Pulse Sediment Event Does Not Impact the Metabolism of a Mixed Coral Reef Community

Ocean and Coastal Management xxx (xxxx) xxx

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Ocean and Coastal Management

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Pulse sediment event does not impact the metabolism of a mixed coral reef community

K.D. Bahr a,*, K.S. Rodgers b, P.L. Jokiel b, N.G. Prouty c, C.D. Storlazzi c a Texas A&M University – Corpus Christi, Corpus Christi, TX, 78414, USA b University of Hawai’i, Hawaiʻi Institute of Marine Biology, Kane� ʻohe, HI, 96744, USA c US Geological Survey, Pacific Coastal and Marine Science Center, Santa Cruz, CA, 95060, USA

ARTICLE INFO ABSTRACT

Keywords: Sedimentation can bury corals, cause physical abrasion, and alter both spectral intensity and quality; however, Sedimentation few studies have quantified the effects of sedimentation on coral reef metabolism in the context of episodic Coral reefs sedimentation events. Here, we present the first study to measure coral community metabolism - calcification Community metabolism and photosynthesis - in a manipulative mesocosm experiment simulating a pulse sediment event. We exposed a mixed benthic community composed of 75% live carbonate rubble cover and 25% Montipora capitata coral cover À to an approximately 275 mg cm 1 (sediment accumulation) acute pulse sediment loading event. No differences were found in net calcification or net photosynthesis between the control and treated mesocosms 48 h and 25 d following exposure to pulse sediment input. Results from this community experiment indicate the ability of Montipora capitata, a common reef coral, to persist under these acute sediment levels, demonstrating resistance to episodic sediment events.

À 1. Introduction volume (mg l 1) or as sediment accumulation rates per unit surface area À À (mg cm 2 d 1) in sediment traps. Corals are estimated to be impacted by À À Coral reefs have high biological diversity and high rates of produc chronic sediment accumulation rates greater than 10 mg cm 1 day 1 À tivity; however, reefs are undergoing significant ecological change due and TSS above 10 mg l 1 (Rogers, 1990). These estimations may vary to local and global stressors. Sedimentation has been widely identifiedas dependent on the sediment properties (Flores et al., 2012). For example, a major detrimental factor on coral reefs (Cort�es and Risk, 1985; Fab corals have the greatest difficulty in removing the finest sediment ricius, 2005; Grigg and Birkeland, 1997; Johannes, 1975; Marshall and fractions (i.e., silt <63 μm) (Weber et al., 2006). Orr, 1931; Risk, 2014; Rogers, 1990). Direct and indirect impacts from Coral physiological stress occurs within hours of exposure to sedi sedimentation include burial, abrasion of coral surfaces, and a reduction mentation (Philipp and Fabricius, 2003; Weber et al., 2006). Sediment in the amount of photosynthetically active radiation (PAR). deposition on the coral colony leads to down-regulation of photosyn Extensive reviews (e.g., Fabricius, 2005; Rogers, 1990) have deter thesis and increased rates of respiration and mucous production for mined response of corals and coral reefs to sedimentation depends on: 1) sediment and particle removal (Riegl, 1995; Yentsch et al., 2002; Philipp stress response mechanisms from light reduction or sediment accumu and Fabricius, 2003; Telesnicki and Goldberg, 1995). Although corals lation; 2) amount and type of sediment, and the ability of the coral to have a variety of mechanisms to actively remove sediment particles (e. remove sediment; and 3) species-specific capabilities such as coral g., mucous production, tentacle movement, etc.), mortality can occur by morphology (calices, colony surface), orientation (vertical, horizontal) suffocation under anoxic conditions and startvation through depression and behavior (Fabricius, 2005; Rogers, 1990). Additionally, coral of photoynthesis or heterotrophic feeding (Hubbard and Pocock, 1972; response varies with episodic (infrequent) versus chronic sediment input Rogers, 1990; Philipp and Fabricius, 2003). (e.g., mudslide from 50-yr storm, versus chronic runoff due to poor land Organismal-level effects of sedimentation are well documented in use, etc.) and their drivers (Field et al., 2008). Quantitative studies have corals, but less is known about the impacts of sediment accumulation on generally described sediment impacts on corals in terms of suspended the coral community metabolism such as primary production, respira sediment concentrations as a mass of total suspended solids (TSS) per tion, calcification, and dissolution. The contribution of a coral reef

