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Hard Coral Cover in the Halmahera Waters: Spatial

Distribution and Environmental Factors

Abdul Motalib Angkotasan, Dietriech G Bengen, I

Wayan Nurjaya, Neviaty P Zamani, Nyoman M.N
Natih, Andi Zulfikar

PII: S2352-4855(23)00424-3
DOI: https://doi.org/10.1016/j.rsma.2023.103234
Reference: RSMA103234

To appear in: Regional Studies in Marine Science

Received date: 4 August 2022
Revised date: 30 September 2023
Accepted date: 2 October 2023
Please cite this article as: Abdul Motalib Angkotasan, Dietriech G Bengen, I
Wayan Nurjaya, Neviaty P Zamani, Nyoman M.N Natih and Andi Zulfikar,
Hard Coral Cover in the Halmahera Waters: Spatial Distribution and
Environmental Factors, Regional Studies in Marine Science, (2023)
doi:https://doi.org/10.1016/j.rsma.2023.103234
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Hard Coral Cover in the Halmahera Waters: Spatial Distribution and
Environmental Factors
Abdul Motalib Angkotasan1*), Dietriech G Bengen1*), I Wayan Nurjaya1, Neviaty P Zamani1,
Nyoman M.N Natih1, Andi Zulfikar2
1
Department of Marine Sciences and Technology, Faculty of Fisheries and Marine Science,
IPB University, Bogor 16680, Indonesia
2
Raja Ali Haji Maritime University, Tanjung Pinang 29155, Indonesia
*)
Corresponding author: angkotasanmotalib@apps.ipb.ac.id; dieter@indo.net.id

Abstract
Differences in the geographical location and geomorphology of small islands contribute to
variations in aquatic environmental factors, spatial distribution of corals, and percentage of
hard coral cover. This study was conducted in the open waters of the Termadoreh Islands in
the middle of the Maluku Sea, and the semi-enclosed waters of Buli Bay. This study aimed to

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examine the distribution of hard coral cover in the Halmahera coral ecoregion with respect to
differences in geographic location, geomorphology and water quality. This study found that

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the spatial distribution of hard corals differed among sites. Spatially, the total area of shallow
water habitat at the study site showed the largest area of coral habitat in Termadoreh, at
1,313.99 ha. Hard coral cover and coral diversity differed between sites and depths. Higher
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hard coral cover was found on the coral islands of Teluk Buli and lower on the volcanic
islands of the Termadoreh Archipelago. The highest percentage of hard coral cover per site
was found on Maitara Island (site MaT05) at 71.60%, and the lowest percentage of cover was
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found on Tidore Island (site TiT08) at 14.9%. An optimal temperature, salinity, and
brightness parameters support the high percentage of hard coral cover. The highest coral
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diversity value in the Termadoreh Islands correlated with water brightness. This study is
important for recording the conditions of hard corals in the Halmahera reef ecoregion. The
results of this study provide data on the benefits of a coral reef management plan for the
Halmahera coral ecoregion. We also provide recommendations regarding the life forms of
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hard corals that are appropriate for making coral seeds to restore and rehabilitate coral reef
ecosystems at the research sites.
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Keywords:
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Coral reef, Coral triangle, Ecoregion, Halmahera, Vulcanic island.

