Marine Pollution Bulletin 183 (2022) 114054

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Marine Pollution Bulletin

journal homepage: www.elsevier.com/locate/marpolbul

Effects of watershed land use on coastal marine environments: A multiscale

exploratory analysis with multiple biogeochemical indicators in fringing
coral reefs of Okinawa Island
Takashi Sakamaki a, b, *, Akiko Morita a, b, c, Shouji Touyama b, d, Yasushi Watanabe e,
Shouhei Suzuki b, Takashi Kawai b, f
a
Department of Civil and Environmental Engineering, Tohoku University, Sendai 980-8579, Japan
b
Department of Civil Engineering and Architecture, University of the Ryukyus, Okinawa 903-0213, Japan
c
Oriental Consultants Co., Ltd., Tokyo 151-0071, Japan
d
Stargate Entertainment, Okinawa 905-0005, Japan
e
GIS Okinawa Laboratory, Okinawa 901-0401, Japan
f
Tokyo Kyuei Co., Ltd., Tokyo 101-0032, Japan

A R T I C L E I N F O A B S T R A C T

Keywords: The analytical spatial scale and selection of biogeochemical indicators affect interpretations of land-use impacts
Land–sea connection on coastal marine environments. In this study, nine biogeochemical indicators were sampled from 36 locations of
Multiscale buffers coral reefs fringing a subtropical island, and their relationships with watershed land use were assessed by spatial
Primary production
autoregressive models with spatial weight matrixes based on distance thresholds of a few to 30 km. POM-relevant
Anthropogenic nitrogen
Stable isotopes
indicators were associated with agricultural and urban lands of watersheds within relatively small ranges (6–14
Coral reef conservation km), while the concentrations of inorganic nutrients were associated with watersheds within 20 km or more. The
macroalgal δ15N showed a strong relationship with agricultural lands of watersheds within 7 km and urban/
forest lands of watersheds within 24 km. These results demonstrate significant effects of land use on the coral reef
ecosystems of the island, and the importance of appropriate combinations of analytical scales and biogeo­
chemical indicators.

1. Introduction ecosystems, such as chemical environments (e.g., McClelland et al.,

The environments and biogeochemical processes in coastal marine
ecosystems are significantly impacted by land-derived nutrients and
organic matter which originate from both natural (e.g., forest vegetation
and soils) and anthropogenic (e.g., fertilizer, sewage, and organic waste)
sources (e.g., Lapointe and Clark, 1992; Nixon, 1995; Galloway et al.,
2004; Álvarez-Romero et al., 2014, 2016). Coral reefs, characterized by
remarkable biodiversity, are highly susceptible to, and affected by,
environmental changes associated with anthropogenic activities (e.g.,
Dutra et al., 2021; Pan et al., 2021). Both the quantity and composition
of organic matter and nutrients transported through riverine systems are
affected by watershed environments which are substantially modified
by human activities (e.g., Carpenter et al., 1998; Sakamaki and
Richardson, 2011, 2013; Manning et al., 2020). Inputs of land-derived
organic matter and nutrients further impact various aspects of coastal
1997; Sakamaki et al., 2010; Morita et al., 2017), biogeochemical pro­
cess (e.g., Sakamaki and Richardson, 2009), community structure (e.g.,
Deegan et al., 2002; Sakamaki and Richardson, 2008a; Garmendia et al.,
2011), productivity (e.g., Schmidt et al., 2012; Silva et al., 2022), and
food web dynamics (e.g., Tewfik et al., 2005; Martinetto et al., 2006;
Sakamaki and Richardson, 2008b). Therefore, to understand the impacts
of anthropogenic activities on coastal ecosystems and enhance the
management of these environments, materials transported from water­
sheds to coastal environments must be carefully evaluated (e.g., Brodie
et al., 2012; Carlson et al., 2019, 2021; Pearson et al., 2021).
Coral reefs have the highest biodiversity of marine ecosystems
(Connell, 1978; Hoegh-Guldberg, 1999; Roberts et al., 2002). However,
the deterioration of coastal ecosystems, including coral reefs, due to
many stressors including rising seawater temperature, overfishing,
coastal development, and pollution from land, has been documented in

* Corresponding author at: Department of Civil and Environmental Engineering, Tohoku University, Sendai 980-8579, Japan.
E-mail address: takashi.sakamaki.a5@tohoku.ac.jp (T. Sakamaki).

https://doi.org/10.1016/j.marpolbul.2022.114054
Received 11 April 2022; Received in revised form 13 August 2022; Accepted 15 August 2022
Available online 22 August 2022
0025-326X/© 2022 Elsevier Ltd. All rights reserved.
T. Sakamaki et al. Marine Pollution Bulletin 183 (2022) 114054

many regions over the last few decades (e.g., Bellwood et al., 2004;
Wilson et al., 2006; Mora et al., 2011; Reimer et al., 2015). Based on a
series of analyses of a three-decadal data set from Florida, Lapointe et al.
(2019) demonstrated that the increase of anthropogenic nitrogen inputs,
as well as rising nitrogen:phosphorus stoichiometry, possibly increased
the risk of coral bleaching and their mass mortality. These situations
highlight the urgent need to design effective and integrated conserva­
tion management plans for coral reef ecosystems which include the
management of watershed environments.
Many field-based studies have been conducted on the effects of river-
transported materials on biogeochemical processes in coastal marine
systems. Based on data collected from multiple locations along transects,
these studies demonstrated that the quantity of materials declined from
the river mouth towards offshore locations (e.g., Lapointe and Clark,
1992; Goñi et al., 1998; Washburn et al., 2003). Spatiotemporal varia­
tions in biogeochemical conditions near river mouths are often
described using process-based models, that deductively explain relevant
processes, such as advection, diffusion, and biological reactions, and can
be adequately predicted (e.g., Kourafalou et al., 1996; Fennel et al.,
2011; Wolff et al., 2018). These approaches, that is, the measurement
along a transect and process-based modeling, are usually effective when
considering the effects of small numbers of specific watersheds/rivers.
Conversely, these approaches are limited when many small rivers
entering coastal marine systems and major rivers cannot be defined a
priori. Under such conditions, to properly evaluate the effects of wa­
tersheds on coastal marine systems, a spatial range within which wa­
tersheds influence a coastal marine system must first be explored. A
limited number of studies have compared different spatial scales to
assess land-sea connections or explore spatial ranges of land-use effects
in coastal marine systems (Diefenderfer et al., 2009; Abaya et al., 2018;
Beck et al., 2019), while river studies have proposed concrete method­
ologies and applied multiscale analyses on the relationships between
river-water chemistry and watershed land use (e.g., Mwaijengo et al.,
2020; Wu et al., 2021; Hanna et al., 2021). Effective spatial ranges for
the analysis of land-sea connections or evaluation methodology have not
been reported in coastal marine studies.
Many land-derived materials are involved in chemical and/or bio­
logical reactions, and thus, some are transformed in coastal marine
systems; for instance, dissolved inorganic nutrients from watersheds can
be rapidly converted into organic particles by coastal primary pro­
biogeochemical indicators for assessing the impacts of land use on
coastal marine environments and 2) estimate spatial ranges within
which land-derived materials affect the local coastal marine environ­
ments of a subtropical island with fringing coral reefs. The findings of
this study will provide novel insights into the impacts of terrestrial
human activity on biogeochemical processes in coastal environments.
Our results will also highlight the responsibilities of stakeholders that
influence terrestrial environments, and their impacts on coastal envi­
ronments, and facilitate better environmental management by consid­
ering land-sea connections.
2. Materials and methods
In this study, 36 locations on coral reef slopes of a subtropical island
in southwestern Japan were sampled, and nine biogeochemical in­
dicators of organic matter and nutrients were examined. The relation­
ships between the biogeochemical indicators and GIS-based watershed
land-use data were analyzed at various spatial scales.
2.1. Study sites and field sampling
Field surveys were conducted in fringing coral reefs of Okinawa Is­
land (26.1–26.9◦ N and 127.6–128.3◦ E) in the western Pacific (Fig. 1).
Sample collection was conducted between June and August 2011 as part
of an ecological survey of the island (Suzuki et al., 2018). The island
covers an area of 1206 km2 and is partitioned into small watersheds (≤
52 km2). It has relatively high levels of precipitation, approximately
2000 mm yr− 1 and 100–280 mm mo− 1, compared with the global
average of annual precipitation (approximately 990 mm yr− 1). To more
clearly detect the effects of material inputs from watersheds, sampling
was conducted in summer which has relatively higher levels of precip­
itation, > 200 mm mo− 1, than other seasons, and was therefore expected
to show seasonally larger inputs of land-derived materials due to greater
fluvial transport. Sampling was avoided during or immediately after (<3
d) heavy rainfall events. The island hosts a population of 1.2 million
people, most of which inhabit urbanized areas that spread from the
south to the center of the island. The central to northern parts of the
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diverse forms of organic matter). This complicates their assignment to

riverine/oceanic origins and hampers the detection of land-derived
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materials in coastal marine systems. To overcome these limitations HI

and detect inputs of land-derived materials in coastal marine systems,
biogeochemical indicators must be carefully selected by comparing
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multiple potential indicators in terms of their detectability in coastal 䖃 䖃

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mental sciences for distinguishing land- and marine-derived materials
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(e.g., Cloern et al., 2002; Canuel and Hardison, 2016; Howe et al., 2017), Forest
may serve as useful indicators and hence their applicability should be Agriculture
evaluated. Furthermore, the entry locations of land-derived materials
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agement tactics. Exploratory analyses with statistical approaches would 䖃

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derived material inputs. This approach is particularly relevant when 䖃
the locations of major inputs are not definable a priori and deductive
process-based models cannot provide reliable estimations of spatial Fig. 1. Map showing the land-use types and sampling locations (black dots)
distributions of land-derived materials in coastal marine areas. from which coral reefs were sampled around Okinawa Island, south­
The objectives of this study are to: 1) highlight effective western Japan.