* Corresponding author. 6300 Ocean Drive, Unit 5800, Corpus Christi, TX, 78412-5800, USA. E-mail address: [email protected] (K.D. Bahr). https://doi.org/10.1016/j.ocecoaman.2019.105007 Received 4 April 2019; Received in revised form 24 September 2019; Accepted 25 September 2019 0964-5691/Published by Elsevier Ltd.

Please cite this article as: K.D. Bahr, Ocean and Coastal Management, https://doi.org/10.1016/j.ocecoaman.2019.105007 K.D. Bahr et al. Ocean and Coastal Management xxx (xxxx) xxx ecosystem to the global carbon cycle is a balance between organic car Inflowand outflowin all mesocosms was suspended for a 4 h period to bon production (photosynthesis) and consumption (respiration), and allow the sediment to settle. The duration of the pulse sediment event between calcium carbonate precipitation and dissolution. Sedimenta was set to be on the order naturally observed off high islands in the tion may disrupt this balance at the local scale and shift the role coral Pacifc Ocean (Field et al., 2008; Presto et al., 2010; Storlazzi et al., 2008, reefs play in the carbon cycle, from either serving as a carbon source or 2009, 2010, 2012). The other three mesocosms were left untreated to sink to the atmosphere. Therefore, the goal of this study was to deter serve as controls (Fig. 2). Diurnal coral community metabolism was mine the effect of an acute pulse sedimentation event on the metabolism characterized for 48 h following the sediment exposure (30 March of a mixed benthic coral reef community. 2016), and again 25 d (22 April 2016) later to assess recovery.

2. Methods 2.2. Analytical procedures

2.1. Experimental setup Environmental parameters were recorded hourly in the inflow and outflow of each mesocosm during diurnal sampling on 28 March 2016, This research was conducted in the flow-through mesocosm system 30 March 2016, and 22 April 2016. The HIMB meteorological station ʻ ʻ at the Hawai i Institute of Marine Biology (HIMB) at Moku o Lo e, located on site provided subaerial irradiance measurements (total irra � ʻ ʻ � � Kane ohe Bay, Hawai i (21.4 N, 157.8 W). This mesocosm system is diance, ultra violet, photosynthetically active radiation) as well as wind located in full sunlight and replicates the physical, chemical, and bio direction and speed, air temperatures, and precipitation data; these data logical conditions on a shallow reef flat (Jokiel et al., 2008; Kuffner are available at http://www.pacioos.hawaii.edu/weather/obs- et al., 2008). Flow rates for the open-system mesocosms averaged 10 l À mokuoloe/. 1 � À min for an approximately 1-hr turnover rate. Temperature ( C), polarographic dissolved oxygen (mg l 1), and Six continuous flowmesocosms were used for this experiment (660 l o salinity ( /oo) were measured in the inflow and outflow of each meso each). Each mesocosm contained a mixed benthic community composed cosm using a YSI multiparameter meter (YSI 556MPS) that has an ac of 75% live carbonate rubble (~8 cm) cover and 25% Montipora capitata � À 1 � curacy of �0.15 C, �0.2 mg l , and �2 /oo (Table 1), respectively. An (~20 cm colonies) coral cover (Fig. 1). Monitpora capitata is a major Accumet AP72 pH/mV/temperature meter with an accuracy of �0.01 reef-forming coral in Kane� ʻohe Bay and the third most dominant coral pH and �0.02 mV was used to measure pHNBS. Unfiltered seawater ’ species throughout Hawai i (Forsman et al., 2010; Maragos, 1972). samples for total alkalinity (TA) measurements were collected hourly Although it possesses encrusting, plating, and branching growth forms, and stored in 250-ml clear borosilicate glass bottles and analyzed within the most common branching morphology was used in this study. Coral 2 h of collection. TA was measured independently using an automatic and calcareous rubble were collected from the adjacent reef flat(~0.5 m titrator (Titrino Plus 877, Metrohm) with pH glass electrode (LL Aqua ’ depth) around Moku o Lo e. The coral and calcareous rubble were trode plus Pt1000, Metrohm) and normalized to salinity. Accuracy of the acclimated to ambient mesocosm conditions for 5 days before beginning automatic titrator was confirmed with certified reference materials the experiment. (Batch 127 from A. Dickson Laboratory, Scripps Institution of Ocean Diurnal community metabolism was measured prior to sediment ography). Two-point NBS (YSI 3822) standards (at pH 4 and pH 7) were loading on 24 March 2016 to generate a baseline and range of com use to calibrate the pH glass electrodes (i.e., Accumet AP72, Metrohm LL munity metabolism (i.e., calcificationand photosynthesis) in all 6 tanks. Aquatrode plus Pt1000). Temperature, TA, pHNBS, and salinity were Sediment loading commenced on 28 March 2016. Standard brass sieves used to calculate pCO2 and dissolved inorganic carbon (DIC) using the (USA Standard Testing Sieve: A.S.T.M.E.-11 specifications)were used to program CO2SYS (Pierrot et al., 2006) with the stoichiometric dissoci < evaluate the sediment size fraction. The silt/clay fraction ( 63 μm) was ation constants (K1, K2) defined by Mehrbach (1973) and refit by determined according to the Wentworth scale (Folk, 1974). A terrige Dickson and Millero (1987) using pHNBS parameters. Nutrient samples nous clay collected from an undisturbed eroding area in an isolated were not collected during the experiment. section near the highest point of Moku o Lo’e was used to avoid con taminants, therefore sediment was untreated. Sediment was combined 2.3. Sediment accumulation with 20 l of seawater to create a slurry and added to three randomly-selected mesocosms to simulate an acute sedimentation event. Three sediment traps, constructed from PVC, collected sediment in

