REPORT

Environmental and ecological controls of coral communitymetabolism on Palmyra Atoll

David Koweek • Robert B. Dunbar •

Justin S. Rogers • Gareth J. Williams •

Nichole Price • David Mucciarone • Lida Teneva

Received: 17 January 2014 / Accepted: 17 September 2014

� Springer-Verlag Berlin Heidelberg 2014

Abstract Accurate predictions of how coral reefs may

respond to global climate change hinge on understanding

the natural variability to which these ecosystems are

exposed and to which they contribute. We present high-

resolution estimates of net community calcification (NCC)

and net community production (NCP) from Palmyra Atoll,

an uninhabited, near-pristine coral reef ecosystem in the

central Pacific. In August–October 2012, we employed a

combination of Lagrangian and Eulerian frameworks to

establish high spatial (*2.5 km2) and temporal (hourly)

resolution coral community metabolic estimates.

Lagrangian drifts, all conducted during daylight hours,

resulted in NCC estimates of -51 to 116 mmol C m-2 h-1,

although most NCC estimates were in the range of

0–40 mmol C m-2 h-1. Lagrangian drift NCP estimates

ranged from -7 to 67 mmol C m-2 h-1. In the Eulerian

setup, we present carbonate system parameters (dissolved

inorganic carbon, total alkalinity, pH, and pCO2) at sub-

hourly resolution through several day–night cycles and

provide hourly NCC and NCP rate estimates. We compared

diel cycles of all four carbonate system parameters to the

offshore surface water (0–50 m depth) and show large

departures from offshore surface water chemistry. Hourly

Eulerian estimates of NCC aggregated over the entire study

ranged from 14 to 53 mmol C m-2 h-1, showed substantial

variability during daylight hours, and exhibited a diel cycle

with elevated NCC in the afternoons and depressed, but

positive, NCC at night. The Eulerian NCP range was very

high (-55 to 177 mmol C m-2 h-1) and exhibited strong

variability during daylight hours. Principal components

analysis revealed that NCC and NCP were most closely

aligned with diel cycle forcing, whereas the NCC/NCP ratio

was most closely aligned with reef community composition.

Our analysis demonstrates that ecological community com-

position is the primary determinant of coral reef biogeo-

chemistry on a near-pristine reef and that reef

biogeochemistry is likely to be responsive to human

behaviors that alter community composition.

Communicated by Handling Editor Chris Perry

Electronic supplementary material The online version of thisarticle (doi:10.1007/s00338-014-1217-3) contains supplementarymaterial, which is available to authorized users.

D. Koweek (&) � R. B. Dunbar � D. Mucciarone � L. Teneva

Department of Environmental Earth System Science, Stanford

University, 473 Via Ortega, Room 140, Stanford, CA 94305,

USA

e-mail: dkoweek@stanford.edu

J. S. Rogers

Department of Civil and Environmental Engineering, Stanford

University, Stanford, CA 94305, USA

G. J. Williams � N. Price

Center for Marine Biodiversity and Conservation, Scripps

Institution of Oceanography, University of California San Diego,

La Jolla, CA 92093, USA

Present Address:

N. Price

Bigelow Laboratory for Ocean Sciences, East Boothbay,

ME 04544, USA

Present Address:

L. Teneva

Hawai‘i Fish Trust, Betty and Gordon Moore Center for Science

and Oceans, Conservation International, Honolulu, HI 96825,

USA

123

Coral Reefs

DOI 10.1007/s00338-014-1217-3

Keywords Net community calcification � Net community

production � Lagrangian drifts � Eulerian measurements �Coral reefs � Coral ecology

Introduction

Global-scale models based largely on open ocean simula-

tions suggest the demise of coral reefs in the warmer and

more acidic ocean of the future (Kleypas et al. 1999;

Hoegh-Guldberg et al. 2007; Doney et al. 2009; Ricke et al.

2013). Thermal stress on corals is anticipated to increase

with climate change, resulting in bleaching, increased

mortality, bioerosion, and loss of coral cover (Glynn 1993;

Hughes et al. 2003; van Hooidonk et al. 2013). Simulta-

neously, as anthropogenic carbon dioxide enters the surface

ocean from the atmosphere, a series of carbonate buffering

reactions lowers both carbonate mineral saturation state

(XAragonite and XCalcite) and surface ocean pH (Kleypas

et al. 1999). Ocean acidification (OA) is anticipated to

induce a host of changes in coral reef communities,

including decreased calcification rates, increased dissolu-

tion, erosion of reef-building corals, decreased community

diversity, physiological stress on calcifying organisms, and

exacerbated phase shifts toward algal dominance (An-

dersson and Mackenzie 2004; Hoegh-Guldberg et al. 2007;

Doney et al. 2009; Kroeker et al. 2010, 2013; Fabricius

et al. 2011; Andersson and Gledhill 2013).

Field-based studies on individual reefs have revealed a

far more heterogeneous perspective for the fate of many

coral reefs under future scenarios of climate change and

OA. Observations of diel, seasonal, and interannual phys-

ical and biogeochemical variability on individual reefs

often exceed the long-term background forcing on sea

surface temperature and surface pH from climate change

and OA (Barnes 1983; Gattuso et al. 1993, 1996; Kayanne

et al. 1995; Price et al. 2012). Coral and algal communities

are active components in their biogeochemical environ-

ments, manipulating their biogeochemistry via calcifica-

tion, primary production, and respiration (Smith and Key

1975; Barnes 1983; Suzuki and Kawahata 2003; Anthony

et al. 2011; Smith et al. 2013) However, the extent to which

coral reef communities metabolically regulate their bio-

geochemical environments is not uniform across reefs and

depends on a suite of hydrodynamic, biogeochemical, and

ecological factors (Anthony et al. 2011).

