic water. During this low-tide period, the reef flat becomes a semi-closed system, although some seawater is exchanged with the offshore region through channels on the reef crest. Measuring the changes in seawater parameters on the reef flat during this low-tide period can provide information on the biological activities of benthic and planktonic organisms in the coral reef.
Fig. 2.1

Aerial photo of Shiraho Reef (Obtained from Tanaka et al. 2011b, with permission from ©Springer). The symbols indicate the sampling sites in Tanaka et al. (2011b). CR1, CR2, S1, and S2: coral-dominated areas. SG1 and SG2: seagrass-dominated areas. B: offshore site

Land-derived groundwater with high nitrate (NO3) concentrations is continuously discharging into the reef flat at Shiraho Reef (Kawahata et al. 2000; Umezawa et al. 2002a, b). Although most of the seawater on the reef flat contains low NO3 concentrations (<1 μM) (Miyajima et al. 2007a, b; Tanaka et al. 2011a, b), the effect of groundwater NO3 appeared to accumulate in benthic algae several hundred meters offshore from the shoreline, and the amount of NO3 that was discharged from the backland depended on the land use (Umezawa et al. 2002a, b). Many other fringing reefs around the world are also susceptible to adjacent terrestrial ecosystems through groundwater seepage or river discharge (Lapointe et al. 2010; Tedetti et al. 2011).

This chapter reviews DOM studies in coral reefs around the world and provides the present understanding of biogeochemical cycles of DOM. First, the distribution and fluctuation of DOM concentrations in coral reefs are reviewed, with a special focus on Shiraho Reef. Then, DOC production rates from individual organisms, especially corals and benthic algae, are compared among reef organisms to obtain a general range of DOC production rates. Finally, the abundance and growth rate of bacteria in coral reef waters are reviewed to estimate the general DOM consumption rate by pelagic bacteria.

2.2 Distribution and Fluctuation of DOM

2.2.1 DOM Distribution

The DOM concentrations at Shiraho Reef have been measured since the late 1990s, with the observed concentrations constantly ranging between 49 and 87 μM and between 3.8 and 8.0 μM for DOC and DON , respectively (Hata et al. 2002; Miyajima et al. 2007a; Tanaka et al. 2011a, b) (Table 2.1). These observations suggest that the production and consumption processes of DOM on this coral reef have not changed drastically over the past 10 years. Compared to other coral reefs, Paopao Bay (French Polynesia), Noumea (New Caledonia), and La Saline (Reunion) exhibited similar DOC concentrations on the reef flat or in the lagoon (Table 2.1). On the other hand, much higher DOC concentrations have been observed at Tuamotu Atolls (French Polynesia), Great Astrolabe Reef (Fiji), and Curaçao (Netherlands Antilles) (Table 2.1). DON concentrations were measured at Tuamotu Atolls and Ningaloo Reef (Western Australia), which were higher than those at Shiraho Reef (Table 2.1). There are some possibilities to explain the difference in the DOC and DON concentrations among these study sites: (1) the local environmental conditions (e.g., groundwater seepage, artificial wastewater, and nutrient discharge) could affect organic matter and nutrient concentrations around the reef (Kawahata et al. 2000; Umezawa et al. 2002a, b; Lapointe et al. 2010; Tedetti et al. 2011); (2) the oceanic DOM concentrations outside the reef might affect the baseline concentration in the reef water because the oceanic seawater continuously circulates in and out of the reef (Tanaka et al. 2011b; Watanabe et al. 2013); and (3) the analytical accuracy of the DOC and DON concentrations in the seawater samples might differ between laboratories (Sharp et al. 2002a, b, 2004).
Table 2.1

Summary of the DOC and DON concentrations in coral reefs

Site

References

Specific sampling site

DOC (μM)

DON (μM)

Japan

Shiraho Reef, Ishigaki Island

Hata et al. (2002)

Reef flat

60–87

Offshore

68

Miyajima et al. (2007a)

Reef flat

53–76

4.0–7.7

Offshore

49–64

4.0–8.0

Tanaka et al. (2011a)

Reef flat

66–75

4.8–5.7

Offshore

57–58

3.8

Tanaka et al. (2011b)

Reef flat

57–77

3.8–5.7

Offshore

57

4.0

Fukido Reef, Ishigaki Island

Thibodeau et al. (2013)

Reef flat

4.5–5.5

Offshore

3.6–4.5

Bora Bay, Miyako Island

Suzuki et al. (2000)

Reef flat

64–129

5.6–11

Offshore

69–83

5.4–6.2

Sesoko, Okinawa Island

Tanaka et al. (2011c)

Reef flat

62

4.0

Pacific Ocean

Tuamotu Atolls, French Polynesiaa

Torréton et al. (1997)

Lagoon

105

Offshore

87

 

Pagès et al. (1997)

Lagoon

62–159

Offshore

82–86

Torréton et al. (2000)

Lagoon

3.9–15.3

Offshore

5.5

Bouvy et al. (2012)

Lagoon

73–100

Offshore

80–83

Paopao Bay, French Polynesia

Nelson et al. (2011)

Reef flat

63–73

Offshore

75–85

Northern Line Islandsa

Dinsdale et al. (2008)

Lagoon

29–69

 

Great Astrolabe Reef, Fiji

Torréton et al. (1997)

Lagoon

114

 

Offshore

102

 

Noumea, New Caledonia

Mari et al. (2007)

Lagoon

62–74

Offshore

63

Rochelle-Newall et al. (2008)

Lagoon

55–99

Indian Ocean

Ningaloo Reef, Western Australia

Wyatt et al. (2012)

Reef flat

8–13

Offshore

9–11

La Saline, Reunion

Tedetti et al. (2011)

Reef flat

63–74

Offshore

75

Atlantic Ocean

Curaçao, Netherlands Antilles

van Duyl and Gast (2001)

Reef flat

125–200

Offshore

125–225

The concentrations are separated between the interior of the reef and the offshore seawater. The interior seawater is described as either a reef flat (fringing reef) or lagoon (atoll). Some values were visually interpreted from figures

aDetails from the Tuamotu Atolls and Northern Line Islands are shown in Table 2.4. Some additional data are also found in Table 2.4

The DOC and DON concentrations on the Shiraho reef flat were always higher than those in the offshore waters. Most of the other coral reefs around the world also exhibited higher DOM concentrations on the reef flat or in the lagoon than offshore (Table 2.1). These results indicate that most of the coral reefs that have been studied so far are functioning as a net source of DOM to the ambient open ocean. Contrarily, the DOC concentration at Paopao Bay was lower on the reef flat than offshore (Nelson et al. 2011), which indicates that the reef flat was a net sink of DOC. Whether a coral reef acts as a net sink or source of DOM could be influenced by the baseline concentration of DOM (oceanic DOM outside the reef) and the composition of the organisms in the coral reef (Haas et al. 2016). The baseline concentration of DOM indicates the degradability of DOM in the seawater: higher concentrations of DOM indicate that the seawater has more degradable DOM. When this degradable fraction of oceanic DOM is decomposed faster than the DOM production rate in the reef, the coral reef appears to be a net sink of DOM, as is the case for Paopao Bay (Nelson et al. 2011). When oceanic DOM is mainly composed of refractory organic matter and the decomposition rate is slower than the DOM production rate in the reef, the reef ecosystem appears to be a net source of DOM, as is the case for most other reefs. The DOM production rate depends on the composition of the reef organisms, as shown below.