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1. Introduction
Hard corals contribute to the complexity of interactions of species in coral reefs, and are
indicators to geomorphology and biodiversity playing an important role in carbonate
production (McWilliam et al., 2018), water productivity processes (Anthony et al., 2008), and
the structural formation of coral reef habitats (Pratchett et al., 2008), providing important
resources (food and shelter) for many reef organisms (Cole et al., 2008; Duckworth et al.,
2017; Rotjan and Lewis, 2008; Stella et al., 2011). Corals are contributors to key ecosystem
functions, such as calcification, photosynthesis, nutrient cycling, and habitat structure
(McWilliam et al., 2018). Hard coral cover is correlateds with regional coral biodiversity, and
contributes to global coral biodiversity.
Globally, the highest level of coral diversity is found in the Coral Triangle region. The
Halmahera coral ecoregion is one of the areas in the coral reef triangle that has the third
highest level of coral diversity out of 141 ecoregions in the world; there are 544 species of
coral are found in these waters (Veron et al., 2009). It is an important habitat for various
endemic animals, including Hemicilius halmahera (Madduppa et al., 2020). This area has a
variety of coral species because of its high level of rugosity as a habitat for coral growth
(Best et al., 1989). The level of coral roughness depends on its constituent substrate, which is
determined by the geological and geomorphological processes of the island.
The geomorphology of small islands in the Indonesian Archipelago is diverse; there
are plain islands (alluvium islands, coral islands, and atoll islands) and hilly islands (volcanic
islands, tectonic islands, rising terrace islands, Petabah islands, and mixed genesis islands)
spread from Papua to Aceh (Bengen et al., 2012). The waters of Halmahera Island are
surrounded by a group of volcanic islands to the west, namely Ternate Island, Maitara Island,
Tidore Island, and Hiri Island (Mutaqin et al., 2021; Van Gorsel, 2018). in the waters east of
Halmahera Island, there is a group of coral islands, namely Plun Island, Lelewi Island,
Englan Island, and Pakal Island, which are tectonic islands (Bengen et al., 2012). Differences
in the geomorphology of these islands contribute to differences in the distribution of hard
corals in their waters.
The geographical location and differences in island geomorphology contribute to

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differences in oceanographic conditions and the spatial distribution of hard corals in the
waters of small islands. Volcanic islands of the proven type have steep water topography,

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while plain islands have sloping topography (Angkotasan et al., 2022). Geographically, this
region is located at low latitudes ranging from 20 South Latitude to 30 North Latitude and
1260 to 1300 East Longitude. This area is a route for the movement of Indonesian
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Throughflow (ITF) water masses through the Maluku and Halmahera Seas(Atmadipoera et
al., 2018; Wattimena et al., 2018; Wirtky, 1961). Oceanographic conditions and geological
phenomena contribute to the formation of ecological characteristics and geomorphic zones of
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coral reefs (Done, 1983; Kennedy et al., 2021; Kim et al., 2022). As is the case in Jakarta Bay
and the Thousand Islands, where water quality influences the distribution of coral reefs
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(Baum et al., 2015). In addition, HCC fluctuations in the Great Barrier Reef (GBR) are
caused by environmental factors such as the predation of acanthos (COTs) and coral disease
(Osborne et al., 2011). Justification of the relationship between geographic location and the
morphogenesis of different islands affecting the spatial distribution of hard corals in waters is
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a new matter that requires comprehensive study.

This research considered studies on hard coral cover in the area, including geological
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studies from the Hawaiian volcanic islands, where wave action and sedimentation also affect
coral distribution (Fletcher et al., 2008), and studies of hard corals in the Mauritius volcanic
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island (Montaggioni and Martin-Garin, 2020). In the case of HCC in Ternate island, the
topography and substrate influence their growth (Paembonan et al., 2021); in Seribu islands
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coral cover was high in the upper areas (Fahlevy et al., 2019); and in the Great Barrier Reef
in Australia from 1995-2009 showed fluctuations in cover, with Acropora being a pioneer for
natural recovery (Osborne et al., 2011). In Philippines, the coral reefs were influenced by
wave pressure and local environmental conditions (Feliciano et al., 2023). Previous research
has photographed the phenomenon in the same water conditions in one location, for example,
only on a volcanic island or in a bay. There has been no research comparing the distribution
of hard coral cover between open and semi-enclosed waters, waters on small volcanic islands,
and coral islands, and their relationship to aquatic environmental factors.
This study aimed to determine the spatial distribution of HCC in the Halmahera coral
ecoregion and its relationship with various environmental factors. Furthermore, this study
aimed to describe the main variables or components affecting the spatial distribution of corals
at different spatial levels in the waters of Halmahera Island. The conditions of HCC on
volcanic islands (oceanic) and coral islands (bays) where also compared. These data and
information are important for analyze whether specific characteristics distinguish the spatial
distribution of corals and HCC. It is also important to monitor the conditions of coral reefs in
the future to examine the impacts of climate change and local environmental conditions on
the distribution of coral diversity in these two locations.