2
T. Sakamaki et al. Marine Pollution Bulletin 183 (2022) 114054

island are mountainous (altitudes up to 500 m) and dominated by sub­ distance between tips of topographical features was utilized for the
tropical evergreen forests. Agricultural land use occurs predominantly in calculation.
the south of the island and is scattered over the other parts. The farmed The coastline enclosure (XE) was determined using the GIS at each
lands mainly produce sugarcane, fruits (e.g., pineapples, flat lemons), sampling location based on spatial scales (dE_range) of 5, 10, 15, 20, and
vegetables, and cut flowers. 30 km. The enclosure was defined as the angle between two vectors from
Twelve sites comprising three sampling locations at intervals of the sampling location to the intersection of the coastline which crosses a
approximately 2–5 km were visited during the surveys, thereby yielding circle with a radius equal to the dE_range (Fig. 2).
36 sample locations. All samples were collected on coral reef slopes at
depths of 7 ± 1 m. According to previous studies, the species diversity of
2.4. Data analysis
coral reefs is generally highest at a depth of approximately 10 m (e.g.,
Harborne et al., 2006; Williams et al., 2013). Therefore, the 7 m sam­
Principal component analysis (PCA) was used to analyze biogeo­
pling depth was selected to evaluate the chemical environment in this
chemical characteristics in the sampling locations. Pearson's correlation
high biodiversity system while facilitating sampling by SCUBA diving.
analysis was then utilized to assess relationships between different
All sampling locations were accessed using a boat, and three 100-mL
biogeochemical indicators.
near-bottom seawater samples were collected by SCUBA divers at each
To evaluate the effects of coastline enclosure and watershed land use
location to analyze inorganic nutrients and dissolved organic carbon
on coastal chemical environments at varying spatial scales, the data
(DOC). At each sampling location, the most diverse taxa of benthic
were analyzed with spatial autoregressive (SAR) models (LeSage and
macroalgae possible were collected during the approximately 30–60
Pace, 2009). The base model was as follows:
min of diving. In addition, 20 L of near-surface water was collected at
each location to evaluate the suspended particulate organic matter. Y = ρW S Y + βE XE + βLl WL XLl + βI XE WL XLl + ε (1)

2.2. Sample processing and chemical analysis where Y is a biogeochemical indicator analyzed for a sampling location
(i.e., POC, Chl. a, C:NPOM, δ13CPOM, DOC, NH+ 3−
4 , NO2 + NO3 , PO4 , or
− −
15
The near-bottom water samples were immediately filtered using δ NMA), WS and WL are spatial weights matrices, XE is the coastline
0.45-μm membrane filters (Merck Millipore HA). These samples were enclosure based on the sampling location, XLl is the area covered by a
used to determine the concentrations of ammonium (NH+ 4 ), nitrite + land-use type (i.e., l = agricultural, forest, or urban land) in each
nitrate (NO−2 + NO−3 ) nitrogen, and phosphate (PO3− 4 ) through an auto watershed, ε represents an error term, ρ denotes the SAR parameter, βE is
analyzer (QUAATRO, BLTEC). The DOC concentration was measured a parameter for the coastline enclosure, βLl represents a parameter for
using a TOC analyzer (SHIMAZU, TOC-V, Tokyo, Japan). the area of the land use type (l), and βI is a parameter for the effect of
To quantify suspended particulate organic matter (POM) in the interaction between XE and XLl. The area (XLl) of each land-use type in a
seawater and observe the relative contribution from different origins (e. watershed (i.e., agricultural, forest, and urban land) was separately
g., marine phytoplankton and terrestrial vegetation) to the bulk POM, interpolated in the model.
four variables were determined for each sampling location; particulate The WS was an n × n matrix, in which n represented the number of
organic carbon (POC), chlorophyll a (Chl. a), ratio of carbon to nitrogen sampling locations (36). This matrix was utilized to generate a weighted
(C:NPOM), and carbon stable isotope ratio (δ13CPOM). The near-surface
water from each sampling location was filtered through four glass
fiber filters (Whatman GF/F), that were precombusted at 450 ◦ C for 2 h
to collect fine particles suspended in the seawater. Two of these filter
samples were placed in brown glass vials containing 5 mL of N,N-
dimethylformamide (DMF) and stored in a freezer at − 30 ◦ C for sub­
sequent analysis of Chl. a. The concentration of Chl. a in each DMF
extract was determined using a fluorometer (Turner Designs TD-700).
The remaining two filter samples were acidified to eliminate carbon­
ate, and analyzed to determine the concentrations of POC, C:NPOM, and
δ13CPOM.
The nitrogen stable isotope ratio of macroalgae (δ15NMA) was
measured to assess the input of anthropogenic nitrogen in the sampling
dE_Range for XE
locations (McClelland et al., 1997; Bannon and Roman, 2008; Abaya or
et al., 2018). Macroalgae in the samples were identified at the genus or
family level. Taxa identified across sampling locations were dried at
dL_Range for XL
60 ◦ C and utilized for analysis of the nitrogen stable isotope ratio
(δ15NMA). The carbon and nitrogen contents and corresponding stable
isotope ratios of suspended particles and macroalgae were determined
using an isotope ratio mass spectrometer system (Delta V Advantage +
FLASH 2000, Thermo Scientific).

2.3. GIS-based watershed land use and coastline enclosure calculations

The entire island was partitioned into 2238 watersheds using a
geographic information system (GIS; SuperMap Japan Co., Ltd), and the
areas (XLl) occupied by three different land-use types (l: agricultural,
forest, and urban lands) in each watershed were estimated (Fig. 1,
Fig. S1). The distances between sampling locations (dS) and between
these locations and river mouths (dL) in all watersheds were also
determined using the GIS. In measuring distances, a direct approach was
preferred, but in some cases, because of geomorphological obstacles, the
Fig. 2. Schematic illustration of the methods used for calculation of the
coastline enclosure and watershed land use at a given spatial scale. The
coastline enclosure (XE) is the angle between two lines within a length scale
(dE_Range) from a sampling location to the intersection with the coastline. To
calculate the area covered by each land-use type influencing the chemical
environment in a sampling location, the areas of each land use type in all
watersheds (XL) within the dL_Range (river-mouths of which are indicated by the
solid circles) were summed using the spatial weights matrix, WL in the spatial
autoregressive models (Eq. (1)).

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T. Sakamaki et al. Marine Pollution Bulletin 183 (2022) 114054

average of Y for neighboring sampling locations and to determine the Table 1

effects of spatial autocorrelations at different spatial scales. The element Summary of results for the nine biogeochemical indicators measured in 36
of the WS, wSij, can be expressed as follows: sampling stations.
Indicators Quantiles
wSij = 0 if dSij > dS Range
5% 25 % 50 % 75 % 95 %
/
wSij = 1 ni if dSij ≤ dS Range POC (μmol L− 1) 3.9 4.9 5.8 7.4 16.0
Chl.a (μg L− 1) 0.02 0.03 0.04 0.08 0.14
where dSij is the distance between sampling location i and a neighboring C:NPOM (at molar) 5.8 6.1 6.6 7.1 8.4
δ13CPOM (‰) − 21.9 − 21.1 − 20.4 − 19.6 − 16.9
location j, dS_Range represents the assumed range within which sampling
DOC (μmol L− 1) 67 69 72 77 104
locations can influence location i, and ni is the number of neighboring PO3− (μmol L− 1) 0.06 0.09 0.11 0.15 0.24
4
sampling locations within the dS_Range associated with sampling location NH+4 (μmol L− 1) 0.16 0.22 0.26 0.32 0.43
i. NO−2 + NO−3 (μmol L− 1) 0.25 0.41 0.49 0.73 0.96
Relatedly, the WL was an n × m matrix in which m represented the DIN:PO3−
4 (at molar) 4.0 5.1 6.4 8.0 14.8
δ15NMA (‰) 1.0 1.6 2.5 3.5 4.5
number of watersheds (2238). This matrix was used to sum the XLl
values of watersheds within the dL_Range of each sampling location and to
evaluate the effects of watershed land use on sampling locations at
different spatial scales. The element of the WL, wLik, can be expressed as
follows:
wLik = 0 if dLik > dL Range