2.2.2 DOM Fluctuation

The diel fluctuation of DOC and DON concentrations in coral reefs has only been observed at Shiraho Reef (Hata et al. 2002; Tanaka et al. 2011b). These studies showed that the concentrations of DOM decreased to the lowest level, which was close to oceanic DOM concentrations, during flood-tide periods (Fig. 2.2). This fluctuation in the DOM concentrations suggests that DOM was not produced in the water column but primarily from benthic communities because the contribution of benthic organisms to the bulk DOM concentration in seawater changes with the water depth (Fig. 2.3). This result was not unexpected because the benthic biomass in shallow coral reefs is generally much higher than that in the water column (Atkinson 2011). For example, if we suppose that the concentration of POC in the water column on the Shiraho reef flat is 5–10 μM (Hata et al. 2002; Miyajima et al. 2007a; Tanaka et al. 2011a, b), the POC per unit surface area corresponds to 10–20 mmol m−2 when the water depth on the reef flat is assumed to be 2 m. POC consists of both C in microbes, such as phytoplankton, and C in detritus, so the contribution of planktonic organisms to the bulk POC must be smaller than the estimate (Nakajima et al. 2011). On the other hand, corals, which are a representative benthic organism, have a C biomass of approximately 100–400 μmol cm−2 per unit coral skeletal surface area (Muller-Parker et al. 1994; Tanaka et al. 2007, 2009). By simply extending this C biomass to the horizontal squared area, the coral C biomass is calculated to be 1000–4000 mmol m−2. This estimate is conservative because corals and other benthic organisms form three-dimensional structures on the sea bottom. The benthic biomass would be at least two orders of magnitude higher than the C biomass of planktonic organisms on the Shiraho reef flat.
Fig. 2.2

Diel variations in the DOC and DON concentrations on the reef flat of Shiraho Reef (Obtained and modified from Tanaka et al. 2011b, with permission from ©Springer). DOC: filled circles, DON: open triangles. The range of oceanic DOM concentrations is shown with gray shadows

Fig. 2.3

Diagram of the DOM fluxes at Shiraho Reef. The C:N ratios of DOM were derived from Tanaka et al. (2011a, b)

Another possible source of DOM from the benthic environment may be groundwater seepage from the adjacent land, which is often reported at fringing reefs worldwide (Kawahata et al. 2000; Umezawa et al. 2002a, b; Lapointe et al. 2010; Tedetti et al. 2011; Cawley et al. 2012). However, if groundwater seepage and/or river water discharge are considerably responsible for DOM fluctuations, a negative correlation between the DOM concentration and salinity should be detected on the reef flat. Such a correlation was not observed at Shiraho Reef (Tanaka et al. 2011b), which indicates that the DOM fluctuation was caused by autochthonous sources.

The observation that the DOM concentrations at Shiraho Reef returned to the offshore oceanic level during high-tide periods indicates that the seawater on the reef flat is almost completely replaced with oceanic waters every day (Tanaka et al. 2011b). In this type of coral reef with a short water residence time, much of DOM that is produced on the reef flat could be exported offshore before this material is decomposed by bacteria (Fig. 2.3). This process actually depends on the water residence time and the degradability of organic matter (Mari et al. 2007). More DOM is exported offshore when the water residence time is shorter and the DOM is less degradable. DOM degradability is discussed later in Subsect. 4.3.

2.3 Production Processes of DOM

2.3.1 Corals

DOM is released from various organisms and communities in coral reefs. Scleractinian corals have been frequently studied as DOM producers or sometimes as consumers (Crossland 1987; Ferrier-Pagès et al. 1998; Brown and Bythel 2005; Grover et al. 2006, 2008; Tanaka et al. 2009; Nakajima et al. 2010; Naumann et al. 2010; Levas et al. 2015). These organisms continuously release or absorb DOM from the ambient seawater and sometimes release a copious amount of visible mucoid organic matter called coral mucus under stressful conditions such as air exposure (Wild et al. 2004a, b). Several reasons have been proposed to explain the release of DOM and mucus from corals, including excretory pathways for excess organic matter (Davies 1984), defense against sedimentation (Riegl and Branch 1995), and defense against pathogens (Cooney et al. 2002). These functions of coral mucus were reviewed by Brown and Bythel (2005). The production or consumption rate of DOM by corals is usually expressed as a rate that is normalized to the unit area of the coral skeletal surface. The net production rate of DOC showed a very wide range from −22 to 23 mmol m−2 h−1 (Table 2.2; Fig. 2.4), and the median value was 0.20 mmol m−2 h−1. This large range of DOC production rates could be caused by various factors, e.g., coral species, the environmental conditions around the coral, and experimental techniques.
Table 2.2

Major DOM producers and their production rates per unit surface area of the producers in coral reefs

Group

Species

DOC release rate (mmol m−2 h−1)

References

Corals

Acropora millepora

0.31

Levas et al. (2015)

Acropora muricata (A. formosa)

1.25

Nakajima et al. (2010)

Acropora pulchra

0.16

Tanaka et al. (2008a)

Acropora pulchra

0.37

Tanaka et al. (2009)

Acropora robusta (A. nobilis)

2.21

Nakajima et al. (2009)

Acropora sp.

2.56

Naumann et al. (2010)

Euphyllia sp.

−9.91 to 0.83 (−3.30)

Wild et al. (2012)

Fungia sp.

−1.18

Naumann et al. (2010)

Goniastrea sp.

1.83

Naumann et al. (2010)

Madracis mirabilis

−0.87

Mueller et al. (2014)

Manicina sp.

−13.03

Haas et al. (2010a)

Millepora sp.

0.77

Naumann et al. (2010)

Montipora digitata

0.09

Tanaka et al. (2010)

Montipora digitata

6.74–22.98 (14.68)

Wild et al. (2012)

Orbicella annularis

0.15

Mueller et al. (2014)

Pocillopora damicornis

0.06

Haas et al. (2013)

Pocillopora sp.

−21.93

Naumann et al. (2010)

Porites cylindrica

0.14

Tanaka et al. (2008a)

Porites lobata

0.20

Haas et al. (2011)

Porites lobata

4.06

Levas et al. (2013)

Porites sp.

3.17

Haas et al. (2010a)

Stylophora sp.

−1.17

Naumann et al. (2010)

Turbinaria reniformis

0.25

Levas et al. (2015)

Macroalgae

Avrainvillea sp.

−0.50

Haas et al. (2010a)

(Chlorophyta)

Caulerpa sp.

0.56–1.11 (0.83)

Haas et al. (2010b)

Enteromorpha

0.14

Haas et al. (2010b)

Halimeda opuntia

0.20

Haas et al. (2011)

Halimeda sp.