A growing number of recent field-based studies are

illuminating the temporal dynamics of coral reef commu-

nity metabolism (Falter et al. 2008, 2012; Shamberger et al.

2011; Shaw et al. 2012; McMahon et al. 2013; Teneva

et al. 2013). Limited work has characterized coral com-

munity metabolism in the central equatorial Pacific (Price

et al. 2012), largely because of the difficulties associated

with working in these remote locations. Yet, this isolation

creates de-facto natural laboratories where coral commu-

nity metabolism can be studied without the confounding

effects of localized anthropogenic stressors associated with

adjacent human populations.

We present a coupled spatial and temporal approach to

studying coral community metabolism on Palmyra Atoll,

an isolated, near-pristine coral reef ecosystem in the central

equatorial Pacific. We use Lagrangian drifts to estimate

coral community metabolism over reef terrace and back-

reef environments encompassing *2.5 km2 of coral reef

habitat with a variety of benthic ecological communities.

We complement our spatial measurements with diel cycle

hourly estimates of net community calcification (NCC) and

net community production (NCP) from a mixed-commu-

nity backreef environment using the Eulerian approach. We

evaluate the spatial and temporal patterns of coral com-

munity metabolism, as well as their environmental and

ecological controls. We emphasize the importance of field-

based measurements for enhancing our ability to predict

impacts on coral reef ecosystem functions under the

anticipated stresses of climate change and OA.

Methods

Study site

Jointly administered by The Nature Conservancy and the

US Fish and Wildlife Service, Palmyra Atoll (5�520N,

162�050W) is part of the Northern Line Islands of the

central equatorial Pacific (Fig. 1a). Due to its isolation

(*1,700 km south-southwest of Hawai’i), Palmyra has

never held a permanent human population except for a

brief period of US military occupation during World War II

that resulted in extensive modifications to the Atoll’s land

area and interior lagoons (Collen et al. 2009, 2011; Gardner

et al. 2010). Largely because of the absence of acute

anthropogenic stressors on the ecosystem, its exterior reefs

contain abundant calcifiers, large fish populations and

biomass, and apex predators (Stevenson et al. 2006; Sandin

et al. 2008; Williams et al. 2013). Palmyra Atoll has been a

US National Wildlife Refuge since 2001 and part of the

Pacific Remote Islands Marine National Monument since

2009.

Lagrangian drifts

Lagrangian drifts (i.e., flow respirometry) provide a pow-

erful technique to estimate coral community metabolism

over spatial scales of tens to hundreds of meters (Barnes

1983; Barnes and Lazar 1993; Gattuso et al. 1993). In order

to estimate spatial variability in coral reef community

Coral Reefs

123

metabolism, we conducted 21 Lagrangian drifts (hence-

forth referred to as ‘‘drifts’’) in August–October 2012 on a

combination of reef terrace (Western Terrace: WT) and

backreef environments (Penguin Spit: PS; Fig. 1b). Both

the WT and PS environments are mixed benthic commu-

nities featuring hard coral, soft coral, calcifying and non-

calcifying macroalgae, crustose coralline algae (CCA), and

turf algae (Electronic Supplementary Material, ESM,

Fig. 1, 2). The drifter was 1.4 m in length with a drogue

located near its mid-point (ESM Fig. 3). An SBE 37SM

(Sea-Bird Electronics, Inc.) was attached to the bottom of

the drifter to record water temperature and conductivity in

order to calculate salinity and density. Drifts were con-

ducted only during daylight hours and ranged from 1 to 2 h

in length. Bottom water samples (collected 0–1 m above

the bottom) and water depth measurements were taken via

free-diving every 8–15 min, depending on the length of the

drift. Water depths ranged from 0.6 to 8.2 m with a mean

depth of 4.3 m. Samples were analyzed for total alkalinity

(TA) immediately upon the completion of the drift and for

dissolved inorganic carbon (DIC) within several days of the

drift, although DIC was not analyzed on every drift. If the

DIC was not analyzed within a few hours after drift

completion, samples were preserved by adding saturated

mercuric chloride solution (\0.1 % by volume).

Drifts, or portions of drifts, that showed evidence of

water mass mixing (based on salinity discontinuities

greater than 0.05 psu and/or erratic, non-trending TA

throughout the drift) were eliminated from further analysis.

One drift conducted in the early morning was divided into

two drifts based on its TA profile, which suggested a

transition from static, near-zero NCC in the early-morning

to-late morning positive NCC. In total, we made NCC

estimates from 16 of the 22 drifts and NCP estimates from

nine of the 22 drifts.

Eulerian diel cycle measurements

In order to assess metabolic cycles and variability over

several day and night cycles (20 September 2012, 21–22

September 2012, and 25 September 2012), we conducted a

series of Eulerian measurements on a backreef site on the

southern side of Palmyra Atoll (Surface Interval Buoy,

SIB, site; Fig. 1c). Our observational setup consisted of a

moored mobile laboratory similar to that described in Te-

neva et al. (2013) and is briefly summarized here. Five

Fig. 1 Overview of study site

showing, a the location of

Palmyra Atoll in the central

Pacific, b Palmyra Atoll’s

western side with the Western

Terrace and Penguin Spit

regions, and c a diagram of the

SIB site. b Shows numbered

drift tracks (red lines with red

dot marking the start of each

drift), the SIB site for Eulerian

sampling, modeled flow from

the forereef on to the backreef

(magenta line), locations of

offshore hydrocasts south of

Palmyra Atoll (green circles),

and locations of ecological

surveys (yellow circles) used to

generate spatially interpolated

landscapes of reef community

composition metrics (see ESM

Figs. 1, 2). c Shows the position

of the mobile laboratory (peach

square), the position of tubes

1–5 (pink circles), and the drift

tracks of drift 16 (red line)