Fig. 1. Experimental setup at the Hawaiʻi Institute of Marine Biology at Moku o Loʻe, Kane� ʻohe Bay, Hawaiʻi during the simulated acute sediment loading event À (~275 mg cm 1 sediment accumulation) (A., B.). Each flow-throughmesocosm (660 l) contained mesocosm contained a mixed benthic community composed of live carbonate rubble (75%) cover and Montipora capitata (25%) coral cover was either exposed to sediment or held at ambient conditions.

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Fig. 2. Photographs of each mesocosm (Control and sediment) 6 h after sediment loading commenced on 28 March 2016.

Table 1 Environmental and chemical conditions for each treatment.

À 1 � À 1 À 2 À 1 Sampling Date Treatment pHNBS TA (μmol kg ) Temperature ( C) DO (mg L ) pCO2 (ppm) Irradiance (μmol photons m s )

Mean � SE Mean � SE Mean � SE Mean � SE Mean � SE Mean � SE Max

0 Control 8.06 � 0.01 2217.02 � 2.68 24.55 � 0.01 6.47 � 0.02 365.34 � 0.72 502 � 127 1624 Sediment 8.06 � 0.01 2215.21 � 3.42 24.53 � 0.01 6.46 � 0.01 366.74 � 2.06 2 Control 8.05 � 0.01 2177.08 � 0.61 25.37 � 0.02 7.00 � 0.01 376.52 � 0.68 633 � 128 1364 Sediment 8.04 � 0.01 2153.90 � 24.67 25.36 � 0.01 6.86 � 0.01 382.28 � 7.15 25 Control 8.07 � 0.01 2292.63 � 3.11 24.93 � 0.01 6.89 � 0.01 376.87 � 0.89 676 � 125 1354 Sediment 8.06 � 0.01 2290.30 � 1.30 24.94 � 0.02 6.85 � 0.01 377.32 � 0.71 each mesocosm (n ¼ 18). Traps were removed once all sediment had dO2 settled after 4 h under no-flowconditions, and thus accurately measured Pnet ¼ FinO2 À FoutO2 À dt (2) net sediment accumulation and not sediment dynamics (Storlazzi et al., 2010). Sediment within the traps was collected in pre-weighed What man 114 wet-strength filters, air dried, and weighed. Trap diameter 2.5. Statistical analysis (5 cm) and sediment weight were used to calculate sediment accumu À 1 lation in mg cm (Butman, 1986; Butman et al., 1986; Gardner, 1980, Environmental parameters (i.e., irradiance and pCO2) were 1980b). compared across sampling dates using a One-way ANOVA. Total daily GNet and PNet were calculated during daylight hours (07:00–19:00 HST) 2.4. Community metabolism and dark hours (20:00–06:00 HST). Total daily GNet and PNet were averaged among treatments and analyzed using a One-way ANOVA by Net calcification (Gnet) was calculated from the changes in TA be sampling date with fixed factors of treatment (i.e., sediment and tween the hourly inflow and outflow of each mesocosm using the TA control). anomaly method (Smith and Kinsey, 1978). Gnet represents the sum of all the calcificationprocesses minus the sum of all the dissolution processes 3. Results (Eq. (1)). Thus, all positive numbers represent net calcification and all negative numbers characterize net dissolution. Net calcification is Prior to the acute sedimentation event, environmental conditions À 2 À 1 expressed as mmol CaCO3 m h (Jokiel et al., 2014; Murillo et al., such as irradiance (one-way ANOVA; F(2,41) ¼ 0.5135; p ¼ 0.6024) and 2014). pCO2 (one-way ANOVA; F(2,29) ¼ 1.38; p ¼ 0.2694), parameters that