−0.07

Haas et al. (2010a)

Penicillus sp.

0.25

Haas et al. (2010a)

Rhipocephalus sp.

1.01

Haas et al. (2010a)

Ulva sp.

0.28

Haas et al. (2010b)

(Phaeophyta)

Dictyota ceylanica

0.30

Haas et al. (2013)

Hydroclathrus sp.

0.40

Haas et al. (2010b)

Lobophora sp.

0.85

Haas et al. (2010a)

Lobophora sp.

0.40

Haas et al. (2010b)

Sargassum

0.47

Haas et al. (2010b)

Turbinaria ornata

0.50

Haas et al. (2011)

(Rhodophyta)

Amansia rhodantha

0.80

Haas et al. (2011)

Hydrolithon reinboldii

0.45

Haas et al. (2011)

Hydrolithon reinboldii

0.10

Haas et al. (2013)

Liagora sp.

0.40

Haas et al. (2010b)

Lithophyllum congestum

5.35

Mueller et al. (2014)

Peyssonnelia sp.

0.24–2.96 (1.0)

Haas et al. (2010b)

Red algae

1.03

Haas et al. (2010a)

Turf algae

Turf algae

0.52–5.53 (2.56)

Haas et al. (2010b)

Turf algae

2.80

Wild et al. (2010)

Turf algae

1.4

Haas et al. (2011)

Turf algae

0.18

Haas et al. (2013)

Cyanobacteria

Oscillatoria bonnemaisonii

1.36

Brocke et al. (2015)

Seagrass

Syringodium sp.

2.49

Haas et al. (2010a)

Thalassia sp.

0.18

Haas et al. (2010a)

The values in parentheses are the means of several data in the study

Fig. 2.4

DOC release rates from benthic organisms in coral reefs. The data in Table 2.2 are ranked in descending order. Four data points (14.68, −3.31, −13.03, and −21.93 mmol m−2 h−1; see Table 2.2) that lay outside the y-axis range are not shown in the figure

When a DOM production rate is measured for corals, these organisms are usually incubated in a closed system for a period by using glass or plastic bottles, and changes in the DOM concentrations are measured. Many conditions differ among these types of cultural experiments, including the type and intensity of provided light, the seawater temperature, and the stirring conditions of the seawater. For example, higher light intensity could increase the photosynthetic rates of endosymbiotic algae (genus Symbiodinium) in the coral, which increases the release rates of DOC from the coral colony (Crossland 1987; Naumann et al. 2010). Higher nutrient concentrations in seawater might reduce DOM release rates because the production of endosymbiont cells is promoted with nutrients and less organic matter is available for release (Dubinsky and Berman-Frank 2001; Naumann et al. 2010; Tanaka et al. 2010). Moreover, the concentration of DOM that is available for corals in the initial culture media might affect the net DOM production rates from the corals because these organisms are known to both release and absorb DOM (Grover et al. 2006, 2008; Levas et al. 2013, 2015). The information of these experimental conditions is not available for all studies, so statistically analyzing what factor is most influential to DOM production rates is difficult.

Although absolute release rates of DOM have been reported in many studies as shown in Table 2.2, the relative release rates of DOM to other coral metabolic rates, such as photosynthesis, have scarcely been measured. A few studies showed that 5.4–14% of the net photosynthesis of coral endosymbiotic algae was released as DOC from the corals Galaxea fascicularis (Ferrier-Pagès et al. 1998), Acropora pulchra (Tanaka et al. 2009), and Porites lobata (Haas et al. 2011). The contribution of POC to the TOC that is released from corals was reported to be <40% (Nakajima et al. 2009, 2010), so the ratio of the released TOC to the net photosynthetic rate would be roughly 5–20%. Estimating this type of relative flux would be useful and essential to establish a general concept of coral metabolism and to narrow the extremely wide range of DOM production rates that have been reported.

2.3.2 Benthic Algae

Although the number of research articles is still limited, benthic algae have recently been receiving attention as DOM producers in coral reefs (Wild et al. 2010; Haas et al. 2010a, b, 2011, 2013, 2016; Mueller et al. 2014). The net production rates of DOC from macroalgae and turf algae (benthic microalgae) range from −0.50 to 5.5 mmol m−2 h−1, and the median value is 0.45 mmol m−2 h−1 (Table 2.2, Fig. 2.4). Haas et al. (2010b) compared the DOC release rates among nine benthic algal species and showed that turf algae (various consortia of the green alga Cladophora, red alga Gelidium, and associated cyanobacteria assemblages) had the highest DOC release rates (Table 2.2). The release rate was basically activated with elevated temperature and light intensity but inhibited under the highest conditions (28 °C or 500 μmol m−2 s−1).

The DOC production rates from turf algae and macroalgae (Amansia rhodantha and Turbinaria ornata) were higher than those from the coral Porites lobata (Haas et al. 2011). The ratio of released DOC to the net photosynthetic rate was also higher for benthic algae than the coral: the macroalgae (A. rhodantha and T. ornate) and turf algae released approximately 20–40% as DOC, while the coral P. lobata released 11% (Haas et al. 2011). The ratios of the released DOC to the net photosynthesis of macroalgae in coral reefs were comparable to the ratios for macroalgae in other aquatic ecosystems: for example, the brown alga Ecklonia cava, which was collected at Oura Bay (temperate climate zone in Japan), released 18–62% of its net photosynthesis as DOC (Wada et al. 2007). The brown alga Laminaria hyperborea, which was collected along the coast of Norway, also released 26% of its net algal production as DOC (Abdullah and Fredriksen 2004). These studies showed a significant contribution of macroalgae to the production and cycling of DOM in aquatic ecosystems, when the macroalgae are one of the dominant benthic communities.

The cover of benthic algae in coral reefs is highly variable and is affected by the environmental conditions. Basically, elevated nutrient concentrations and lower herbivory tend to increase the cover of benthic algae, allowing them to outcompete corals and crustose coralline algae (Smith et al. 1981, 2001, 2005, 2016; Lapointe 1997; Burkepile and Hay 2009; Littler et al. 2010). Macroalgae did not seem to be a dominant benthic community at Shiraho Reef (Nakamura and Nakamori 2009), but turf algae (microphytobenthos) comprised 14–27% of the whole benthic primary production (Suzumura et al. 2002). The cover of macro- and microalgae seemed to be equivalent to what was observed at Kingman Atoll in the Northern Line Islands (20%, Sandin et al. 2008) but seemed to be much lower than what was observed at Tabuaeran and Kiritimati Atolls in the Northern Line Islands (50–70%, Sandin et al. 2008). DOM production rates were not measured in these studies, but the benthic algal communities might considerably contribute to DOM production in the reef (Haas et al. 2011, 2013, 2016).