wLik = 1 if dLik ≤ dL Range

where dLik is the distance between sampling location i and a river mouth
in watershed k and dL_Range is the assumed range within which the
encompassed watersheds affect the Y of sampling location i.
Different spatial scales were explored to evaluate the associated ef­
fects of the coastline enclosure and watershed land use on each
biogeochemical indicator for the sampling locations by comparing
models that incorporated diverse combinations of dE_Range, dS_Range, and
dL_Range. These included six levels of the dE_Range between 5 and 30 km, 10
levels of the dS_Range between 5.5 and 30 km, and 17 levels of the dL_Range
between 4 and 30 km. Further, we tested the model presented in Eq. (1)
and eight models in which single/combinations of explanatory variables
were dropped from the full model. The truncated models included all
possible combinations with one to three of the four explanatory vari­
ables involved in Eq. (1), except for models including the interaction
term, XEWLXLk, but without one or two of the main effect terms, XE and/
or WLXLk. Overall, there were 7650 models with different spatial scales
and explanatory variable combinations for each biogeochemical indi­
cator vs. land-use type combination. These included five levels in the Fig. 3. Plot showing the results of the principal component analysis of chemical
dE_Range, 17 levels in the dS_Range, and 10 levels in the dL_Range as well as environments in the sampling locations. Refer to Fig. 1 for the abbreviations of
nine combinations of the explanatory terms. sampling locations. POC: particulate organic carbon, Chl. a: chlorophyll a, C:
Statistical analyses were performed using R version 3.6.1 (R Core NPOM: the ratio of carbon to nitrogen of suspended particulate organic matter
Development Team). For the SAR models, the parameters were esti­ (POM), δ13CPOM: carbon stable isotope ratio of POM, DOC: dissolved organic
3−
mated using the maximum likelihood method. All values for dependent carbon, NH+ 4 : ammonium, NO2 + NO3 : nitrite + nitrate, PO4 : phosphate.
− −

and explanatory variables were subtracted from the mean and divided
by the standard deviation for standardization. This enabled a compari­
son of the explanatory variables using standardized coefficients. The
Akaike information criterion (AIC) was used to compare models of each
relationship between biogeochemical indicator vs. land use, and the
model with the lowest AIC value for each was selected. Pseudo R2 values
were calculated using the pR2 function of the “pscl” package for R.
3. Results
All sampling locations were categorized into the oligotrophic state
based on the concentrations of Chl. a and inorganic nutrients (e.g.,
Nasrollahzadeh et al., 2008), although the composition of the chemical
constituents varied across locations (Table 1, Fig. S2). In the PCA, data
for the sampled locations produced a PC1 based on the concentrations of
POC and Chl. a and a PC2 which was associated with inorganic nutrient
concentrations (Fig. 3). The POC was positively correlated with Chl. a (r
correlation with NH+ 4 (r = 0.39 and p = 0.019) and a negative correla­
tion with C:NPOM (r = − 0.35 and p = 0.038).
The SAR model predictions varied for the biogeochemical indicators;
the AIC and pseudo R2 values of the best models produced ranges of
48.9–104.1 and 0.06–0.64, respectively (Table 2). Estimated spatial
variations of the POC and Chl. a concentrations from the models were
better than those of the other indicators.
The POC, Chl. a, C:NPOM, and DOC exhibited strong positive spatial
autocorrelations (i.e., high ρ values) when dS_Range values of ≤12 km
were used in the models (Table 2 and Fig. 4a). At higher dS_Range values of
24–30 km, the concentrations of inorganic nutrients showed negative
spatial autocorrelations overall.
The POC and Chl. a concentrations increased as the coastline
enclosure increased for the lowest dE_Range of 5 km (Table 2 and Fig. 4b).
In contrast, C:NPOM and DOC showed weak negative relationships with
the coastline enclosure for this dE_range. In general, the NH+
4 , NO2 + NO3 ,
− −

= 0.65 and p < 0.001), δ13CPOM (r = 0.46 and p = 0.004), and δ15NMA (r 15
and δ NMA data were positively related to the coastline enclosure for
= 0.43 and p = 0.008). Chl. a also displayed a positive correlation with dE_Range values of 10–20 km. Relatedly, the PO3− 4 was negatively related
δ13CPOM (r = 0.48 and p = 0.003). The NO−2 + NO−3 exhibited a positive to the coastline enclosure for dE_range values of 10–30 km.

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T. Sakamaki et al. Marine Pollution Bulletin 183 (2022) 114054

Table 2
Estimated parameters of the spatial autoregressive models for the effects of land-cover and coastline enclosure on biogeochemical indicators.
Indicator Land-use type Spatial autocorrelation (ρ) Coastline enclosure (βE) Land use (ВL) Interaction (ВI) AIC Pseudo R2

POC Agriculture 0.62 ± 0.08*** (7) 0.27 ± 0.07** (5) 0.21 ± 0.08** (6) 0.37 ± 0.09*** 48.9 0.64
Forest 0.78 ± 0.08*** (7) 0.31 ± 0.09** (5) − 0.23 ± 0.11 (6) 0.20 ± 0.06** 53.7 0.59
Urban 0.75 ± 0.09*** (7) 0.28 ± 0.09** (5) − 0.01 ± 0.09 (24) − 0.17 ± 0.08 61.1 0.51
Chl.a Agriculture 0.71 ± 0.10*** (5.5) 0.21 ± 0.09* (5) 0.15 ± 0.09 (8) 66.7 0.44
Forest 0.76 ± 0.09*** (5.5) 0.20 ± 0.09* (5) 67.3 0.41
Urban 0.82 ± 0.09*** (12) 0.20 ± 0.08* (5) 0.15 ± 0.08 (14) 0.31 ± 0.10** 60.0 0.53
C:NPOM Agriculture 0.65 ± 0.11*** (5.5) − 0.24 ± 0.10* (5) − 0.28 ± 0.12** (30) 69.2 0.41
Forest 0.80 ± 0.10*** (5.5) − 0.17 ± 0.10 (5) 72.8 0.36
Urban 0.78 ± 0.10*** (5.5) − 0.16 ± 0.10 (5) − 0.04 ± 0.10 (20) − 0.21 ± 0.09* 71.7 0.41
δ13CPOM Agriculture − 0.43 ± 0.17* (24) 0.62 ± 0.16** (20) 0.98 ± 0.21*** (12) 0.52 ± 0.17** 92.3 0.21
Forest 0.35 ± 0.15* (12) − 0.29 ± 0.15 (4) 101.1 0.08
Urban 0.37 ± 0.15* (7) 101.5 0.06
DOC Agriculture 0.70 ± 0.11*** (12) − 0.19 ± 0.11 (5) 81.7 0.27
Forest 0.70 ± 0.11*** (12) − 0.19 ± 0.11 (5) 81.7 0.27
Urban 0.64 ± 0.11*** (12) − 0.36 ± 0.14* (5) 0.47 ± 0.20* (4) − 0.48 ± 0.30 79.6 0.33
PO3−
4 Agriculture − 0.73 ± 0.18*** (30) − 0.68 ± 0.17*** (30) 0.50 ± 0.16*** (24) 1.18 ± 0.22*** 85.6 0.27
Forest − 0.31 ± 0.15* (15) 0.19 ± 0.15 (20) − 0.64 ± 0.17*** 95.2 0.15
Urban − 0.34 ± 0.18 (30) − 0.31 ± 0.17 (10) − 0.03 ± 0.19 (24) 0.60 ± 0.19** 99.4 0.14
NH+
4 Agriculture − 0.67 ± 0.12*** (30) 0.50 ± 0.12*** (15) 82.6 0.26
Forest − 0.71 ± 0.10*** (30) 0.51 ± 0.12*** (20) − 0.29 ± 0.10* (20) − 0.36 ± 0.11** 70.6 0.42
Urban − 0.68 ± 0.10*** (30) 0.60 ± 0.10*** (15) 0.41 ± 0.11*** (22) 0.44 ± 0.11*** 68.9 0.44
NO−2 + NO−3 Agriculture − 0.34 ± 0.21 (24) 0.48 ± 0.21* (10) − 0.38 ± 0.21 (14) − 0.43 ± 0.25 104.1 0.09
Forest − 0.26 ± 0.16 (12) − 0.12 ± 0.15 (30) 0.58 ± 0.16** (26) 0.58 ± 0.17** 95.0 0.18
Urban − 0.39 ± 0.21 (24) 0.47 ± 0.21* (10) − 0.35 ± 0.17* (4) − 0.41 ± 0.30 102.8 0.10
δ15NMA Agriculture 0.44 ± 0.15** (15) 0.02 ± 0.12 (5) 0.35 ± 0.16* (7) 0.51 ± 0.15*** 85.8 0.27
Forest − 0.41 ± 0.16* (30) 0.66 ± 0.13*** (10) − 1.14 ± 0.16*** (24) 0.49 ± 0.14*** 69.8 0.43
Urban 0.37 ± 0.13** (10) 0.55 ± 0.15** (24) − 0.23 ± 0.16 88.2 0.23

The results are shown as mean ± SE of coefficients for the model, Y = ρWSY + βEXE + βLWLXLk + βIXEXL. For each biogeochemical indicator, the model with the lowest
AIC in model comparisons, including reduced models and multiple spatial scales of explanatory variables, is shown. In addition, for each biogeochemical indicator,
three models with different land-cover effects (i.e., agriculture, forest, and urban) are shown. The value in parentheses indicates the estimated spatial scale at which the
effect of the explanatory variable is maximized. The asterisks indicate the level of significance of the coefficients; ***p < 0.001, **p < 0.01, and *p < 0.05.