dAT could influencemetabolic response, did not differ across sampling dates FinAT À FoutAT À dt Gnet ¼ (1) (Table 1). Additionally, total daily GNet (p ¼ 0.6156 in light; p ¼ 0.7044 2 in dark), PNet (p ¼ 0.4300), and respiration (p ¼ 0.7438) did not differ Photosynthesis (Pnet) and respiration (R) were calculated from among mesocosms, indicating similar levels of metabolism among the À changes in dissolved oxygen concentration (mg l 1) between the hourly six coral communities in the treatment and control mesocosms prior to inflowand outflowof each mesocosm. Pnet represents the sum of oxygen the simulated sedimentation event. production during daylight hours and R refers to the sum of oxygen Two days (48 h) after exposing the coral communities to the acute consumption during dark hours (Eq. (2)). Surface to volume ratio of each pulse sediment loading, there was no significant difference in total net mesocosm is included in the calculation for community metabolic rates calcification( p ¼ 0.2814; Fig. 3) or total net photosynthesis (p ¼ 0.7831; per m2. Fig. 4) between the control and treatment mesocosms. However, diurnal fluctuations of GNet were variable between the control (min ¼ À 4.52, À 2 À 1 max ¼ 89.87 mmol CaCO3 m d ) and treatment (min ¼ À 66.78

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Fig. 3. Net calcificationof control communities (blue) and sediment-loaded communities (red) before sediment loading (initial), 48 h following the sediment loading event (30 March 2016) and 25 d after (22 April 2016). Shading indicates night-time measurements (20:00–06:00 HST). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

Fig. 4. Net photosynthesis of control communities (blue) and sediment-loaded communities (red) before sediment loading (initial), 48 h following the sediment loading event (30 March 2016) and 25 d after (22 April 2016). Shading indicates night-time measurements (20:00–06:00). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

À 2 À 1 max ¼ 30.70 mmol CaCO3 m d ) mesocosms, although the ranges and pH) remained similar between control and treatment communities À 2 À 1 were similar (control ¼ 94.39; sediment ¼ 97.48 mmol CaCO3 m d ) (Fig. 6). (Fig. 5). Diurnal curves of PNet and GNet were also similar among the control 4. Discussion and treatment mesocosms, therefore unimpacted by sediment loading (Fig. 5). Delayed impacts of sedimentation were not observed. Specif Results of this study reveal that coral community metabolism (i.e., ically, similar levels of GNet and PNet were observed in the control and GNet and PNet) did not differ among the control and treatment mesocosms treatment mesocosms 25 d following exposure (GNet p ¼ 0.7801; PNet 48 h and 25 d following a simulated episodic sedimentation event. This p ¼ 0.5605). Additionally, diurnal changes in concentration of carbon may indicate that a coral community dominated by Montipora capitata ate parameters (i.e., dissolved inorganic carbon, aragonite saturation, may be able to persist under these acute sedimentation accumulation