2.3.3 Phytoplankton

Phytoplankton is a major producer of DOM in general open and coastal oceans (Carlson 2002). Coral reefs, particularly fringing coral reefs, often have a relatively shallow water depth , so the contribution of phytoplankton to the primary production or DOM production is considered to be much lower than that of benthic primary producers. The deeper the coral reef is, the greater the contribution of phytoplankton. Charpy-Roubaud et al. (1988) measured the planktonic and benthic primary production rates in Tikehau Atoll (Tuamotu Archipelago, French Polynesia) by using 14C and O2 budget methods, respectively, and concluded that the benthic primary production was higher in the area with a depth of 0–10 m, with both production rates being equal at a depth of 10–15 m.

DOM production by phytoplankton has not been measured often in coral reefs. The production rate of DOC by phytoplankton in the lagoon of New Caledonia was approximately 0.005–1.8 mmol m−3 h−1 under the area’s light conditions, including eutrophicated coastal bay stations, and the percentage extracellular release (PER, the percentage of released DOC to the total primary production) varied between 5% and 74% with an average of 35% (Rochelle-Newall et al. 2008). Excluding the coastal bay stations, the DOC production rates of phytoplankton were 0.005–0.4 mmol m−3 h−1 with a median value of 0.06 mmol m−3 h−1 (Rochelle-Newall et al. 2008). Strictly comparing this DOC production rate with those of corals and benthic algae from different studies is difficult (Table 2.2) because the rates by these benthos are based on the per unit surface area of the organism and do not consider the reef-scale area (i.e., three-dimensional structure of a sea floor). Nonetheless, if we suppose that a reef flat has a depth of 1 m, the DOC production rate of phytoplankton would be 0.06 mmol m−2 h−1 according to the median rate in Rochelle-Newall et al. (2008). This DOC production rate constitutes 30% of the median DOC production rate of corals (0.20 mmol m−2 h−1; Table 2.2) and 13% of benthic algae (0.45 mmol m−2 h−1; Table 2.2). Phytoplankton at a depth of 25 m in the water column in Takapoto Atoll, French Polynesia, was estimated to produce DOC at 55 mmol m−2 day−1 (Sakka et al. 2002), which is higher than the DOC production rates of benthic organisms from the unit bottom area.

2.3.4 Production of DOM at Shiraho Reef

The net DOC production rates (NPDOC) normalized to the unit horizontal area were reported to be 12–36 mmol m−2 day−1 at Shiraho Reef (Hata et al. 2002; Miyajima et al. 2007a; Tanaka et al. 2011b; Table 2.3). The DOC production rates at reef scales have never been estimated for other coral reefs around the world but have been measured for subtropical and temperate seagrass-dominated communities, such as 4–25 mmol m−2 day−1 (Ziegler and Benner 1999), 81 mmol m−2 day−1 (Barrón et al. 2004), and 2–35 mmol m−2 day−1 (Barrón and Duarte 2009). These production rates fall within a similar range of DOC production rates that were observed on the reef flat of Shiraho Reef. Considering that NPDOC exceeded the gross primary production rate in the seagrass community (Barrón et al. 2004), a part of the DOM could be released from detritus accumulated in the seagrass community (Smith et al. 1992, Miyajima et al. 1998). When the NPDOC at Shiraho Reef is normalized to a unit water volume, the production rate (12–36 mmol m−3 day−1) can be compared to general planktonic ecosystems. For example, NPDOC was 0.3 mmol m−3 day−1 at the surface of the subtropical North Pacific Ocean (Karl et al. 1998) and 0.1–0.7 mmol m−3 day−1 at a coastal upwelling region of Spain (Marañón et al. 2004). This comparison shows a much higher production rate of DOC on the reef flat, although the total production in the open ocean would become higher when the entire photic zone is considered.
Table 2.3

Net primary production (NPP) rates and net DOC production (NPDOC) rates at Shiraho Reef

NPP (mmol m−2 day−1)

NPDOC (mmol m−2 day−1)

Season

References

Community scales

Microphytobenthos

6.9–24

Mar, Sep

Suzumura et al. (2002)

0.8

Jul, Aug

Nakamura and Nakamori (2009)

Seagrass

40

Jul, Aug

Nakamura and Nakamori (2009)

Corals

200

Jul, Aug

Nakamura and Nakamori (2009)

Reef scales

110

Mar

Kayanne et al. (1995)

130

Sep

Suzuki et al. (1995)

36 ± 12

30–36

Sep

Hata et al. (2002)

96–131

Dec, Mar, Sep

Kayanne et al. (2005)

15 ± 57

Dec, Mar, Jun, Sep

Miyajima et al. (2007a)

11

Jul, Aug

Nakamura and Nakamori (2009)

335–359

12–24

Aug, Sep

Tanaka et al. (2011b)

Average of reef-scale studies

125

22

  

Some values were visually interpreted from figures

A comparison between the NPDOC and net primary production (NPP) rates shows that the NPP at Shiraho Reef was highly variable compared to NPDOC (Table 2.3). The lowest range of NPP was 11–36 mmol m−2 day−1 (Hata et al. 2002; Nakamura and Nakamori 2009), which was equivalent to the NPDOC value at the same site. Nakamura and Nakamori (2009) estimated the NPP from a survey on a line transect across the reef flat and described that a large portion of the transect line (64%) was covered by bare carbonate sands, which might have led to the low NPP. Hata et al. (2002) conducted a survey in the summer of 1998, when extensive coral bleaching occurred, so primary production by the coral communities might have not contributed considerably to the entire NPP. These large variations in NPP, which depended on the season, year, and survey area, caused the ratio of NPDOC to NPP to vary greatly from <10% to almost 100% (Table 2.3). By simply averaging the previously obtained data, the NPDOC and NPP at Shiraho Reef were 22 mmol m−2 day−1 and 125 mmol m−2 day−1, respectively, and the ratio of NPDOC to NPP was calculated to be 18%. This estimate shows that a considerable amount of DOM is produced on the reef flat and is most likely lost from the reef flat to offshore through drifting seawater.

The DOC and DON fluctuation patterns at Shiraho Reef were consistent (Fig. 2.2), which indicates that the DOM that is produced on the reef flat has a similar chemical composition irrespective of the diel cycle. The relationship between the observed DOC and DON concentrations around the coral reef must be plotted to estimate the C:N ratio of the reef-derived DOM. According to the slope of this relationship, the C:N ratio of the DOM that is produced at Shiraho Reef was estimated to be 9.3 from the surveys in 2008 and 2009 (Fig. 2.5). This C:N ratio for the DOM was slightly higher than that of POM (4.6–7.3; Tanaka et al. 2011a, b) from the same sites at Shiraho Reef. The C:N ratio of bulk DOM on the reef flat (13–15) was slightly lower than that of oceanic DOM (14–15) (Tanaka et al. 2011a, b; Fig. 2.3), which indicates that most of the DOM on the reef flat was derived from the surrounding ocean. Because the bulk DOM on the reef flat was a mixture of oceanic DOM and reef-derived DOM, the properties of the bulk DOM might differ between locations on the reef flat. Similar C:N ratios were also observed at the lagoon of New Caledonia: the C:N ratio of the DOM in the lagoon (12–14) was slightly lower than that of oceanic DOM (15; Mari et al. 2007). These observations indicate that relatively N-rich DOM is produced in coral reefs compared to the ambient open ocean.
Fig. 2.5

DOC and DON concentrations at Shiraho Reef, which were measured during the surveys in the summer of 2008 (squares) and 2009 (circles). The original data were found in Tanaka et al. (2011a, b). A model II regression was fitted to the plot data: y = 9.3x + 22 (r2 = 0.96, p < 0.01)

2.3.5 What Is the Major DOM Producer at Shiraho Reef?

Specifying the major DOM sources in ecosystems is one of the most important and challenging themes in coral reef biogeochemistry. In this subsection, the major DOM sources are estimated for Shiraho Reef as an example study site. Recall that the DOM would mainly be derived from benthic environments, considering the fluctuations in DOM concentrations with the tidal cycle (Fig. 2.2). Because the production rate of DOM was higher at daytime than nighttime (Tanaka et al. 2011b), the production of DOM would be related to photosynthetic activities. The possible DOM producers are mainly corals, seagrass, and benthic macro- or microalgae. Actually, the contribution of these three communities to the total primary production on the reef flat was almost 100% (Nakamura and Nakamori 2009).