which occurred on 25

September 2012 during Eulerian

sampling

Coral Reefs

123

pieces of polypropylene tubing (3/800 ID, �00 OD; United

States Plastics Corp.), each 67 m in length, were deployed

across a 40 by 60 m area of backreef mixed coral com-

munity. Tubes 1–4 were deployed in the mid-water col-

umn, and tube 5 was deployed into the interior of a

branching Acropora sp. colony. Current meters (Aquadopp

Profilers-ADP, and Acoustic Doppler Velocimeters-ADV)

were co-located with the ends of each tube to measure the

flow regime at each tube (ESM Table S1). Water from all

five tubes was continuously pumped at an aggregate rate of

14 L min-1 (2.8 L min-1 tube-1) using an impeller pump.

Equal lengths of tubing and constant pumping rates

ensured the same residence time for water in all of the

tubes (1.7 min). The low residence time of water in the

tubes helped minimize oxygen and CO2 diffusion across

the tubing walls. Upon reaching the mobile laboratory, a

custom manifold successively introduced each tube to a

continuous flow system on board.

Biogeochemical instrumentation

The mobile laboratory was equipped with a peristaltic

pump operating at 2 L min-1 which moved water

sequentially through a suite of instruments including a SBE

45 thermosalinograph (Sea-Bird Electronics, Inc.), a Du-

raFET III pH sensor (Honeywell, Inc.), a ProCO2 pCO2

sensor (Pro-Oceanus Systems, Inc.), and an Aanderaa 3830

oxygen optode. We used the internal calibration procedure

for the ProCO2 pCO2 sensor. The Aanderaa 3830 oxygen

optode was factory calibrated in July 2012. We estimated

the volume of this suite of instrumentation to be 1 L, which

yielded a flushing time of 30 s. We instead used a con-

servative estimate of 1 min to minimize cross contamina-

tion between tubes. The manifold switched between tubes

every 5 min so data from each of the sensors is an average

of all measurements during the final 4 min of sampling.

Upon passing through the suite of sensors, pumped

water arrived in a free-surface interface cup from which it

was sampled for DIC and TA. DIC was measured with a

custom-built sample acidification and delivery system

coupled to an infrared gas analyzer (Licor 7000) described

in Long et al. (2011) and Teneva et al. (2013). The

instrument was calibrated daily using certified reference

materials (CRM) Batch 116 provided by A. Dickson

(Scripps Institution of Oceanography). Instrumental preci-

sion from 201 CRM analyses over the several weeks of this

study (including drift and hydrocast results) was

2.8 lmol kg-1 (1 SD). Immediate duplicate analyses of

samples usually yielded instrumental precision of

1–2 lmol kg-1. This instrument has an analysis time of

five min, allowing the entire set of five tubes to be sampled

every 25 min.

Discrete samples were collected from the continuous

flow system for TA analysis at an onshore temperature- and

humidity-controlled laboratory. Samples for TA were pre-

filtered through a 0.2-lm polyvinylidene fluoride filter

before being analyzed on a Metrohm 855 Robotic Titro-

sampler (Metrohm USA, Inc.) using certified 0.1 N HCl

provided by A. Dickson (Scripps Institution of Oceanog-

raphy). TA calculations from raw titration data follow

Dickson et al. (2003). Instrumental precision from 124

CRM analyses (Batches 110 and 116) over the several

weeks of this study (including drift and hydrocast results)

was 1.5 lmol kg-1 (1 SD). All samples were corrected

based on the offset between the measured and certified

value of the CRM, which increased from 0 to

12 lmol kg-1 in a nearly linear fashion over the duration

of the study. We attribute this drift to a gradual increase in

the concentration of the HCl due to evaporation.

Offshore hydrocasts were made across Palmyra’s for-

ereef environments and in deeper offshore waters using a

SBE 19?V2 mounted on a SBE 55 Niskin bottle sampling

rosette (Sea-Bird Electronics, Inc.; Fig. 1b). All hydrocasts

were conducted in late morning to mid-afternoon hours

with maximum depths ranging from 100 to 150 m. Discrete

water samples were collected for DIC and TA in accor-

dance with best practices for sample collection (Dickson

et al. 2007). Discrete DIC and TA measurements from

hydrocast and drift samples were analyzed on the same

analytical instrumentation as described above.

Carbon system calculations

Direct measurements of all four carbonate system param-

eters during the Eulerian measurements resulted in an over-

determined carbonate system. This provided an opportunity

to cross-check the measurements as a means of quality

control. During this validation procedure, we discovered

discrepancies in the measured pH data, possibly due to

faulty calibration of the sensor. As a result, all pH data

presented in this study are calculated, reported on the total

scale (pHT; Zeebe and Wolf-Gladrow 2001), and at the

in situ temperature.

pHT and aragonite saturation state (XAr) from Eulerian

sampling at the SIB site, as well as offshore pHT and pCO2,

were calculated in CO2SYS (van Heuven et al. 2011) using

temperature, salinity, DIC, TA, carbonate dissociation

constants from Mehrbach et al. (1973) as refit by Dickson

and Millero (1987), and the KSO4 for the bisulfate ion from

Dickson (1990). Without direct measurements of dissolved

silica or phosphate concentrations, carbon system calcula-

tions in CO2SYS were performed with concentrations of

dissolved silica and phosphate set to zero.