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Fig. 5. Time series of coral community response 48 h after exposure to sediment treatment. A. Average net photosynthesis. B. Average net calcification.Response of control (no sediment) communities indicated in blue and sediment loaded communities indicated in red. Irradiance is indicated by black dashed line. (For inter pretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) levels (~275 mg cm1) over the short exposure period (4 h) typically adaptive strategy to optimize diverse ecological factors such as light and observed in nature (Field et al., 2008; Presto et al., 2010; Storlazzi et al., water motion and to reduce the effects of sedimentation (Rogers, 1990). 2008, 2009, 2010, 2012). The removal mechanism, metabolic cost, size, and location, may explain The observed community response of M. capitata may depend on species-specific responses (Fabricius, 2005; Telesnicki and Goldberg, sediment type and duration of exposure (Piniak, 2007). Exposure time in 1995). Some coral morphologies (e.g., those with tall polyps and convex this study was short (4 h); however, physiological stress occurs within colonies) substantially reduce the need for active removal thereby hours of exposure to sediment (Philipp and Fabricius, 2003; Weber et al., reducing energy expenditure (Lasker, 1980), while mucus production by 2006) and is strongly related to grain size, organic content, and nutrient M. peltiformis traps silt-sized sediments therefore increasing energy composition of the sediment (Weber et al., 2006). For example, Philipp expenditure (Weber et al., 2006). Previous studies (Brown et al., 1986; and Fabricius (2003) found that short-term sediment loading stress on Maragos, 1972; Rogers, 1990) have shown larger colonies to be more M. peltiformis increased linearly with increasing amounts and duration of resistant to sediment loading than smaller ones. Lastly, many coral sediment exposure. Conversely, Piniak et al. (2004) found only slight species located close to shore are also known to have higher tolerances damage and rapid recovery to the symbiotic zooxanthellae and its to sedimentation and a greater ability to remove sediment than corals in photosynthetic capacity. They report little immediate effect with rapid deeper waters (Salvat, 1987). recovery following 6 h of sediment exposure but no severe damage after Adult corals can survive and continue to grow in high sedimentation 30 h with recovery after 24 h. With longer exposure periods (12–68 h), environments (Jokiel et al., 2014a, 2014b); however, there recruitment recovery was incomplete after 96 h and required up to 4 weeks of new corals is significantly impaired in the presence of sediment following exposure in previous studies (Wessling et al., 1999; Weber (Gilmour, 1999; Babcock and Davis, 1991; Jokiel et al., 2014a, 2014b; et al., 2006). In comparison with this study, by the 48 h and 25 Perez et al., 2014).Previous work has shown coral larvae settlement to À d sampling period, corals showed no changes in metabolism. Clearly be inhibited with a fine sediment layer (>0.9 mg cm 2) (Perez et al., duration of sediment loading is a contributing factor to speed and po 2014). Without successful settlement and recruitment of young corals tential of recovery. the sustainability and resilience of the coral reef is lessened. The resil The resistance of M. capitata to acute sediment loading may also be ience and recovery of coral reefs will be greatly reduced by land-derived attributed to a number of adaptations including morphology, polyp size, sediment. and rapid growth. An extensive review on coral response to sedimen High volcanic islands such as those in Hawaiʻi generally erode during tation (turbidity and/or loading) found that tolerance was significantly episodic, high-intensity rainfall events (Ferrier et al., 2013; Fontaine and related to coral growth morphology but not calyx size (Erftemeijer et al., Hill, 2002; Gayer et al., 2008), and generally during the winter when 2012). Branching morphologies, such as those used in this study, are an wave energy is high (Draut et al., 2009). This, together with the