Here, we stress that the DOM concentrations were significantly higher at inshore seagrass-dominated sites (SG1 and SG2 in Fig. 2.1) than at offshore coral-dominated sites (CR1 and CR2 in Fig. 2.1) (Tanaka et al. 2011a, b), which suggests that the seagrass-dominated site contributed more to the DOM production on the reef flat. However, the C:N ratio of DOM that was produced on the reef flat was approximately 9.3 (Fig. 2.5), which implies that seagrass and macroalgae are not the major DOM producers because their cells generally have much higher C:N ratios (15–23; Atkinson and Smith 1983; Duarte 1992; Fourqurean et al. 1992). Thus, the remaining possible sources of DOM might be benthic microalgae (turf algae), including cyanobacterial mats, which tend to have similar C:N ratios in their cells to those of the observed DOM, e.g., 7.0 for Cladophora sp. (turf algae) and 7.9–9.4 for cyanobacteria (Atkinson and Smith 1983). Benthic cyanobacterial mats were reported to release DOC more than turf algae and contributed to 79% of the total DOC production at the fringing reef of Curaçao (Brocke et al. 2015). At Shiraho Reef, benthic cyanobacteria are extensively observed around the seagrass-dominated zone because of relatively high nutrient concentrations (Blanco et al. 2008) and thus might be a major DOM source on the reef flat alongside other turf algae.

2.4 Bacterial Consumption of DOM

The DOM and POM that are produced in coral reefs are mainly removed from the reef by two processes: (1) physical exportation from the reef to the surrounding ocean by water currents (Mari et al. 2007; Wyatt et al. 2010, 2013) and (2) biological decomposition and mineralization in the coral reef (Wild et al. 2010; Haas et al. 2011; Morrow 2011; Tanaka et al. 2011a; Nelson et al. 2013). The former largely depends on the water residence time and hydrodynamics in the reef (Mari et al. 2007; Wyatt et al. 2012). The latter process is mainly driven by heterotrophic bacteria, which rapidly recycle and transfer organic energy to other reef organisms via a microbial loop (Wild et al. 2004a; Naumann et al. 2012; Nakajima et al. 2015). In this section, we focus on the bacterial consumption of DOM in coral reef waters.

2.4.1 Distribution of Bacterial Abundance

Bacteria are the most abundant organisms on coral reefs (Rohwer et al. 2002). The abundance of bacteria over coral reefs drastically varies but generally ranges from 2 to 15 × 105 cells mL−1, except for some extreme values (Table 2.4). The lowest value (0.7 × 105 cells mL−1) was reported in Kingman Atoll, Northern Line Islands, which exhibited no local anthropogenic or terrestrial influence (Dinsdale et al. 2008). In contrast, the highest values, which exceed more than 15 × 105 cells mL−1, have often been reported in the lagoons of Tuamotu Atolls, French Polynesia (Torréton and Dufour 1996a, b; Torréton et al. 1997; González et al. 1998; Ferrier-Pagès and Furla 2001; Sakka et al. 2002). The median and average values of bacterial abundance that are observed in coral reef waters around the world are 7.0 × 105 cells mL−1 and 9.2 × 105 cells mL−1, respectively (Table 2.4).
Table 2.4

DOC concentrations, bacterial abundances, and growth rates in various coral reef waters

Site

References

Specific sampling site

DOC (μM)

Bacterial abundance (105 cells ml−1)

Bacterial growth rate (day−1)

Pacific Ocean

Bora bay (Miyako Island, Japan)

Ferrier-Pagés and Gattuso (1998)

Reef flat

6.2–13 (7.0)

1.3–2.8 (2.1)

Casareto et al. (2006)

Reef flat

70–77 (72)

1.1–5.8 (3.3)

Kushimoto (Japan)

Taniguchi et al. (2014)

Reef flat

5.2–8.3 (6.6)

2.7–6.4 (5.2)

Bidong Island (Malaysia)

Nakajima et al. (2013)

Reef flat

69–73 (71)

13–14 (14)

0.72–0.81 (0.76)

Offshore

63

14

0.79

Majuro Atoll (Marshall Islands)

Yoshinaga et al. (1991)

Lagoon

53–188 (145)

8.0–14 (11)

0.04–0.87 (0.35)

Offshore

72–143 (109)

6.2–13 (8.9)

Ponape Island (Micronesia)

Yoshinaga et al. (1991)

Lagoon

163–355 (235)

7.8–16 (11)

0.17–4.3 (2.5)

Lizard Island (GBR, Australia)

Moriarty (1979)

Reef flat/lagoon

1.6–6.1 (3.9)

Moriarty et al. (1985)

Reef flat

2.9–6.5 (4.2)

0.10–6.8 (1.6)

Reef front

3.7–8.0 (6.1)

0.05–2.5 (0.68)

Ocean

3.1–8.0 (6.2)

0.10–1.5 (0.56)

One Tree Island (GBR, Australia)

Linley and Koop (1986)

Reef flat

2.5–6.8 (4.8)

1.6–4.2 (2.4)

Tikehau Atoll (Tuamotu, French Polynesia)

Torréton and Dufour (1996a)

Lagoon

23

0.10

Reef flat spillway

3.0

0.17

Offshore

4.5

0.051

Torréton and Dufour (1996b)

Lagoon

18

0.18

Torréton et al. (1997)

Lagoon

105

24

0.12

Offshore

87

5.0

0.090

González et al. (1998)

Lagoon

12–26 (19)

0.11

Takapoto Atoll (Tuamotu, French Polynesia)

Torréton and Dufour (1996b)

Lagoon

6.4

0.28

Offshore

5.0

0.10

Torréton et al. (1997)

Lagoon

121

6.5

0.26

Sakka et al. (2000, 2002)

Lagoon

16

0.90

Rangiroa atoll (Tuamotu, French Polynesia)

Ferrier-Pagés and Furla (2001)

Reef flat spillway/channel

4–18 (11)

0.48–1.4 (0.96)

Fakarava atoll (Tuamotu, French Polynesia)