Coral Reefs

123

Coral community metabolism calculations

Lagrangian drifts

NCC estimates on coral reefs have traditionally used the

alkalinity anomaly technique, where changes in TA can be

entirely prescribed to net calcification (Smith and Key

1975). Drift mean estimates of NCC (denoted by the

overbar) are thus:

NCCdrift ¼ �1

2qqx

DsTA

Dx

where q is the mean water density and sTA is salinity-

normalized TA wherein TA is normalized to the mean

salinity observed during the drift. DsTA and Dx refer to the

changes in sTA and transect distance between subsequent

sampling points along a drift. The depth-integrated flow,

qx, is calculated by assuming logarithmic boundary flow

(Reidenbach et al. 2006; Rosman and Hench 2011)

u zð Þ ¼ u�j

lnz� d

z0

� �

where u is the velocity of the drifter center of mass, u* is

the frictional velocity, k is the von Karman constant (0.41),

z is the height above the substrate, z0 is the roughness

height, and d is an offset applied to boundary layer flow

over corals. Based on log-layer regression from the mea-

sured velocity at the SIB site (tube 1 ADP), z0 = 0.05 m

and d = 0.13 m which are consistent with values obtained

in similar reef environments (Rosman and Hench 2011).

After solving for u* at each point along a drift, integrating

from the roughness height and offset (z0 ? d), which was

assumed to be spatially and temporally uniform, through

the height of the entire water column (h) yields the depth-

integrated velocity, qx, at each point along the drift:

qx ¼Z h

z0þd

u zð Þdz ¼ u�j

z0 þ d � hþ ðh� dÞ ln h� d

z0

� �� �

Drift estimates of net community production (NCPdrift)

are based on changes in salinity-normalized DIC (sDIC)

after accounting for NCC and air/sea gas exchange (F):

NCPdrift ¼ �q qx

DsDIC

Dx� 1

2qx

DsTA

Dx

� �� F

Air/sea gas exchange, F, was calculated in CO2Calc

(Robbins et al. 2010) using the gas transfer velocity

parameterization of Ho et al. (2006), TA, DIC, tempera-

ture, and salinity (to calculate pCO2, water), and assuming

pCO2, atmosphere was 400 latm. We obtained hourly 10 m

height wind speed data from NASA’s MERRA Data

Assimilation System 2D atmospheric single-level diag-

nostic with a resolution of 2/3�longitude 9 1/2�latitude

(NASA 2007). F was never greater than

0.40 mmol C m-2 h-1 throughout the duration of the

entire study, so although we included it for completeness,

its effects on NCP estimates were negligible.

Error estimates for NCCdrift and NCPdrift are reported as

±1SD from the mean. NCCdrift error estimates were cal-

culated from the standard deviation (SD) of the product of

qx and DsTA/Dx for all points along the drift multiplied by

1/2q. Error estimates for NCPdrift were derived by first

calculating the SD of the first two terms of the NCPdrift

equation using the same methodology as for the NCCdrift

error estimate and then calculating the SD of the sum of the

two terms (we assumed no error for F).

Eulerian estimates of community metabolism

Eulerian NCC and NCP estimates are based on the time

rates of change of sTA and sDIC measured from a fixed

position (Silverman et al. 2007).

NCCi ¼ �1

2qh

DsTAi

si

where h is the transit time weighted mean height of the

water column and DsTAi is the difference in sTA between

the sTA at tube i and the mean sTA of the upper 50 m of

seven offshore hydrocasts (see ‘‘Results’’). si is the transit

time between the forereef and tube i (i = 1–4). The transit

time model is based on the ratio of measured Eulerian

velocities at the SIB site and the computed velocity of drift

16 that transited through the SIB site during Eulerian

sampling on 25 September (Fig. 1c; see ESM for details of

si calculations). TA and DIC were salinity-normalized to

the mean salinity from the upper 50 m of the seven off-

shore hydrocasts (34.87).

NCP measured at tube i is the change in sDIC from the

forereef to the SIB site (DsDIC) corrected for calcification

and air/sea gas exchange:

NCPi ¼�qh

si

DsDICi �1

2DsTAi

� �� F

Error estimates of NCC and NCP for each tube (also ±1

SD) were calculated using a single-sample uncertainty

analysis (Kline and McClintock 1953). We assumed no

error on the q calculation, 0.5 m error on h, a 20 min error

on s, and 2 lmol kg-1 for both sTA and sDIC measure-

ments to account for analytical error. We used the SD of all

samples taken in the upper 50 m depth of the water column

from the seven offshore hydrocasts as error estimates for

the sTAoffshore and sDICoffshore (see ‘‘Results’’). We then

performed another single-sample uncertainty analysis using

the NCC and NCP estimates from each tube, along with

their corresponding error estimates, to calculate the mean

NCC and NCP estimates with associated error.

Coral Reefs

123

Controls on coral community metabolism

We used principal components analysis (PCA) to explore

the relative importance of diel cycle environmental factors

and ecological community composition in controlling the

observed NCC and NCP rates. We combined NCC, NCP,

the NCC/NCP ratio, environmental parameters [photosyn-

thetically active radiation (PAR), water temperature, air

temperature, fractional time of day, precipitation], and

ecological community composition metrics (percent cover

and important ratios of major functional groups) from both

the drifts and Eulerian sampling at the SIB site to perform

the PCA (see details in ESM). Prior to PCA, all variables

were standardized to their z-scores to account for differ-

ences in unit measurements across the variables.

Results

Lagrangian drifts

Drifts lengths were variable and ranged from 200 to 850 m.

Most NCCdrift estimates were between 0 and

40 mmol C m-2 h-1, but reached extremes of -51 and

116 mmol C m-2 h-1. Even after excluding the maximum

and minimum NCC estimates (both measured on the WT),

NCCdrift estimates on the WT are more spatially heteroge-

neous than those from PS. NCCdrift estimates from PS fell in a

narrow range between 12 and 21 mmol C m-2 h-1,

possibly reflecting the similarity of drift tracks, and hence

flow characteristics, between drifts (Fig. 2). Drift NCP

estimates reached from -7 to 67 mmol C m-2 h-1,

although there are fewer NCP estimates than those of NCC.