Significant effects of land use, as indicated by the high βL and low AIC
values, were observed for all biogeochemical indicators for the specified
dL_Range values (Table 2 and Fig. 5), although these effects were weaker
than those linked to the spatial autocorrelation and coastline enclosure.
The POC, Chl. a and δ13CPOM were positively related to the area occu­
pied by agricultural land in watersheds with dL_Range values of 6–12 km.
The DOC was positively related to urban land use for dL_Range values ≤4
km. In addition, the POC and δ13CPOM were negatively related to forest
cover for the dL_Range values of 4–6 km. Meanwhile, the C:NPOM displayed
negative relationship to the agricultural and urban lands for dL_Range
values of 20–30 km. Relatedly, the NH+ 4 was positively related to urban
land cover and negatively related to forest land cover for dL_Range values
of 20–22 km. Further, the PO3− 4 showed positive relationships with
agricultural and forest lands for dL_Range values of 20–24 km. The NO−2 +
NO−3 showed weak negative relationships with the agricultural and
urban lands for dL_Range values of 4–14 km and a positive relationship
with the forest land for a dL_Range of approximately 26 km. The δ15NMA
was positively related to the agricultural land use in nearby watersheds
for a dL_Range of approximately 7 km. This parameter also displayed a
positive relationship to the urban land use and a negative relationship
with forest cover for a dL_Range of approximately 24 km.
Thirteen of the 27 SAR models selected for their low AIC values
included the significant interaction term, βIs. Nine of the selected models
had a consistent direction (i.e., positive or negative coefficients) for the
effect of land use and its interactions with the effect of coastline
enclosure (POC vs. agriculture, Chl. a vs. urban, δ13CPOM vs. agriculture,
C:NPOM vs. urban, PO3− 4 vs. agriculture, NH4 vs. forest/urban, NO2 +
+ −
NO−3 vs. forest, and δ15NMA vs. agriculture). In addition, four of the
selected models with significant interaction terms had inconsistent di­
rections (i.e., positive and negative coefficients) between the effects of
land use and its interactive effects with coastline enclosure (POC vs.
forest, PO3− 15
4 vs. forest/urban, and δ NMA vs. forest).
4. Discussion
4.1. Land-use effects on the coastal biogeochemical indicators
The study island has relatively small watersheds with short river
networks and steep gradients; thus, the chemical constituents undergo
fewer biological alterations within the river systems owing to the rela­
tively shorter retention time. Furthermore, the material transports from
watersheds varied based on the seasonal flow regimes of the inflow
rivers. In general, coastal chemical environments exhibit more apparent
responses to downstream material transports as well as watershed en­
vironments in rainy seasons, while being controlled by processes within
coastal marine systems, such as upwelling and biological metabolism, in
dry seasons (e.g., Jennerjahn et al., 2004; Fernandez and Farias, 2012;
Paparazzo et al., 2021; Cardoso-Mohedano et al., 2022). The regional-
specific hydrological environments (i.e., relatively small and steep wa­
tersheds, and high precipitation) may be responsible for the significant
linkages between the coastal chemical environments and watershed
land use in the study island which were demonstrated by the SAR model
analyses.
In general, nitrogen from septic waste and manure is characterized
by higher δ15N values relative to nitrogen from atmospheric deposition
and forest soils (e.g., Mayer et al., 2002; Ohte, 2013). Therefore, the
positive relationships between the δ15NMA and the areas covered by
agricultural and urban lands possibly reflected the incorporation of ni­
trogen derived from such anthropogenic sources into the macroalgae (e.
g., Abaya et al., 2018; Panelo et al., 2022). In addition, although
chemical fertilizers, which are industrially produced from atmospheric
nitrogen and involved in aquatic environmental systems (e.g., Galloway
et al., 2004; Nishina et al., 2017), show low δ15N values (e.g., Mayer
et al., 2002; Ohte, 2013), denitrification causes isotopic fractionation,
and thus substantially increases the δ15N of nitrite and nitrate (e.g.,
Kendall, 1998; Sebilo et al., 2019). Therefore, nitrogen from chemical
fertilizers utilized in farms can be isotopically fractionated, and thus
increase the δ15N of the inorganic nitrogen before this reaches aquatic

5
T. Sakamaki et al.
a a
pseudo-R2
pseudo-R2
dS_Range dE_Range
environments (Diebel and Vander Zanden, 2009). The positive rela­
tionship between the δ15NMA and agricultural land use can also be
attributed to the incorporation of nitrogen from chemical fertilizers.
Primary producers assimilate 13C slower than 12C, but weaken the
13 12
C/ C fractionation under low concentrations of dissolved inorganic
carbon (DIC) associated with active primary production (e.g., Fogel
et al., 1992; Fry, 1996; Finlay, 2004). Thus, active primary production
increases the δ13C values of primary producers. The high values of
6
Marine Pollution Bulletin 183 (2022) 114054
Fig. 4. Plots displaying (a) effects of the dS_Range (to
define neighboring stations in the spatial weight ma­
trix) on the spatial autocorrelation strength (ρ) esti­
mates in the spatial autoregressive models and (b)
effects of the dE_Range (to define the spatial scale for the
coastline enclosure) on the impact of the enclosure
(βE) estimates in the spatial autoregressive models.
The 5, 50, and 95 % values of the pooled ρ or βE,
which were estimated for all combinations of dS_Range,
dE_Range, and dL_Range are represented by thick black
lines relative to the dS_Range or dE_Range, respectively.
The 5 % value of the AIC (thick gray line) and 95 %
value of the pseudo-R2 (dotted black line) from esti­
mates for all combinations of dS_Range, dE_Range, and
dL_Range, are also shown. The triangles represent the
dS_Range or dE_Range values for the best models presented
in Table 2; the solid and open triangles indicate the
significance of βL in the model, p < 0.05 or 0.05 ≤ p <
0.1, respectively.
δ13CPOM, which was also positively correlated with POC, Chl. a, and
δ15NMA, likely reflected enhanced primary production associated with
the input of nutrients from anthropogenic sources. Relatedly, the
negative relationships of C:NPOM with the agricultural and urban lands,
which were demonstrated by the SAR models, suggest that the input of
anthropogenic nitrogen enhanced the nitrogen content of the bulk par­
ticulate organic matter (POM). Bacteria have higher nitrogen contents
than algae (Nagata, 1986); nitrogen-rich environments may have
T. Sakamaki et al. Marine Pollution Bulletin 183 (2022) 114054

pseudo-R2
L

dL_Range
Fig. 5. Plots displaying effects of the dL_Range (to define the spatial range within which encompassed watersheds affect the chemical environment of sampling lo­
cations) on estimates of the watershed land-use effects (agricultural, forest or urban; βL) in the spatial autoregressive models. The 5, 50, and 95 % values of the pooled
βL estimated for all combinations of the dS_Range, dE_Range and dL_Range are plotted against the dL_Range. The 5 % value of the AIC (thick gray line) and 95 % value of the
pseudo-R2 (dotted black line) from the estimates for all combinations of the dS_Range, dE_Range and dL_Range, are also shown. The triangles represent the dL_Range values for
the best models presented in Table 2; the solid and open triangles indicate the level of significance of βL in the model, p < 0.05 or 0.05 ≤ p < 0.1, respectively.