Ferrier-Pagés and Furla (2001)

Reef flat spillway/channel

9–14 (12)

0.48–0.96 (0.72)

Haraiki Atoll (Tuamotu, French Polynesia )

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

65–72 (69)

13–21 (17)

0.24–0.29 (0.27)

Hikueru Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

74–89 (82)

9.0–9.3 (9.2)

0.16–0.18 (0.17)

Hiti Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

79–80 (80)

17–24 (21)

0.10–0.14 (0.12)

Kauehi Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

72–78 (75)

12

0.07–0.11 (0.09)

Marokau Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

62–73 (68)

15–16 (15)

0.070

Nihiru Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

62

11–12 (12)

0.08–0.17 (0.13)

Rekareka Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

88–102 (95)

14–23 (19)

0.99–1.3 (1.1)

Taiaro Atoll (Tuamotu, French Polynesia )

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

144–161 (153)

18–19 (19)

0.12–0.18 (0.15)

Tekokota Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

61–62 (62)

2.2–3.0 (2.6)

0.16–0.22 (0.19)

Tepoto Sud Atoll (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Lagoon

64–76 (70)

6.4–15 (11)

0.22–0.33 (0.28)

Amanu Atoll (Tuamotu, French Polynesia)

Torreton et al. (2002)

Lagoon

9.3

0.15

Tuanake Atoll (Tuamotu, French Polynesia)

Torreton et al. (2002)

Lagoon

10

0.070

Tuamotu Atolls (Tuamotu, French Polynesia)

Pagés et al. (1997) and Torréton et al. (2000)

Offshore

64–76 (85)

6.4–15 (5.5)

0.028–0.038 (0.033)

Great Astrolabe Reef (Fiji)

Torréton et al. (1997)

Lagoon

114

7.5

0.28

Offshore

102

5.0

0.050

Torréton (1999)

Lagoon

114

7.7

0.28

Offshore

110

5.1

0.033

Maître Island (New Caledonia)

Torréton et al. (2010)

Lagoon

5.5–7.4 (6.4)

0.12–0.55 (0.28)

Kingman Atoll (Northern Line Islands)

Dinsdale et al. (2008)

Offshore

38–46 (42)

0.31–0.90 (0.57)

Palmyra Atoll (Northern Line Islands)

Dinsdale et al. (2008)

Offshore

47–61 (50)

1.3–3.5 (2.4)

Tabuaeran Atoll (Northern Line Islands)

Dinsdale et al. (2008)

Offshore

42–69 (50)

2.6–4.6 (3.7)

Kiritimati Atoll (Northern Line Islands)

Dinsdale et al. (2008)

Offshore

29–35 (32)

1.4–8.5 (5.2)

Atlantic Ocean

Florida Keys (USA)

Hoch et al. (2008)

Reef flat

91–130 (104)

3.4–9.0 (5.5)

0.57–1.5 (1.1)

Dry Tortugas (Florida, USA)

Paul et al. (1986)

Reef flat

2.6–6.3 (4.6)

0.10–0.99 (0.55)

Curaçao (Caribbean Sea)

Gast et al. (1998)

Reef flat

3.3–8.2 (5.7)

0.13–0.58 (0.26)

Scheffers et al. (2005)

Reef flat

4.4–6.2 (5.3)

0.11–0.46 (0.20)

van Duyl and Gast (2001)

Reef flat

142

0.30

van Duyl and Gast (2001)

Offshore

143

0.13

Belize (Caribbean Sea)

Haas et al. (2016)

 

62–72 (69)

5.6–6.7 (6.1)

Tobago (Caribbean Sea)

Haas et al. (2016)

 

47–57 (51)

6.1–15 (8.5)

Panama (Caribbean Sea)

Haas et al. (2016)

 

45–52 (48)

7.0–19 (15)

Puerto Rico (Caribbean Sea)

Haas et al. (2016)

 

47–54 (50)

6.4–19 (11)

Indian Ocean

Mayotte (Comoros Islands)

Vacelet et al. (1999)

Lagoon

4.3

Houlbrèque et al. (2006)

Lagoon

4.5

Sri Lanka

Haas et al. (2016)

 

43–57 (51)

4.3–19 (11)

 

Some values were visually interpreted from figures. The values in parentheses are the means of several data in the study

Several authors have reported that the bacterial abundance is higher in lagoons or reef flats compared to that in the surrounding oceanic waters (Table 2.4). For example, the bacterial abundance in the atoll lagoons of Tuamotu Archipelago was 1.5–5.3 times higher than that in the surrounding ocean (Torréton and Dufour 1996a, b; Torréton et al. 1997). A similar pattern was also found in Great Astrolabe Reef, Fiji, and Majero Atoll, Marshall Islands (Yoshinaga et al. 1991; Torréton 1999). These bacterial distribution patterns are similar to those of DOM, as reviewed above, and indicate that bacterial growth is enhanced by bioavailable DOM that is produced in the reef.

2.4.2 Bacterial Growth and DOM Consumption

2.4.2.1 Bacteria Growth in Natural Environments

The bacterial growth rate is usually defined as the specific growth rate during a period of exponential increase in the bacterial abundance:
$$ \mathrm{Specific}\kern0.56em \mathrm{growth}\kern0.56em \mathrm{rate}=\frac{\ln N-\ln {N}_i}{t} $$
where N and Ni indicate the bacterial abundances at the end and beginning of a period (t), respectively. The bacterial growth rates in coral reefs have been reported to be 0.03–6.8 day−1 (Table 2.4). The median and average growth rates are 0.26 day−1 and 0.58 day−1, respectively. The median rate indicates that the bacterial abundance takes 2.7 days to double in seawater.

The bacterial growth in a reef water column was not completely supported by DOM that was released from phytoplankton alone (Torréton et al. 2002; Rochelle-Newall et al. 2008). This observation indicates that benthic organisms other than phytoplankton play a major role in providing DOM to pelagic bacteria . In the southwestern lagoon of New Caledonia, only 10–20% of the bacterial C demand in seawater was met by planktonic DOC production (Rochelle-Newall et al. 2008). When seawater becomes more eutrophic, primary production in the seawater is enhanced and more DOM is produced, with the bacterial C demand largely being met by planktonic DOC production, as observed in the coastal bay stations of New Caledonia (Rochelle-Newall et al. 2008).

The bacterial growth rate at Lizard Island, Great Barrier Reef, was higher at daytime than nighttime (Moriarty et al. 1985), which suggests that bacterial production was enhanced as organic matter released from photosynthesizing organisms. This observation corresponds to the DOM production rate on the Shiraho reef flat, which was higher at daytime than nighttime (Tanaka et al. 2011b). Additionally, the bacterial growth rates at Lizard Island were 15 times higher during the summer than those during the winter (Moriarty et al. 1985), which suggests that higher temperatures increased the release rates of organic matter from benthic organisms (Haas et al. 2010b; Naumann et al. 2010).