NCPdrift estimates were more variable than NCCdrift esti-

mates at both the WT and PS regions (Fig. 2).

Neither NCCdrift nor NCPdrift shows any relationship

with PAR, as might be expected (Barnes and Lazar 1993;

Gattuso et al. 1993; Falter et al. 2012). The lack of a

metabolic rate–PAR relationship is likely due to a combi-

nation of factors. First, spatial changes in community

composition (ESM Fig. 1, 2) and other environmental

variables likely mask the influence of light variability on

coral community metabolism. Second, flow estimates (i.e.,

qx) based on constant z0 and d values measured at a single

location likely fail to represent the true depth-integrated

flow everywhere along a drift. The errors associated with

the flow characterization probably decreased our ability to

detect the influence of PAR on metabolic rates. Third,

estimates of PAR are not site-specific (i.e., we used PAR

sensor data from one location) and localized cloud cover

impacts are not well represented in the PAR data.

Offshore hydrocasts

Discrete samples collected for carbon system properties

from the offshore hydrocasts (Fig. 1b) did not show lati-

tudinal, longitudinal, or depth gradients in the upper sur-

face ocean (surface to 50 m depth). The four hydrocasts

3 4 5 6 7 9 10 12 13 15 19 22 16 18 20 21 −150

−100

−50

0

50

100

150

200

250

NC

C o

r N

CP

(m

mol

C m

−2 h

−1 )

Lagrangian Drift (#)

(a) Western Terrace (b) Penguin Spit

NCC

NCP

Fig. 2 Lagrangian drift NCC

and NCP results from, a the

Western Terrace and, b the

Penguin Spit regions. X-axis

labels denote the drift number

for reference. Error bars are ±1

SD

Coral Reefs

123

closest to the SIB site did not provide any evidence for diel

cycle variability in the offshore upper water column carbon

system chemistry. Overall, the hydrocasts provide evidence

for a relatively constant offshore upper 50 m (mean ± SD)

with sTA of 2,293 ± 3.6 lmol kg-1, sDIC of 1,982 ±

3.8 lmol kg-1, pHT of 8.01 ± 0.007, pCO2 of 436 ± 9 latm,

and XAr of 3.58 ± 0.05.

Eulerian measurements

Physical conditions

The array of physical oceanographic instrumentation was

deployed on 19 September and left in place through the end

of sampling on 25 September (Fig. 3). The tidal height, g,

varied by approximately 0.8 m on a semi-diurnal cycle

typical of Palmyra Atoll (Fig. 3a). Incoming PAR was near

zero during the night, and approached 2,000 lmol m-2 s-1

during midday (Fig. 3b). Salinity varied from 34.4 to 34.9

psu during Eulerian sampling, except for a brief intense

rainstorm beginning at 2100 hrs on 21 September that

decreased salinity to a minimum of 33.8 psu (Fig. 3c).

Variation in salinity between the tubes was negligible

(Fig. 3c). Water temperature varied from 28.2 to 30.1 �C

on 20 September and was less variable for the duration of

the sampling (Fig. 3d). Horizontal temperature gradients

between all of the tubes ranged from 0 to 0.2 �C. Vertical

temperature gradients at tubes 2 and 4 were 0 to 0.1 �C

(Fig. 3d). Thus, temperature variation in both horizontal

and vertical directions is considered negligible. Based on

the negligible horizontal salinity variation (we do not have

vertical salinity profiles), and the strong horizontal and

vertical temperature agreements, we consider the SIB site

to be well mixed.

Flow direction was generally to the west or northwest

with deviations likely due to localized flow effects

(Fig. 3e). Velocity magnitude varied from 0.05 to

0.23 m s-1 for tube sites 1–4, while velocities near tube 5

were much lower (0.007 to 0.07 m s-1) due to its location

within a branching coral colony (Fig. 3f). Significant wave

height calculated from the ADP and ADV pressure sensors

was 0.05–0.24 m. The calculated Stokes drift wave com-

ponent of velocity was insignificant (about 1 % of the

mean Eulerian velocity) and therefore was not included in

the velocity calculations. Transit time from the forereef to

the SIB site, s, varied from 47 to 274 min (Fig. 3g). Transit

times from tubes 1 and 2 to tubes 3 and 4 ranged from 2 to

8 min. The low residence time within the SIB site

09/20 09/21 09/22 09/23 09/24 09/25

−0.4

0

0.4

0

1000

2000

3434.5

35

28

29

30

0

180

360

0

0.1

0.2

0100200

η (m

)P

AR

(µm

ol m

-2 s

-1)

Sal

inity

(ps

u)T

(°C

)U

dir (

°)|U

| (m

s-1)

τ (m

in) (g)

(f)

(e)

(d)

(c)

(b)

(a)

1 2 3 4 5

Fig. 3 Physical oceanography of the SIB site over the week of

Eulerian sampling. Time series of, a tidal height, b PAR (lmol m-2 s-1)

collected from the Palmyra Atoll runway weather station, c salinity,

d water temperature, e water velocity direction (compass heading

N = 0�), f water velocity magnitude, and g transit time between the

forereef and each tube where the black dashed line is the transit time

from the forereef to start of drift 16 (magenta line in Fig. 1b). Colors

correspond with tubes 1–5 as indicated in the legend at the top of the

figure. Dashed and broken dashed lines in Fig. 3d correspond with

mid-water column and surface water temperatures, respectively, from

tubes 2 (blue) and 4 (cyan). Light blue shading shows periods of

Eulerian sampling for reference

Coral Reefs

123

precluded the use of control volume techniques to estimate

coral community metabolism (such as in Falter et al. 2008).