7
T. Sakamaki et al.
increased the bacterial production of POM, thereby increasing the ni­
trogen content of the bulk POM (Caraco et al., 1998).
Biogeochemical indicators associated with non-marine and marine
materials that are not associated with human activities also exhibit
distinct signatures. In particular, nitrate associated with precipitation
and unpolluted stream waters generally yields low δ15N values (e.g.,
Mayer et al., 2002; Ohte, 2013). Thus, the negative relationship between
the δ15NMA and forest cover in the watersheds may have reflected both a
minor input of nitrogen from anthropogenic sources and input from
natural sources characterized by low δ15N values. Meanwhile, coarse
and fine POM derived from forest vegetation produce low δ13C and δ15N
values and high C:N ratios, and these commonly dominate the POM in
estuarine systems connected to forest-rich watersheds (e.g., Sakamaki
et al., 2010; Morita et al., 2017). However, the range of C:NPOM ratios of
5.7–8.6 obtained in the present study is distinctly lower than that of
organic matter derived from terrestrial plants (generally >20) (e.g.,
Enríquez et al., 1993; Sakamaki and Richardson, 2011). In addition, the
δ13CPOM ranged between − 22.0 ‰ and − 15.6 ‰, except for a sample
from one location which produced a markedly lower δ13C (− 27.2 ‰).
These values are notably higher than general δ13C values of POM from
terrestrial vegetation (e.g., < − 27 ‰) (e.g., Cloern et al., 2002). Ac­
cording to these POM-related indicators, the POM inputs from water­
sheds into the sampling locations in the present study were likely low.
The positive relationship between the DOC and urban land use in
nearby watersheds (i.e., approximately 4 km), which was indicated by
the SAR models, probably reflected inputs of anthropogenic dissolved
organic matter (DOM) and/or DOM of microbial/algal origin produced
in urban eutrophicated unshaded streams (e.g., Lambert et al., 2017;
Xenopoulos et al., 2021). Meanwhile, the relatively higher concentra­
3−
tions of NH+ 4 and PO4 suggest inputs of anthropogenic nutrients from
watersheds involving high urban or agricultural land use. In contrast,
the NO−2 + NO−3 showed negative relationships to the agricultural and
urban lands. In oligotrophic coral reefs, the nitrogen uptake and turn­
over by various biological constituents, such as micro/macro primary
producers, symbiotic corals, nitrogen fixers, and denitrifiers, are high,
and these complicate the nitrogen dynamics (e.g., Capone et al., 1992;
Miyajima et al., 2001; Archana et al., 2018; Pan et al., 2021). The pos­
itive relationship between the δ15NMA and human land use was probably
due to the rapid assimilation of anthropogenic nitrogen by macroalgae.
Considering the molar Redfield ratio of 16, the N:P ratios of inorganic
nutrients in the present study are relatively low (i.e., 2.0–20.4 with a
median of 6.4). Therefore, the NO−2 + NO−3 may have been rapidly used,
especially in locations with high inputs of PO3−4 , and this could explain
the contrasting responses between NO−2 + NO−3 and PO3− 4 to the land use.
4.2. Spatial variation of coastal chemical environment and assessment
scale
As the estimated model parameter for the land-use effect, βL, and AIC
values substantially varied based on the gradient of the spatial scale
parameter, dL_Range, the setting of the analytical spatial scale is critical for
the evaluation of the effects of land use. In other words, assessments
involving inadequate spatial scale settings can result in misinterpreta­
tion of the effects of the watershed land use on coastal chemical envi­
ronments. Furthermore, our results indicated that the responses of βL to
dL_Range differed between the biogeochemical indicators, possibly due to
the dispersion, retention, and reactions of land-derived materials
occurring within spatial ranges that are specific to each chemical con­
stituent in coastal marine systems. The POC, Chl. a, and δ13CPOM data
better explained the effects of watershed land use at low spatial ranges
than the dissolved inorganic nutrients. Dissolved inorganic nutrients are
rapidly consumed by local biological communities after entry into
oligotrophic coastal marine systems. Conversely, POM, which represents
the final product of primary production and is associated with low
biological reactivity, can be retained in coastal areas. Thus, POM may
better reflect anthropogenic nutrient inputs from nearby watersheds.
8
Marine Pollution Bulletin 183 (2022) 114054
The significant interaction term, βI, indicates non-additive effects of
land use and coastline enclosure on the biogeochemical indicators. In
particular, the consistent direction of the effect of human land use and
its interactions with the effect of coastline enclosure (e.g., SAR models
for POC vs. agriculture, Chl. a vs. urban, δ15NMA vs. agriculture) suggest
that the effects of land use on the biogeochemical indicators are facili­
tated by the coastline enclosure. The inlet/coastal complexity and water
circulation affect the retention of materials and ecological processes in
embayment systems (e.g., Filgueira et al., 2021). The effects of anthro­
pogenic materials on coastal chemical environments were probably
amplified by long retention times and weak dilution with offshore water
in more enclosed coastal systems of the island.
Interestingly, our analyses using the SAR models captured the spatial
distribution patterns of δ15NMA at two spatial scales. The δ15NMA data
showed a strong relationship with agricultural land use in watersheds
involving low spatial ranges. However, SAR models that included high
spatial scales revealed positive and negative relationships between the
δ15NMA data and the urban and forest lands, respectively. The significant
variation in δ15NMA at high spatial scales likely reflected the contrasting
conditions of the nutrient inputs between the north and south of the
island. In the north, forests are dominant, while urban and agricultural
lands are prevalent in the south.
Notably, the spatial variation in biogeochemical indicators and the
associations with the watersheds depend on the spatial structure of en­
vironments (e.g., coastal geomorphology, heterogeneity of watershed
land use, river size, and material loads), and are region-specific. The
significant variation in the δ15NMA data attributed to distinct differences
in the land-cover types between the north and south of the island is
specific to this island. The positive relationships of the POC, Chl. a, and
δ15NMA with the agricultural land use at low spatial scales (e.g., ≤ 8 km)
reflect the fragmented distribution of farms at such scales, especially in
the south of the island. In addition, highly-enclosed bays located mostly
in the east coast of the island are approximately 5–15 km in diameter.
These diameters are similar to the estimated spatial scales of enclosures
(5 km) at which the POC and Chl. a exhibit strong positive relationships
with the coastline enclosure.
4.3. Applicability and limitation of land use-based models
Evaluating the effects of human activity on ecosystems is dependent
on the spatial scale of the assessment, as human activity and ecosystem
structures are both spatially heterogeneous and exhibit different distri­
bution patterns (e.g., Allan et al., 1997; Townsend et al., 2003 Sakamaki
and Richardson, 2013; Cohen et al., 2016; Sakamaki et al., 2022). In this
study, we provided insights into the responses of biogeochemical in­
dicators to land-use types on the island, as well as the spatial scales of
land-use effects on coastal marine systems. However, assessments of
watershed–coast relationships can be influenced by the positions and
density of sampling locations because of the nature of statistical ap­
proaches. Further analyses of spatially dense data to fill gaps between
sampling locations used in the present study can enhance the reliability
of the watershed–coast relationships and spatial structures proposed.
Meanwhile, efforts for data sampling are often limited; therefore, further
studies in different regions using similar approaches would generate
data to improve empirically-derived a priori assumptions for the spatial
ranges associated with watershed effects on coastal marine systems.
Appropriate settings of spatial scales can enhance the sampling design
and data analysis reliability, which will provide novel, and more accu­
rate, insights into the relationships between biogeochemical processes in
coastal ecosystems and watershed environments.
Spatial variation in biogeochemical indicators depends on other
factors that differ among regions, such as the hydrology, geology,
coastal hydrodynamics, and human activities. Notably, the relationship
between biogeochemical indicators in coastal environments and
watershed land use is not direct evidence of the input of anthropogenic
materials into coastal marine systems. Hence, additional studies in other
T. Sakamaki et al.
regions are necessary to improve understanding of the impacts of
anthropogenic activities on biogeochemical processes in coastal marine
systems. Furthermore, these processes vary temporally at diurnal, sea­
sonal, and annual scales. Even though the results of the present study are
based on data from one survey at each location, the models, especially
those from the δ15NMA and indicators related to the POM (e.g., POC, Chl.
a and C:NPOM), produced adequate predictions. The results indicate that
these chemical variables can be useful indicators for reliable assessments
of the effects of land-derived materials on coastal environments. The
chemical properties of macroalgae and possibly POM last longer, and
these are expected to reflect local biogeochemical conditions for a spe­
cific temporal range. In general, the concentrations of dissolved nutri­
ents in seawater exhibit high temporal variability because of short-term
changes in environmental processes, such as hydrodynamic conditions
and biological uptake. Viana and Bode (2013) indicated that the δ15N of
macroalgae in coastal environments is unrelated to the occasionally
measured concentrations of inorganic nutrients in seawater, which is
consistent with the results of the present study. Therefore, the utilization
of biogeochemical indicators that persist temporally can decrease tem­
poral data sampling efforts in the field and enhance the efficiency and
reliability of assessments. Evaluation of the temporal representativeness
of these biogeochemical indicators in coastal marine systems is an
important avenue for further studies (a related study was conducted by
Viana and Bode, 2013).
Based on a GIS, reliable quantitative data on land use and coastal
geomorphology can be generated. In the present study, a practical
approach for estimating the impacts of anthropogenic activities on
coastal marine environments and the associated spatial structures is
provided. Groundwater is another avenue for the transportation of land-
derived nutrients to coral reefs (Umezawa et al., 2002; Bishop et al.,
2017; Panelo et al., 2022; Silva et al., 2022). Therefore, if spatial
boundaries of groundwater basins deviate from those of watersheds, the
uncertainty involved in estimating effects of watershed land use on
coastal environments can be elevated. In addition, inputs of anthropo­
genic nutrients from treated or untreated sewage also alters biogeo­
chemical processes in coastal environments (e.g., Abaya et al., 2018;
Wiegner et al., 2021). Sewage treatment systems, including four major
centralized systems, are in the south of the island, while many small
centralized and domestic septic systems are distributed across the island.
Previous studies based on field data analysis have shown that inputs of
anthropogenic materials from such point sources can substantially alter
river water quality and obscure relationships between river water
quality indices and watershed land use (e.g., Zhou et al., 2016; Williams-
Subiza et al., 2022). Therefore, the consideration of point source inputs
as additional factors during modeling can improve estimates on the ef­
fects of land-derived materials on coastal marine environments.
Furthermore, land-use data with finer classifications (e.g., agricultural
produce and forest vegetation type) might provide better insights for
enhancing environmental management by considering watershed-coast
connections and effectively controlling material loadings from water­
sheds. However, the land-use data used herein do not contain informa­
tion on relevant point sources or detailed classifications of land-use
types. Quantitative data on the loading of sewage-derived nutrients,
performance of treatment systems, and spatial distributions are also
limited. In general, information on the boundaries of groundwater ba­
sins is limited and associated with high uncertainty. Even if such
detailed information is accessible (e.g., boundaries of groundwater ba­
sins, point sources, finer classifications of land-use type), more field data
on the chemical environments will be needed for higher degrees of
freedom for the analysis, which may cause excessive parameterization.
In future studies, the effects of incorporating these additional factors
into the models should be examined by comparing them with more
parsimonious models based on watershed land use.
9
Marine Pollution Bulletin 183 (2022) 114054
5. Conclusions
Evaluating the effects of land use on coastal environments and their
associated spatial ranges is vital for enhancing coastal environmental
management by highlighting the responsibilities of stakeholders who
influence terrestrial environments. In the present study, an approach to
spatially delineate land-use effects in watersheds on chemical environ­
ments in the coral reef-dominant systems of an island was introduced.
The spatial patterns of biogeochemical indicators and their relationships
to land use in watersheds varied between coastal biogeochemical in­
dicators. Useful biogeochemical indicators that were effective in
assessing the impacts of land use on coastal marine environments were
highlighted (the first study objective). In particular, the concentration
and chemical characteristics of POM suspended in seawater and δ15N of
macroalgae exhibited high potential as indicators of the land-use effects
on coastal marine environments. Our analyses that included those in­
dicators revealed that agricultural and urban land use significantly alters
the chemical environments in fringing coral reefs of the study island.
This is essential information for local environmental managers respon­
sible for protecting the valuable and vulnerable coastal ecosystems. The
modeling associated with GIS-based watershed land-use data utilized in
the present study is a practical approach for estimating the extent and
spatial ranges of the impacts of anthropogenic activities on coastal
marine environments. Using this approach, adequate spatial scales for
the assessments were obtained and these captured the impacts of
anthropogenic activity on the chemical environments of the fringing
coral reefs of the study island (the second study objective). As the
adequate spatial scales for the assessment differed between the
biogeochemical indicators, appropriate combinations of analytical
scales and biogeochemical indicators should be used to effectively assess
the effects of watershed land use on coastal marine environments.
CRediT authorship contribution statement
Takashi Sakamaki: Conceptualization, Methodology, Formal anal­
ysis, Writing- Original draft preparation, Akiko Morita: GIS analysis,
Data curation, Shouji Touyama: Investigation, GIS analysis, Yasushi
Watanabe: Analytical methodology, GIS analysis, Shouhei Suzuki:
Investigation, Takashi Kawai: Investigation, Writing- Reviewing and
Editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgements
We thank C. Fukuda, S. Inafuku, M. Katayama, Y. Miyaoka, K. Toda,
N. Yamaga, and M. Yamamura for their assistance with the field sam­
pling and laboratory work. This work was funded by the Japan Society
for the Promotion of Science: Funding Program for the Next Generation
World-Leading Researcher GR083 and KAKENHI 22H03753.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.marpolbul.2022.114054.
T. Sakamaki et al. Marine Pollution Bulletin 183 (2022) 114054