2.4.2.2 Bacterial Growth Enhanced by Specific Organisms

Bacterial aggregation on coral mucus was first found several decades ago (Sorokin 1973; Ducklow and Mitchell 1979), and a number of studies have reported higher bacterial densities and oxygen consumption rates in coral mucus (Table 2.5). For example, Nakajima et al. (2015) observed that the bacterial abundance in seawater increased much more quickly with the experimental addition of coral mucus than in the control seawater (Fig. 2.6). The other benthic primary producers, e.g., macroalgae, turf algae, and crustose coralline algae, also exuded significant amounts of DOM into the surrounding seawater, which enhanced bacterial growth (Table 2.5).
Table 2.5

Bacterial growth rates with the addition of DOM that was released from coral reef organisms

References

Species or genus

Medium size (μm)

Initial DOC (μM)

Initial bacterial abundance (105 cells mL−1)

Bacterial growth rate (day−1)

Coral

Herndl and Velimirov (1986)

Cladocora caespitosa

<5

219

5.3

1.6

Seawater control

<5

158

2.5

1.3

van Duyl and Gast (2001)

Madracis mirabilis/favelota

<0.7

211

1.1

2.1

Seawater control

<0.7

173

1.1

2.1

Tanaka et al. (2008a)

Acropora pulchra

<0.7

63

2.0

0.33

Porites cylindrica

<0.7

63

5.0

0.62

Tanaka et al. (2008b)

Acropora pulchra

<0.7

83

0.036

3.5

Porites cylindrica

<0.7

91

0.058

2.8

Nakajima et al. (2009)

Acropora robusta (A. nobilis)

<3

252

7.1

2.6

Seawater control

<3

87

3.5

0.62

A. muricata (A. formosa)

<3

124

5.6

3.3

Seawater control

<3

59

3.4

0.65

Haas et al. (2011)

Porites

<0.2

80

2.0

1.0

Nelson et al. (2013)

Porites

<0.2

78

0.35

Nakajima et al. (2015)

A. robusta/A. muricata

<0.7

341

21.1

2.7

Seawater control

<0.7

82

8.2

0.72

Benthic algae

    

Haas et al. (2011)

Amansia

<0.2

238

2.0

0.88

Turbinaria

<0.2

192

2.5

0.91

Halimeda

<0.2

123

4.0

0.84

Seawater control

<0.2

73

3.8

0.43

Nelson et al. (2013)

Amansia

<0.2

177

1.1

Turbinaria

<0.2

181

0.61

Halimeda

<0.2

113

0.65

Seawater control

<0.2

70

0.41

Some values were visually interpreted from figures

Fig. 2.6

Increase in bacterial abundance in the seawater with coral mucus (Modified from Nakajima et al. 2015, with permission from ©Blackwell Verlag GmbH)

Measuring bacterial growth rates by using organic matter that is released from coral reef organisms has shown that the growth rates range from 0.33 to 3.5 day−1 (Table 2.5). This range of bacterial growth rates seems to be much higher than that observed in natural coral reef waters (Table 2.4), which suggests that bacterial growth in natural reef waters is more or less limited by the availability of organic matter. The bacterial production rates that were measured near the surface of corals were higher than that in the ambient seawater (van Duyl and Gast 2001; Scheffers et al. 2005), which shows that the bacterial growth rates in coral reefs are enhanced if more organic matter is available in the seawater.

2.4.2.3 Relationship Between the DOC Concentration and Bacterial Growth Rates

In theory, a higher DOM concentration supports a higher rate of bacterial DOM consumption and subsequent bacterial cell production until the consumption rate reaches a maximum according to the Michaelis-Menten equation (Kirchman 2012). We tested the relationship between DOC concentrations and bacterial growth rates by using the data in Tables 2.4 and 2.5 to find a general pattern. When only the data from natural reef waters were used (Table 2.4), a significant correlation was not found between these two parameters (Fig. 2.7). This unexpected result may have been caused by differences in the composition of organic matter, such as the C:N ratios, and/or the analytical precision of the determination of DOC concentration (Sharp et al. 2002a) and bacterial abundance (Shibata et al. 2006). Several studies have reported higher bacterial growth rates in seawater with higher DOC concentrations at local scales (Nelson et al. 2011; Rochelle-Newall et al. 2008; Bouvy et al. 2012). However, when the data on incubations with additional organic matter, such as coral mucus (Table 2.5), were combined with the data from natural reef waters, a statistically positive correlation was found between the DOC concentrations and bacterial growth rates (Spearman’s rank test, p < 0.01; Fig. 2.7). This result shows that bacterial growth rates are clearly enhanced with high DOC concentrations of approximately >100 μM.
Fig. 2.7

Relationship between the DOC concentration and bacterial growth rate in coral reefs (The data from Table 2.4 (natural environments) and Table 2.5 (artificial enrichment in organic matter) are shown in open circles and filled triangles, respectively)

The uptake of media from seawater by microbes is limited by kinetic controls or mass transfer controls (Sanford and Crawford 2000). When the reaction rates at or below the surface of microbes are faster than the mass transfer rates, the uptake rate is controlled by mass transfer (Thomas and Atkinson 1997). Conversely, when the reaction rates are slower than the mass transfer rates, the uptake rate is kinetically controlled and thus increases with the concentration of the medium up to a maximum rate (Badgley et al. 2006). Nutrient uptake by primary producers in oligotrophic environments such as coral reefs occurs under mass transfer rather than through kinetics (Thomas and Atkinson 1997; Hearn et al. 2001; Atkinson and Falter 2003; Badgley et al. 2006; Atkinson 2011), where nutrients in seawater are not rapidly taken up because of the limitations of diffusion from the seawater to the consumer. Atkinson and Smith (1987) showed that only 11% of 32P that was artificially added to seawater on a coral reef flat was removed after the water traveled 450 m across the reef flat. The relationship between DOC concentrations and bacterial growth rates (Fig. 2.7) suggests that DOM consumption by bacteria in natural coral reef waters may be regulated by both the DOM concentration in the seawater and the water flow or turbulence, which controls the mass transfer rates (Peters et al. 1998; Sanford and Crawford 2000).

The median bacterial abundances and growth rates that were observed in natural reef waters (7.0 × 105 cells mL−1 and 0.26 day−1, respectively; Table 2.4) allowed us to calculate a general production rate of bacterial cells of 2.1 × 105 cells mL−1 day−1. If we suppose that each bacterial cell contains 20 fg C (Fukuda et al. 1998), the production rate is estimated to be 0.35 μmol C L−1 day−1. This estimated production rate of bacterial cells in coral reef waters actually covers most of the previously measured rates: 0.04–0.48 μmol C L−1 day−1 (Torréton et al. 1997), 0.2–2.3 μmol C L−1 day−1 (Ferrier-Pagès and Gattuso 1998), 0.02 μmol C L−1 day−1 (Torréton 1999), and 0.29 μmol C L−1 day−1 (Rochelle-Newall et al. 2008). The bacterial growth efficiency is defined as the ratio of increased bacterial C to consumed organic C (Kirchman 2012). If we suppose that this efficiency is between 15% and 35% as the values for general marine bacteria (Kirchman 2012), the total C consumption by pelagic bacteria in coral reef waters is calculated to be 1.0–2.3 μmol C L−1 day−1. The reef flat at Shiraho Reef has an approximate average depth of 2 m, so the bacterial consumption rate of organic C in the seawater is 2.0–4.6 mmol m−2 day−1, which is <21% of the net production rate of DOC on the reef flat (22 mmol m−2 day−1; Table 2.3).