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Fig. 6. Diurnal changes in concentration of carbonate parameters for control (blue) and sediment (red) treated coral communities before (initial; 28 March 2016), 48 h (30 March 2016) and 25 d (22 April 2016) after sediment loading. A. Total alkalinity (TA). B. Dissolved inorganic carbon (DIC). C. Aragonite saturation (ΩArag). D. Dissolved oxygen (O2). E. pHNBS. Grey shading indicates night time hours. Error bars are SE of the mean of mesocosms (n ¼ 3). (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) relatively short stream drainages, results in episodic run-off events that characterized by persistent high turbidity and chronic sediment loading, deliver a pulse of terrestrial sediment to the nearshore during a rela M. capitata showed increased mortality with increased turbidity (Jokiel tively short time interval (Field et al., 2008; Presto et al., 2010; Storlazzi et al., 2014b; Perez et al., 2014). This suggests that although able to et al., 2008, 2009, 2010, 2012). Such reefs are therefore naturally survive episodic pulse sedimentation events, M. capitata may not be exposed to such pulse terrestrial sedimentation events for a relatively suited to chronic turbidity and/or sediment deposition (Ogston et al., short duration, as subsequent winter large wave events would resuspend 2004; Presto et al., 2006; Storlazzi and Jaffe, 2008; Storlazzi et al., and advect the sediment away from the nearshore reefs (Presto et al., 2004). Anthropogenic activities (e.g., land-use change) are more readily 2006; Storlazzi and Jaffe, 2008). Thus, over the time scales of the islands linked to chronic sediment loading and increase terrestrial sediment and their associated coral reef development, nearshore corals were delivery to the nearshore (Field et al., 2008), especially in coral reef subjected to natural, episodic pulse sedimentation events and thus they locations that are generally exposed most of the year to Trade-wind must have evolved to occupy such environmental niches. forcing. Temporal results of episodic events from field studies vary More importantly, these results suggest that in contrast to chronic (Field et al., 2008; Pineda and Reyns, 2017; Storlazzi et al., 2009a,b). It exposure, episodic sediment input may be less detrimental, consistent is difficultto compare sediment suspension times and exposure of corals with fieldobservations. For example, corals off south Molokai, Hawai’i, to sediment loading at different sites due to a number of factors such as exposed to chronic terrestrial sediment exposure due to runoff from poor hydrodynamics, sediment properties, and physical barriers (Field et al., land-use practices and almost daily resuspension by Trade winds 2008; McCluney, 1975; Ogston et al., 2004; Presto et al., 2006; Storlazzi (Ogston et al., 2004; Presto et al., 2006; Field et al., 2008) exhibited et al., 2004, 2009; Storlazzi and Jaffe, 2008). lower growth rates compared to sites exposed to episodic sedimentation Although chronic sediment loading can be detrimental to corals, the events (Prouty et al., 2010). Episodic events such as measured here indirect impacts of episodic sediment events may contribute to an allow for periods of recovery when sediment levels return to baseline amelioration of bleaching impacts as climate change accelerates. Clays and corals are able to maintain a higher growth rate. At locations and fine organic particles are easily resuspended, reducing irradiance

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levels (Piniak and Storlazzi, 2008; Storlazzi et al., 2015) and thus dedicated to Dr. Paul Jokiel, a pioneer and visionary in the fieldof coral available light that affects energy acquisition for the algal symbionts (i. reef research and founder of the Coral Reef Ecology Laboratory where e., Symbiodinium spp), which, in turn, leads to lower carbon gain, slower this research was conducted. We would also like to thank Kim Yates calcification and thinner tissues (Anthony and Hoegh-Guldberg, 2003; (USGS) and three anonymous reviewers who contributed excellent Rogers, 1979; Telesnicki and Goldberg, 1995). However, during massive suggestions and timely reviews of our work. Use of trademark names coral bleaching events, sunlight and water visibility have been shown to does not imply USGS endorsement of products. be significantfactors in coral response to temperature stress (Jokiel and This publication is referenced as the University of Hawai’i’s School Coles, 1990). 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