References Filgueira, R., Guyondet, T., Thupaki, P., Sakamaki, T., Grant, J., 2021. The effect of
embay-ment complexity on ecological carrying capacity estimations in bivalve
aquaculture sites. J. Clean. Prod. 288, 125739.
Abaya, L.M., Wiegner, T.N., Colbert, S.L., Beets, J.P., Carlson, K.M., Kramer, K.L.,
Finlay, J.C., 2004. Patterns and controls of lotic algal stable carbon isotope ratios.
Most, R., Couche, C.S., 2018. A multi-indicator approach for identifying shoreline
Limnol. Oceanogr. 49, 850–861.
sewage pollution hotspots adjacent to coral reefs. Mar. Pollut. Bull. 129, 70–80.
Fogel, M.L., Cifuentes, L.A., Velinsky, D.J., Sharp, J.H., 1992. Relationship of carbon
Allan, J.D., Erickson, D.L., Fay, J., 1997. The influence of catchment land use on stream
availability in estuarine phytoplankton to isotopic composition. Mar. Ecol. Prog. Ser.
integrity across multiple spatial scales. Freshw. Biol. 37, 149–161.
82, 291–300.
Álvarez-Romero, J.G., Wilkinson, S.N., Pressey, R.L., Ban, N.C., Kool, J., Brodie, J., 2014.
Fry, B., 1996. C-13/C-12 fractionation by marine diatoms. Mar. Ecol. Prog. Ser. 134,
Modeling catchment nutrients and sediment loads to inform regional management of
283–294.
water quality in coastal-marine ecosystems: a comparison of two approaches.
Galloway, J.N., Dentener, F.J., Capone, D.G., Boyer, E.W., Howarth, R.W., Seitzinger, S.
J. Environ. Manag. 146, 164–178.
P., Asner, G.P., Cleveland, C.C., Green, P.A., Holland, E.A., Karl, D.M., Michaels, A.
Álvarez-Romero, J.G., Pressey, R.L., Ban, N.C., Brodie, J., 2016. Advancing land-sea
F., Porter, J.H., Townsend, A.R., Vorosmarty, C.J., 2004. Nitrogen cycles: past,
conservation planning: integrating modelling of catchments, land-use change, and
present, and future. Biogeochemistry 70, 153–226.
river plumes to prioritise catchment management and protection. Plos One 10 (12),
Garmendia, M., Revilla, M., Bald, J., Franco, J., Laza-Martinez, A., Orive, E., Seoane, S.,
e0145574.
Valencia, V., Borja, A., 2011. Phytoplankton communities and biomass size structure
Archana, A., Thibodeau, B., Geeraert, N., Xu, M.N., Kao, S.J., Baker, D.M., 2018.
(fractionated chlorophyll "a"), along trophic gradients of the Basque coast (northern
Nitrogen sources and cycling revealed by dual isotopes of nitrate in a complex
Spain). Biogeochemistry 106 (2), 243–263.
urbanized environment. Water Res. 142, 459–470.
Goñi, M.A., Ruttenberg, K.C., Eglinton, T.I., 1998. A reassessment of the sources and
Bannon, R.O., Roman, C.T., 2008. Using stable isotopes to monitor anthropogenic
importance of land-derived organic matter in surface sediments from the Gulf of
nitrogen inputs to estuaries. Ecol. Appl. 18, 22–30.
Mexico. Geochim. Cosmochim. Acta 62, 3055–3075.
Beck, M.W., Sherwood, E.T., Henkel, J.R., Dorans, K., Ireland, K., Varela, P., 2019.
Hanna, D.E.L., Lehner, B., Taranu, Z.E., Solomon, C.T., Bennett, E.M., 2021. The
Assessment of the cumulative effects of restoration activities on water quality in
relationship between watershed protection and water quality: the case of Québec,
Tampa Bay,Florida. Estuar. Coasts 42 (7), 1774–1791.
Canada. Freshw. Sci. 40 https://doi.org/10.1086/714598.
Bellwood, D.R., Hughes, T.P., Folke, C., Nyström, M., 2004. Confronting the coral reef
Harborne, A.R., Mumby, P.J., Zychaluk, K., Hedley, J.D., Blackwell, P.G., 2006.
crisis. Nature 429, 827–833.
Modeling the beta diversity of coral reefs. Ecology 87, 2871–2881.
Bishop, J.M., Glenn, C.R., Amato, D.W., Dulai, H., 2017. Effect of land use and
Howe, E., Simenstad, C.A., Ogston, A., 2017. Detrital shadows: estuarine food web
groundwater flow path on submarine groundwater discharge nutrient flux. J.Hydrol.
connectivity depends on fluvial influence and consumer feeding mode. Ecol. Appl.
Reg.Stud. 11, 194–218.
27, 2170–2193.
Brodie, J.E., Kroon, F.J., Schaffelke, B., Wolanski, E.C., Lewis, S.E., Devlin, M.J.,
Hoegh-Guldberg, O., 1999. Climate change, coral bleaching and the future of the
Bohnet, I.C., Bainbridge, Z.T., Waterhouse, J., Davis, A.M., 2012. Terrestrial
world&#x27;s coral reefs. Mar. Freshw. Res. 50 (8), 839–866.
pollutant runoff to the Great Barrier Reef: an update of issues, priorities and
Jennerjahn, T.C., Ittekkot, V., Klopper, S., Adi, S., Nugroho, S.P., Sudiana, N., Yusmal, A.,
management responses. Mar. Pollut. Bull. 65, 81–100.
Prihartanto, Gaye-Haake, B., 2004. Biogeochemistry of a tropical river affected by
Canuel, E.A., Hardison, A.K., 2016. Sources, ages, and alteration of organic matter in
human activities in its catchment: Brantas River estuary and coastal waters of
estuaries. Annu. Rev. Mar. Sci. 8, 409–434.
Madura Strait, Java, Indonesia. Estuar. Coast. Shelf Sci. 60 (3), 503–514.
Capone, D.G., Dunham, S.E., Horrigan, S.G., Duguay, L.E., 1992. Microbial nitrogen
Kendall, C., 1998. Tracing nitrogen sources and cycling in catchments. In: Kendall, C.,
transformations in unconsolidated coral reef sediments. Mar. Ecol. Prog. Ser. 80,
McDonnell, J.J. (Eds.), Isotope Tracers in Catchment Hydrology, pp. 519–576.
75–88.
Kourafalou, V.H., Oey, L.Y., Wang, J.D., Lee, T.N., 1996. The fate of river discharge on
Caraco, N.F., Lampman, G., Cole, J.J., Limburg, K.E., Pace, M.L., Fischer, D., 1998.
the continental shelf.1. Modeling the river plume and the inner shelf coastal current.
Microbial assimilation of DIN in a nitrogen rich estuary: implications for food quality
J. Geophys. Res. Oceans 101 (C2), 3415–3434.
and isotope studies. Mar. Ecol. Prog. Ser. 167, 59–71.
Lambert, T., Bouillon, S., Darchambeau, F., Morana, C., Roland, F.A.E., Descy, J.,
Cardoso-Mohedano, J.G., Canales-Delgadillo, J.C., Machain-Castillo, M.L., Sanchez-
Borges, A.V., 2017. Effects of human land use on the terrestrial and aquatic sources
Munoz, W.N., Sanchez-Cabeza, J.A., Esqueda-Lara, K., Gomez-Ponce, M.A., Ruiz-
of fluvial organic matter in a temperate river basin (The Meuse River, Belgium).