2.4.3 Quantitative Evaluation on DOM Degradability

Quantitatively evaluating the degradability of DOM is important to understand the biogeochemical cycles of DOM in coral reefs. Seawater that is collected in a coral reef (reef flat or lagoon) mainly has two fractions of DOM in terms of degradability: (1) newly produced DOM in the coral reef and (2) refractory DOM that ubiquitously exists in the global oceans (Fig. 2.3). Evaluating the degradability of DOM (1) requires collecting seawater samples inside and outside the reef and comparing the degradability of the DOM in those seawater samples.

The DOC in seawater that was collected on the reef flat at Shiraho Reef was mineralized by 10–18 μM for 1 year under dark conditions, while the offshore oceanic DOC was only mineralized by 4–5 μM (Tanaka et al. 2011a). This result indicates that the coral reef water had more bioavailable DOM than the oceanic seawater. When the mineralization of reef-derived DOC was described by an exponential decay model according to two degradability pools, the degradable fraction comprised 63–94% (average 77%) and the non-degradable fraction comprised 6–37% (average 23%). The degradable fraction had mineralization rates of 0.021–0.077 day−1, which means that 63% of the fraction was mineralized within 13–48 days. These mineralization rates (decay constants) of reef-derived DOC are comparable to those of organic C that was released from corals (0.003–0.016 day−1; Tanaka et al. 2011c), DOC that was released from temperate macroalgae (0.0058–0.041 day−1; Wada et al. 2008), or DOC that was collected at the mid-Atlantic bight (0.22 day−1 and 0.018 day−1 for the very labile and labile fraction, respectively; Hopkinson et al. 2002). The determination of decay constants is greatly affected by the experimental designs, such as the sampling intervals (e.g., hours, days, or months) or the number of fractions in the decay model (e.g., labile, semi-labile, or refractory). Nonetheless, these comparisons suggest that DOM that is produced in coral reefs has a similar degradability to DOM that is produced in other aquatic ecosystems.

Longer water residence times in a coral reef mean that more bioavailable DOM is decomposed and mineralized to DIC in the reef ecosystem (Mari et al. 2007). In lagoons with extremely long water residence times, such as the atolls in Tuamotu Archipelago, Phoenix, Marshal, and Line Islands (16–2190 days, Delesalle and Sournia 1992), all the labile and semi-labile DOM would be mineralized in the lagoon. The DOM in coral reefs is also transformed into POM via transparent exopolymeric particles (TEP), which causes the organic matter to become trapped within larger particles and to accumulate in the reef (Mari et al. 2007). This transformation of DOM could facilitate the settling of organic matter on the reef sediment and the mineralization of organic matter by bacteria and consequently reduce the export of DOM from the reef to the ambient ocean (Wild et al. 2004a; Mari et al. 2007; Naumann et al. 2012).

Some of the DOM (6–37%) that was produced on the Shiraho reef flat was not mineralized by bacteria in dark incubations over 1 year (Tanaka et al. 2011a). If we suppose that DOC production comprised 18% of the net primary production on Shiraho Reef (Table 2.3), 1–7% (average of 4%) of the net primary production would remain as refractory organic C for at least 1 year. Some fractions of the DOM that are released from corals have been reported to be resistant to bacterial decomposition (Vacelet and Thomassin 1991; Tanaka et al. 2008b, 2011c). These observations showed that some reef-derived DOM is recalcitrant to bacterial decomposition over long periods, and this fraction could be more or less exported offshore irrespective of the water residence time in the reef. Because the degradability tests in Tanaka et al. (2011a) were performed under dark conditions, the existence of sunlight might make these reef-derived DOM more susceptible to bacterial mineralization because of photoreactions (Moran and Zepp 1997; Wada et al. 2015), although only a minor role of photochemical transformation in the cycling of DOM was proposed in a shallow subtropical seagrass-dominated lagoon (Ziegler and Benner 2000).

This section summarized the decomposition of DOM by planktonic bacteria (bacterioplankton). However, the density of bacteria in reef sediment is much higher than that in the water column, and these benthic bacteria also contribute to the decomposition of DOM (Wild et al. 2004a, b, 2005). The relative contributions of benthic and planktonic bacteria to DOM consumption are also important to understanding DOM cycles in coral reefs, which is a subject to be resolved in the future.

2.5 Summary

This paper is a first review article that summarized our present understanding of DOM cycles in coral reefs. Data from laboratory experiments, such as DOM that is released from individual organisms, have been more frequently collected from various coral reefs around the world, but elaborate studies on DOM cycles at reef scales are limited to several reefs. In particular, the concentration of DON has scarcely been measured for coral reef waters. Further research is required to understand and generalize the behavior and function of DOM in coral reef ecosystems. The summary of this chapter is as follows:
  1. 1.

    In most coral reefs, the DOM concentrations and bacterial abundance are higher on the reef flat or in the lagoon than in the surrounding ocean. This observation indicates that coral reef ecosystems produce labile DOM for bacteria and likely promote energy flows in microbial food web s.

     
  2. 2.

    On average, the net production rate of DOC comprised 18% of the net primary production rate at Shiraho Reef. The C:N ratio of the DOM that was produced on the reef flat was estimated to be 9.3, which was much lower than that of DOM in the ambient open ocean. The major DOM producers at this coral reef were inferred to be benthic microalgae, including cyanobacterial mats.

     
  3. 3.

    Many coral reef organisms release DOM into the ambient seawater. The median DOC release rate was 0.20 mmol m−2 h−1 for corals and 0.45 mmol m−2 h−1 for benthic algae. The contribution of phytoplankton to the DOM production on shallow reef flats is much lower than that of corals or benthic algae.

     
  4. 4.

    The median bacterial abundances and growth rates in the coral reef waters were 7.0 × 105 cells mL−1 and 0.26 day−1, respectively. The estimated bacterial consumption rate of organic C in seawater was 1.0–2.3 μmol C L−1 day−1. The bacterial consumption of DOM might often be controlled by mass transfer.

     
  5. 5.

    Long-term quantitative evaluations of DOM degradability showed that a considerable portion of the DOM that is produced in coral reefs is not mineralized by bacteria over several months. Thus, coral reef ecosystems more or less provide DOM to the surrounding ocean, irrespective of the water residence time in the reef.

     

Notes

Acknowledgment

We are grateful to two anonymous reviewers who gave us plenty of valuable comments to improve this article. This study was supported by Brunei Research Council (S&T-14), the Japan Society for the Promotion of Science (JSPS) Asian CORE Program, and JSPS Postdoctoral Fellowships for Research Abroad.

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© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Faculty of ScienceUniversiti Brunei DarussalamGadongBrunei Darussalam
  2. 2.Scripps Institution of OceanographyLa JollaUSA

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