Biogeochemical time series

Time series of oxygen concentration and carbonate system

variables reveal large daytime (diurnal) and diel cycle

variability (Fig. 4). Oxygen concentrations ranged from

*165 to *280 lM over the course of the entire time

series and showed different patterns on each day (Fig. 4a).

The entire pHT range over the three sampling intervals was

7.95–8.10, although the maximum and minimum values

were observed on different days. pHT was elevated above

the offshore mean during sampling on 20 September,

cycled above and below the offshore mean during sampling

on 21–22 September, and moved from below the offshore

mean to above the offshore mean at approximately

1100 hrs on 25 September (Fig. 4b). Backreef pCO2

showed important differences in diel cycle timing and

magnitude between each sampling period. pCO2 was lower

than the mean offshore pCO2 during sampling on 20 Sep-

tember, showed strong diel cycle variability on 21–22

September (361–510 latm), and switched from being ele-

vated above mean offshore values to below mean offshore

values at approximately 1100 hrs on 25 September

(Fig. 4c).

The sDIC varied from approximately 1,850 to

2,000 lmol kg-1 over the course of the time series and

displayed variability in its diurnal and diel cycle patterns

between the sampling dates. On 20 September, sDIC was

lower than the offshore mean at the start of sampling and

continued to decrease throughout the day. On 21 September,

sDIC moved from being lower than offshore mean values to

elevated above offshore values at 2,000 lmol kg-1 and

100

200

3001 2 3 4 5

20 September 2012 21−22 September 2012 25 September 2012

7.9

8

8.1

300

400

500

18501900195020002050

2200

2250

2300

O2

(µM

)pC

O2

(µat

m)

sTA

(µm

ol k

g−1 )

08:00 12:00 16:00 08:00 12:00 16:00 20:00 00:00 04:00 08:00 12:00 16:00 08:00 12:00 16:003

3.5

4

4.5

pHT

sDIC

(µm

ol k

g−1 )

ΩA

rago

nite

(a)

(b)

(c)

(d)

(e)

(f)

Fig. 4 Time series of, a dissolved oxygen, b pHT, c pCO2, d sDIC,

e sTA, and f XAr collected during Eulerian sampling on 20, 21–22,

and 25 September 2012. Colors correspond with measurements from

each of the five tubes in the study area. Black lines through Fig. 4b–f

show the mean offshore measured (sTA and sDIC) and calculated

(pHT, pCO2, and XAr) values from seven hydrocasts. Dashed vertical

lines show ±1 SD from the offshore mean. Gray shading shows

sundown on 21 September 2012 to sunrise on 22 September 2012 for

reference

Coral Reefs

123

remained elevated until 0900 hrs on 22 September. On 25

September, sDIC was slightly elevated above offshore val-

ues at the beginning of sampling and decreased to

1,940 lmol kg-1 by 1300 hrs where it remained constant for

the rest of the day (Fig. 4d).

sTA did not climb above mean offshore values over the

course of the entire study period indicating that the site was a

continuous sink for TA. sTA ranges were greatest on 20

September, when sTA decreased from 2,270 to

2,230 lmol kg-1. sTA exhibited a smaller diurnal decrease

on 22 September (2,280 to 2,260 lmol kg-1). On 25 Sep-

tember, sTA decreased throughout the morning from 2,275

to 2,255 lmol kg-1, but by 1230 hrs had begun to rise again

and reached 2,275 lmol kg-1 by 1600 hrs (Fig. 4e).

XAr varied from 3.92 to 4.18 on 20 September and

showed no diurnal trend throughout the sampling window.

Elevation of XAr during daytime periods on 21 September

and 22 September, along with decreases during the night of

21–22 September, is consistent with expected changes in

coral community metabolism and resulted in diel ranges of

0.55–0.75 units. On 25 September, XAr rose from 3.2 at

0800 hrs to 3.7 at 1200 hrs. After rising to 3.8 by 1300 hrs,

it remained constant for the rest of the afternoon (Fig. 4f).

Coral community metabolism

NCC exhibited strong variability between the three Eule-

rian sampling periods (Fig. 5a). NCC increased on 20

September from 26 to 48 mmol C m-2 h-1. On 21–22

September, NCC generally varied in accordance with the

diel cycle. Highest NCC was measured at 1930 hrs on 21

September (50 mmol C m-2 h-1) and then quickly drop-

ped, reaching its lowest measured value at 2230 hrs on 21

September (14 mmol C m-2 h-1). NCC rates on the

afternoon of 22 September were slightly lower than those

on the afternoon of 21 September. On 25 September,

growth rates rose from 27 mmol C m-2 h-1 at 0815 hrs to

remain high in the afternoon, reaching a maximum of

53 mmol C m-2 h-1 at 1215 hrs.

NCP rates were large and variable between sampling

intervals (Fig. 5b). On 20 September, NCP reached its

diurnal maximum of 177 mmol C m-2 h-1 at 1145 hrs and

decreased throughout the afternoon. Diurnal maxima dur-

ing the 33-h sampling period were 90 and

119 mmol C m-2 h-1 for 21 September and 22 Septem-

ber, respectively. The coral community was net respiratory

(i.e., NCP \ 0) from 2030 hrs on 21 September until

0900 hrs on 22 September. The lowest NCP observed

during the SIB experiment was -51 mmol C m-2 h-1 at

0430 hrs on 22 September. On 25 September, NCP steadily

increased throughout the diurnal sampling period,

increasing linearly from net respiratory at the start of the

sampling period (-55 mmol C m-2 h-1 at 0815 hrs) to a

maximum NCP of 138 mmol C m-2 h-1 at 1515 hrs. We

estimate the coral community switch from net respiratory

to net productive at 1000 hrs on 25 September.