Fernandez, A.C., Alonso-Rodriguez, R., Lestayo-Gonzalez, J.A., Merino-Ibarra, M.,
Biogeochemistry 136, 191–211.
2022. Contrasting nutrient distributions during dry and rainy seasons in coastal
Lapointe, B.E., Clark, M.W., 1992. Nutrient inputs from the watershed and coastal
waters of the southern Gulf of Mexico driven by the Grijalva-Usumacinta River
eutrophicaltion in the Florida Keys. Estuaries 15, 465–476.
discharges. Mar. Pollut. Bull. 178, 113584.
Lapointe, B.E., Brewton, R.A., Herren, L.W., Porter, J.W., Hu, C.M., 2019. Nitrogen
Carlson, R.R., Foo, S.A., Asner, G.P., 2019. Land use impacts on coral reef health: a ridge-
enrichment, altered stoichiometry, and coral reef decline at Looe Key, Florida Keys,
to-reef perspective. Front. Mar. Sci. 6, 562.
USA: a 3-decade study. Mar. Biol. 166, 108.
Carlson, R.R., Evans, L.J., Foo, S.A., Grady, B.W., Li, J., Seeley, M., Xu, Y., Asner, G.P.,
LeSage, J., Pace, R., 2009. Introduction to Spatial Econometrics. CRC Press, Boca Raton,
2021. Synergistic benefits of conserving land-sea ecosystems. Glob.Ecol.Conserv. 28,
FL.
e01684.
Manning, D.W.P., Rosemond, A.D., Benstead, J.P., Bumpers, P.M., Kominoski, J.S., 2020.
Carpenter, S.R., Caraco, N.F., Correll, D.L., Howarth, R.W., Sharpley, A.N., Smith, V.H.,
Transport of N and P in US streams and rivers differs with land use and between
et al., 1998. Nonpoint pollution of surface waters with phosphorus and nitrogen.
dissolved and particulate forms. Ecol. Appl. 30, e02130.
Ecol. Appl. 8, 559–568.
Martinetto, P., Teichberg, M., Valiela, I., 2006. Coupling of estuarine benthic and pelagic
Cloern, J.E., Canuel, E.A., Harris, D., 2002. Stable carbon and nitrogen isotope
food webs to land-derived nitrogen sources in Walquoit Bay, Massachusetts, USA.
composition of aquatic and terrestrial plans of the San Francisco Bay estuarine
Mar. Ecol. Prog. Ser. 307, 37–48.
system. Limnol. Oceanogr. 47, 713–729.
Mayer, B., Boyer, E.W., Goodale, C., Jaworski, N.A., Van Breemen, N., Howarth, R.W.,
Cohen, J.M., Civitello, D.J., Brace, A.J., Feichtinger, E.M., Ortega, C.N., Richardson, J.C.,
Seitzinger, S., Billen, G., Lajtha, L.J., Nosal, M., Paustian, K., 2002. Sources of nitrate
Sauer, E.L., Liu, X., Rohr, J.R., 2016. Spatial scale modulates the strength of
in rivers draining sixteen watersheds in the northeastern US: isotopic constraints.
ecological processes driving disease distributions. Proc. Natl. Acad. Sci. U. S. A. 113,
Biogeochemistry 57, 171–197.
E3359–E3364.
McClelland, J.W., Valiela, I., Michener, R.H., 1997. Nitrogen-stable isotope signatures in
Connell, J.H., 1978. Diversity in tropical rain forests and coral reefs - high diversity of
estuarine food webs: a record of increasing urbanization in coastal watersheds.
trees and corals is maintained only in a non-equilibrium state. Science 199 (4335),
Limnol. Oceanogr. 42, 930–937.
1302–1310.
Miyajima, T., Suzumura, M., Umezawa, Yu., Koike, I., 2001. Microbiological nitrogen
Deegan, L.A., Wright, A., Ayvazian, S.G., Finn, J.T., Golden, H., Merson, R.R.,
transformation in carbonate sediments of a coral-reef lagoon and associated seagrass
Harrison, J., 2002. Nitrogen loading alters seagrass ecosystem structure and support
beds. Mar. Ecol. Prog. Ser. 217, 273–286.
of higher trophic levels. Aquat.Conserv.Mar.Freshwat.Ecosyst. 12 (2), 193–212.
Mora, C., Aburto-Oropeza, O., Bocos, A.A., Ayotte, A.B., Banks, S., Bauman, A.G., et al.,
Diebel, M.W., Vander Zanden, M.J., 2009. Nitrogen stable isotopes in streams: effects of
2011. Global human footprint on the linkage between biodiversity and ecosystem
agricultural sources and transformations. Ecol. Appl. 19, 1127–1134.
functioning in reef fishes. PLoS Biol. 9, e1000606.
Diefenderfer, H.L., Sobocinski, K.L., Thom, R.M., May, C.W., Borde, A.B., Southard, S.L.,
Morita, A., Touyama, S., Kuwae, T., Nishimura, O., Sakamaki, T., 2017. Effects of
Vavrinec, J., Sather, N.K., 2009. Multiscale analysis of restoration priorities for
watershed land-cover on the biogeochemical properties of estuarine tidal flat
marine shoreline planning. Environ. Manag. 44 (4), 712–731.
sediments: a test in a densely-populated subtropical island. Estuar. Coast. Shelf Sci.
Dutra, L.X.C., Haywood, M.D.E., Singh, S., Ferreira, M., Johnson, J.E., Veitayaki, J.,
184, 207–213.
Kininmonth, S., Morris, C.W., Piovano, S., 2021. Synergies between local and
Mwaijengo, G.N., Msigwa, A., Njau, K.N., Brendonck, L., Vanschoenwinkel, B., 2020.
climate-driven impacts on coral reefs in the Tropical Pacific: a review of issues and
Where does land use matter most? Contrasting land use effects on river quality at
adaptation opportunities. Mar. Pollut. Bull. 164, 111922.
different spatial scales. Sci. Total Environ. 715, 134825.
Enríquez, S., Duarte, C.M., Sand-Jensen, K., 1993. Patterns in decomposition rates among
Nagata, T., 1986. Carbon and nitrogen-content of natural planktonic bacteria. Appl.
photosynthetic organisms: the importance of detritus C:N:P content. Oecologia 94,
Environ. Microbiol. 52, 28–32.
457–471.
Nasrollahzadeh, H.S., Din, Z.B., Foong, S.Y., Makhlough, A., 2008. Trophic status of the
Fennel, K., Hetland, R., Feng, Y., DiMarco, S., 2011. A coupled physical-biological model
Iranian Caspian Sea based on water quality parameters and phytoplankton diversity.
of the Northern Gulf of Mexico shelf: model description, validation and analysis of
Cont. Shelf Res. 28, 1153–1165.
phytoplankton variability. Biogeosciences 8, 1881–1899.
Nishina, K., Ito, A., Hanasaki, N., Hayashi, S., 2017. Reconstruction of spatially detailed
Fernandez, C., Farias, L., 2012. Assimilation and regeneration of inorganic nitrogen in a
global map of NH4+ and NO3- application in synthetic nitrogen fertilizer. Earth Syst.
coastal upwelling system: ammonium and nitrate utilization. Mar. Ecol. Prog. Ser.
Sci.Data 9, 149–162.
451, 1–14.