0

20

40

60

20 September 2012

(a)

21−22 September 2012 25 September 2012

−100

0

100

200 (b)

08:00 12:00 16:00−2

−1

0

1

2

NC

C (

mm

ol C

m−

2 h−

1 )N

CP

(m

mol

C m

−2 h

−1 )

NC

C/N

CP

(c)

08:00 12:00 16:00 20:00 00:00 04:00 08:00 12:00 16:00 08:00 12:00 16:00

Fig. 5 Time series of mean

a NCC, b NCP, and c NCC/

NCP averaged across tubes 1–4

during Eulerian sampling. Error

bars on NCC and NCP show ±1

SD from the mean. Black dots

on 25 September 2012 show the

results of drift 16, which

transited through the Eulerian

sampling site. Error bars on the

drift NCC and NCP are ±1 SD.

Gray shading shows sundown

on 21 September 2012 to

sunrise on 22 September 2012

for reference

Coral Reefs

123

The NCC/NCP ratio reflects the balance between inor-

ganic and organic carbon production. The NCC/NCP ratio

was calculated for all instances with significant NCP rate

measurements (p \ 0.05) in order to avoid extreme NCC/

NCP estimates based on near-zero NCP (Fig. 5c). The

NCC/NCP ratio was nearly constant on 20 September

(0.17–0.37). The NCC/NCP ratio was more variable on

21–22 September, ranging from a maximum of 1.87 near

1200 hrs on 21 September to a minimum of -0.74 at

2230 hrs on 21 September. The change in sign of the NCC/

NCP ratio is attributable to positive NCC and negative

NCP during the night hours. During the morning and

afternoon of 22 September, NCC/NCP ratio varies from

0.32 to 0.82. On 25 September, NCC/NCP ratio was neg-

ative in the morning hours with a diurnal minimum of

-1.12 reflective of the positive NCC and early morning

negative NCP. NCC/NCP ratio reached a maximum of 0.83

at 1115 hrs and slowly decreased through the afternoon,

reaching a final value of 0.34 at 1615 hrs on 25 September.

NCC and NCP rates integrated over a full diel cycle may

reveal more about coral community metabolism than the

maximum and minimum of a time series. We integrated

NCC and NCP over the first and last 24 h of the time series

on 21–22 September. NCC integrated over the diel cycle

was 684 and 664 mmol C m-2 for the first and second 24-h

periods, respectively. The estimates appear close to each

other, suggesting smaller levels of variability for daily-

integrated NCC. NCP integrated over the diel cycle was

240 and 385 mmol C m-2 for the first and second 24-h

periods, respectively. The NCP estimates for each 24-h

period diverge from one another much more than the NCC

estimates, possibly due to variable PAR and the close

relationship between NCP and PAR during the Eulerian

sampling.

We used the daily-integrated NCC and NCP estimates to

calculate daily-integrated NCC/NCP ratios. The daily-

integrated NCC/NCP ratio was 2.85 for the first 24-h per-

iod and 1.73 for the second 24-h period on 21–22 Sep-

tember. These ratios are higher than most of the hourly

NCC/NCP ratios since NCC remained positive throughout

the duration of the sampling period, which led to large

daily-integrated NCC estimates.

Air–sea CO2 fluxes

We used the integrated rate estimates of NCC and NCP to

compute the net flux of CO2 across the coral community.

We adopted the molar ratio of W = 0.6 to estimate the CO2

released by calcification to calcium carbonate precipitated

(Ware et al. 1992; Frankignoulle et al. 1994). The inte-

grated CO2 flux estimate for the first 24-h of the 21–22

September sampling period was 170 mmol C m-2, and for

the second diel cycle was 14 mmol C m-2. Both integrated

CO2 flux estimates were positive, indicating that the reef is

a net source of CO2 to the atmosphere.

We also calculated daily-integrated CO2 fluxes using

measured pCO2 at the SIB site in order to independently

evaluate our net CO2 flux estimates derived from NCC and

NCP. We used the same atmospheric pCO2, gas transfer

velocity parameterization, and wind speed data as with our

calculations of F, the net air/sea gas exchange term in the

NCP calculations. Using measured pCO2, the CO2 flux

estimates for the first and second diel cycles of the 21–22

September sampling period were both 2 mmol C m-2.

Positive CO2 fluxes derived using both metabolic rate

estimates and measured pCO2 enhance our confidence that

the reef was a net source of CO2 during sampling on 21–22

September. However, the discrepancies in the magnitudes

of the fluxes highlight the importance of more direct, as

opposed to parameterized, measurements of air/sea gas

exchange across reef environments. More constrained

estimates of air/sea gas fluxes will improve our under-

standing of the potential of air/sea gas exchange to mod-

ulate diel cycle biogeochemical extremes in reef

environments.

Controls on community metabolism

The first two principal components (PC) were able to

explain 52 % of the observed variability (Fig. 6). PC1

explained 29.3 % of the data, and its strongest loadings (by

absolute value) were the ratio of calcifiers to non-calcifiers,

hard coral (percent cover), and CCA (percent cover). PC2

explained 22.3 % of the data set, and its strongest loadings

were PAR, NCP, and water temperature (see ESM Table

S2 for PC1 and PC2 loadings for all variables).

Discussion

The Lagrangian and Eulerian data sets taken together

provide a more complete picture of coral community

metabolism on Palmyra Atoll. The drifts, all performed

during daylight hours, show a spatially variable landscape

with respect to both NCC and NCP. Our inability to detect

any relationship between NCCdrift and NCPdrift and PAR or

time of day is likely due to the confounding effects of

changing ecological community both within a drift and

between drifts, as well as the absence of in situ PAR

measurements. While drifts provide spatially expansive,

robust metabolic estimates, the difficulties of accurately

characterizing the flow (i.e., qx) and the natural noise in the

geochemical signals (sDIC and sTA) result in large error

estimates. Future Lagrangian studies should consider more

advanced techniques for accurately characterizing the

Coral Reefs

123

boundary layer velocity profile. This might include

downward facing current profilers mounted on the drifters.