10
T. Sakamaki et al.
Nixon, S.W., 1995. Coastal marine eutrophication - a definition, social causes, and future
concerns. Ophelia 41, 199–219.
Ohte, N., 2013. Tracing sources and pathways of dissolved nitrate in forest and river
ecosystems using high-resolution isotopic techniques: a review. Ecol. Res. 28,
749–757.
Pan, K., Zheng, X.Q., Liu, X.M., Jiang, H., 2021. Nitrogen cycling in a tropical coral reef
ecosystem under severe anthropogenic disturbance in summer: insights from isotopic
compositions. Water Res. 207, 117824.
Panelo, J., Wiegner, T.N., Colbert, S.L., Goldberg, S., Abaya, L.M., Conklin, E., Couch, C.,
Falinski, K., Gove, J., Watson, L., Wiggins, C., 2022. Spatial distribution and sources
of nutrients at two coastal developments in South Kohala, Hawai'i. Mar. Pollut. Bull.
174, 113143.
Paparazzo, F.E., Martinez, R.P., Fabro, E., Goncalves, R.J., Crespi-Abril, A.C., Soria, G.R.,
Barbieri, E.A., Almandoz, G.O., 2021. Relevance of sporadic upwelling events on
primary productivity: the key role of nitrogen in a gulf of SW Atlantic Ocean. Estuar.
Coast.Shelf Sci. 249, 107123.
Pearson, R.G., Connolly, N.M., Davis, A.M., Brodie, J.E., 2021. Fresh waters and estuaries
of the Great Barrier Reef catchment: effects and management of anthropogenic
disturbance on biodiversity, ecology and connectivity. Mar. Pollut. Bull. 166,
112194.
Reimer, J.D., Yang, S., White, K.N., Asami, R., Fujita, K., Hongo, C., Ito, S., Kawamura, I.,
Maeda, B., Mizuyama, M., Obuchi, M., Sakamaki, T., Tachihara, K., Tamura, M.,
Tanahara, A., Yamaguchi, A., Jenke-Kodama, H., 2015. Effects of causeway
construction on environment and biota of subtropical tidal flats in Okinawa, Japan.
Mar. Pollut. Bull. 94, 153–167.
Roberts, C.M., McClean, C.J., Veron, J.E.N., Hawkins, J.P., Allen, G.R., McAllister, D.E.,
Mittermeier, C.G., Schueler, F.W., Spalding, M., Wells, F., Vynne, C., Werner, T.B.,
2002. Marine biodiversity hotspots and conservation priorities for tropical reefs.
Science 295, 1280–1284.
Sakamaki, T., Richardson, J.S., 2008a. Retention, breakdown and biological utilisation of
broadleaf deciduous tree leaves in an estuarine tidal flat of southwestern British
Columbia,Canada. Can. J. Fish. Aquat. Sci. 65, 38–46.
Sakamaki, T., Richardson, J.S., 2008b. Effects of small rivers on chemical properties of
sediment and diets for primary consumers in estuarine tidal flats: a comparison
between forested and agricultural watersheds. Mar. Ecol. Prog. Ser. 360, 13–24.
Sakamaki, T., Richardson, J.S., 2009. Dietary responses of tidal flat macrobenthos to
reduction of benthic microalgae: a test for potential use of allochthonous organic
matter. Mar. Ecol. Prog. Ser. 386, 107–113.
Sakamaki, T., Richardson, J.S., 2011. Biogeochemical properties of fine particulate
organic matter as indicators to assess local and catchment impacts on forested
streams. J. Appl. Ecol. 48, 1462–1471.
Sakamaki, T., Richardson, J.S., 2013. Nonlinear variation of stream-forest linkage along
a stream-size gradient: an assessment using biogeochemical proxies of in-stream fine
particulate organic matter. J. Appl. Ecol. 50, 1019–1027.
Sakamaki, T., Shum, J.Y.T., Richardson, J.S., 2010. Watershed effects on chemical
properties of sediment and primary consumption in estuarine tidal flats: importance
of watershed size and food selectivity by macrobenthos. Ecosystems 13, 328–337.
Sakamaki, T., Zheng, Y., Hatakeyama, Y., Fujibayashi, M., Nishimura, O., 2022. Effects of
spatial scale on assessments of suspension bivalve aquaculture for productivity and
environmental impacts. Aquaculture 553, 738082.
11
Marine Pollution Bulletin 183 (2022) 114054
Schmidt, A.L., Wysmyk, J.K.C., Craig, S.E., Lotze, H.K., 2012. Regional-scale effects of
eutrophication on ecosystem structure and services of seagrass beds. Limnol.
Oceanogr. 57, 1389–1402.
Sebilo, M., Aloisi, G., Mayer, B., Perrin, E., Vaury, V., Mothet, A., Laverman, A.M., 2019.
Controls on the isotopic composition of nitrite (delta N-15 and delta O-18) during
denitrification in freshwater sediments. Sci. Rep. 9, 19206.
Silva, B.J., Ibanhez, J.S.P., Pinheiro, B.R., Ladle, R.J., Malhado, A.C., Pinto, T.K., Flores-
Montes, M.J., 2022. Seasonal influence of surface and underground continental
runoff over a reef system in a tropical marine protected area. J. Mar. Syst. 226,
103660.
Suzuki, S., Kawai, T., Sakamaki, T., 2018. Combination of different habitat preferences of
trophic groups determines coral reef fish assemblages. Mar. Ecol. Prog. Ser. 586,
141–154.
Tewfik, A., Rasmussen, J.B., McCann, K.S., 2005. Anthropogenic enrichment alters a
marine benthic food web. Ecology 86, 2726–2736.
Townsend, C.R., Doledec, S., Norris, R., Peacock, K., Arbuckle, C., 2003. The influence of
scale and geography on relationships between stream community composition and
landscape variables: description and prediction. Freshw. Biol. 48, 768–785.
Umezawa, Y., Miyajima, T., Kayanne, H., Koike, I., 2002. Significance of groundwater
nitrogen discharge into coral reefs at Ishigaki Island, southwest of Japan. Coral Reefs
21, 346–356. https://doi.org/10.1007/s00338-002-0254-5.
Viana, I.G., Bode, A., 2013. Stable nitrogen isotopes in coastal macroalgae: geographic
and anthropogenic variability. Sci. Total Environ. 443, 887–895.
Washburn, L., McClure, K.A., Jones, B.H., Bay, S.M., 2003. Spatial scales and evolution of
stormwater plumes in Santa Monica Bay. Mar. Environ. Res. 56, 103–125.
Wiegner, T.N., Colbert, S.L., Abaya, L.M., Panelo, J., Remple, K., Nelson, C.E., 2021.
Identifying locations of sewage pollution within a Hawaiian watershed for coastal
water quality management actions. J. Hydrol. Reg. Stud. 38, 100947.
Williams, G.J., Smith, J.E., Conklin, E.J., Gove, J.M., Sala, E., Sandin, S.A., 2013. Benthic
communities at two remote Pacific coral reefs: effects of reef habitat, depth, and
wave energy gradients on spatial patterns. PeerJ 1, 26.
Williams-Subiza, E.A., Assef, Y.A., Brand, C., 2022. Point source pollution influences
water quality of Patagonian streams more than land cover. River Res. Appl. 38,
69–79.
Wilson, S.K., Graham, N.A.J., Pratchett, M.S., Jones, G.P., Polunin, N.V.C., 2006.
Multiple disturbances and the global degradation of coral reefs: are reef fishes at risk
or resilient? Glob. Chang. Biol. 12, 2220–2234.
Wolff, N.H., da Silva, E.T., Devlin, M., Anthony, K.R.N., Lewis, S., Tonin, H.,
Brinkman, R., Mumby, P.J., 2018. Contribution of individual rivers to Great Barrier
Reef nitrogen exposure with implications for management prioritization. Mar.
Pollut. Bull. 133, 30–43.
Wu, J., Zeng, S.D., Yang, L.H., Ren, Y.X., Xia, J., 2021. Spatiotemporal Characteristics of
the Water Quality and Its Multiscale Relationship with Land Use in the Yangtze River
Basin. Remote Sens. 13, 3309.
Xenopoulos, M.A., Barnes, R.T., Boodoo, K.S., Butman, D., Catalán, N., D’Amario, S.C.,
Fasching, C., Kothawala, D.N., Pisani, O., Solomon, C.T., Spencer, R.G.M.,
Williams, C.J., Wilson, H.F., 2021. How humans alter dissolved organic matter
composition in freshwater: relevance for the Earth's biogeochemistry.
Biogeochemistry 154, 323–348.
Zhou, P., Huang, J.L., Pontius, R.G., Hong, H.S., 2016. New insight into the correlations
between land use and water quality in a coastal watershed of China: does point
source pollution weaken it? Sci. Total Environ. 543, 591–600.