Comparing the Eulerian and Lagrangian estimates of

coral community metabolism is difficult because of a lack

of coordinated measurements. Mean Eulerian estimates of

coral community metabolism tended to be higher than

Lagrangian estimates at the SIB site, but only one drift

(drift 16) was conducted during Eulerian sampling at the

SIB site (1200–1300 hrs, 25 September; Fig. 5). Neither

NCCdrift nor NCPdrift was significantly different from

Eulerian NCC or NCP estimates at this time (Student’s

T test, p [ 0.05). This result is likely due to the high error

associated with drift estimates of community metabolism.

Without additional co-located measurements, we cannot

say anything definitive about methodological bias between

the Lagrangian and Eulerian approaches. We do note,

however, that the close alignment of the Eulerian and

Lagrangian NCC/NCP ratio estimates (which are inde-

pendent of flow estimates) suggests that the flow estimates

are primarily responsible for observed differences in mean

metabolic estimates.

The diel cycle estimates of NCC and NCP from the

Eulerian setup provide insight into the daily metabolic

variability of a single coral community. We observed dif-

ferences in the timing and patterns of NCC and NCP during

the four daytime periods of 20, 21, 22, and 25 September.

Both our NCC and NCP estimates over the full duration of

Eulerian observation show greater amplitude in variability

than many previously published metabolic rates (published

metabolic rates reviewed by Andersson and Gledhill 2013;

Teneva et al. 2013). Yet, our measured values are not

without parallel. Summer NCC and NCP estimates from

Ningaloo Reef in western Australia have been shown to be

approximately equal to those presented here (Falter et al.

2012). High temporal resolution metabolic estimates from

Heron Island, Great Barrier Reef, Australia show daily

NCC ranges from *40 to -20 mmol C m-2 h-1 and NCP

ranges from -80 to 130 mmol C m-2 h-1 (McMahon

et al. 2013). Many field-based estimates of coral commu-

nity metabolism are made on a sub-daily, but not hourly,

basis (Shamberger et al. 2011; Shaw et al. 2012; Teneva

et al. 2013). We emphasize that the dearth of high-reso-

lution (sub-hourly to hourly) estimates of NCC and NCP

across coral reef field studies likely obscures much of the

natural diel cycle variability in coral reef community

metabolism by averaging over longer time-scales.

PCA was used to qualitatively explore the balance

between diel cycle environmental forcing and ecological

community composition in setting the observed coral

metabolism and biogeochemistry. We interpret PC1 to

reflect the ecological community composition and PC2 to

reflect the diel cycle environmental forcing based on the

PC loadings of the original variables. NCC and NCP fall

closer to PC2, suggesting that diel cycle forcing exerts the

greatest control on the magnitudes of NCC and NCP. The

NCC/NCP ratio falls much closer to PC1, indicating that

the ecological community composition is the most impor-

tant control on the balance between organic and inorganic

−0.45 −0.35 −0.25 −0.15 −0.05 0.05 0.15 0.25 0.35 0.45

−0.5

−0.4

−0.3

−0.2

−0.1

0

0.1

0.2

0.3

0.4

0.5

NCC

NCP

NCC/NCP

FractionalDay

Water TemperatureAir Temperature

PAR

Precipitation

Hard Coral

MacroalgaeCCA

Halimeda

Turf Algae

C/NCHC/MA

Component 1

Com

pone

nt 2

Fig. 6 PC loadings of all

metabolic, environmental, and

ecological data on PC1 and 2.

Ecological functional group

units are in percent cover. C/NC

is the ratio of calcifiers to non-

calcifiers and HC/MA is the

ratio of hard coral to non-

calcifying macroalgae

Coral Reefs

123

community metabolism. Given the importance of the NCC/

NCP ratio in shaping the carbonate system by controlling

the relative fluxes of TA and DIC coming from the benthic

community (Andersson and Gledhill 2013), our analysis

demonstrates that ecological community composition is the

primary determinant of coral reef biogeochemistry on a

relatively undisturbed reef. This result suggests reef bio-

geochemistry is likely to be responsive to human behaviors

that alter community composition on the reef.

Additional well-designed field studies with co-located

biogeochemical and ecological measurements, as well as

mesocosm studies, are crucial for isolating the biogeo-

chemical and metabolic signatures of different functional

groups within the coral community under a variety of

environmental conditions. These experiments will help

establish attribution of community metabolism and bio-

geochemistry as well as provide further insight into the

competitive dynamics of coral reef ecology. Ultimately,

more targeted functional-level studies will greatly enhance

predictive capabilities for how coral reef ecosystems will

respond to or potentially buffer forcing from OA and cli-

mate change.

Acknowledgments This manuscript benefitted greatly from the

comments of three anonymous reviewers. Helpful conversations with

Kevin Arrigo, Andreas Andersson, Stephen Monismith, Hans DeJong,

Dan Urban, and Matz Haugen also greatly improved this manuscript.

We thank Claire Zabel for her field assistance. We thank The Nature

Conservancy for logistical support on Palmyra Atoll as well as the US

Fish and Wildlife Service (US FWS) for granting research access.

This research was funded by support from the Gordon and Betty

Moore Foundation to Robert B. Dunbar. This research was conducted

under a permit from the US FWS. This is Palmyra Atoll Research

Consortium contribution number 0109. Data from this study have

been deposited at the NOAA National Oceanographic Data Center

and can be obtained there.

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