2. Materials and Methods

2.1. Study Site
Field data were collected from January to March 2021 from the waters of the small
islands of Halmahera. These data were obtained from two research areas, Buli Bay (Englan
Island, Plum Island, Lelewi Island, and Pakal Island) and Termadoreh Archipelago (Ternate,
Maitara, Tidore, and Hiri) (Figure 1). The data were from 1550 photo transects collected
from 16 sites and 31 transects. Based on island morphogenesis, the Termadoreh Islands are a
group of volcanic islands, whereas the small islands in Buli Bay are are made of coral.
Geographically, the Termadoreh Islands are located in the ITF channel of the Maluku Sea,
whereas Buli Bay is located in the ITF channel of the Halmahera Sea. Therefore, the
dynamics of oceanography in the Maluku Sea, Halmahera Sea, and the Pacific Ocean directly

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affect the water condition at the study site.

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Figure 1. Study Site in: 1). Hiri Island, 2). Ternate Island, 3). Maitara Island, 4). Tidore
Island, 5). England Island, 6). Plun Island, 7). Lelewi Island, 8). Pakal Island
2.2. Spatial Distribution of Shallow Water Benthic and Seafloor Topography
Data on the spatial distribution of shallow water habitats, sourced from Sentinel 2B
satellite imagery with a spatial resolution of 10 m, were acquired on March 5, 2021. The
satellite imagery was then processed in QGIS version 3.16 Hannover (Flenniken et al., 2020).
Using a vector machine classification algorithm to obtain shallow water habitat classification
results on eight islands . Topographical data of the waters are obtained from the results of
depth measurements (bathymetry sounding) using a GPS sounder.

2.3. Coral Cover and Diversity

Coral data was collected using SCUBA diving equipment, a measuring tape 50 m
long, a quadrat 50 cm x 50 cm, and an underwater camera to study and document hard coral
cover in coral reef ecosystems. Data were collected at 5, 10, and 15m water depths. The
method used for coral data collection wais the underwater photo transect, with a distance
between the quadrat for taking the photo transect of 1 m (Giyanto et al., 2010). We obtained

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1550 photo transects from 31 observation transects at 16 research sites on eight islands.
Photographs per quadrat on each transect were then analyzed using the Coral Point Count

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with Excel Extensions software to calculate the percentage of coral cover and diversity of
coral life forms, twenty-five points were used in each quadrat, determined regularly (Kohler
and Gill, 2006). Thirteen hard coral benthic groups were analyzed for this study (Table 2)
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(English et al., 1998). The value of benthic diversity life forms refers to the diversity index
assessment category, namely the Shannon-Weiner (H') diversity index with categories H ≤ 1
(low), 1≤H≤3 (medium), and H ≥ 3 (high) (Odum and Barrett, 1971). The results of the
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percentage of coral cover were then analyzed using the statistical application model R.
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2.4. Acquisition of Environmental Parameter Data

We measured aquatic environmental parameters, or water quality, at 5, 10, and 15 m
depths. Water was sampled at every depth using a Niskin water sampler (General Oceanic
model 1010). Water samples were analyzed using a water quality checker to obtain
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temperature, salinity, pH, and dissolved oxygen (DO) values. Visibility parameters were
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observed using Sechi Disc.

2.5. Statistical Analysis

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We used analysis of variance (ANOVA) and Principal Component Analysis (PCA)

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with R Software (R Core Team, 2021). asbio package (Aho, 2023), MASS (Venables and
Ripley, 2002), FaktoMiner (Lê et al., 2008), factoexsta (Kassambara and Mundt, 2020), and
ggplot2 (Wickham, 2011) for statistical analysis. We used one-way ANOVA for hard coral
(HC) analysis between sites; and two-way ANOVA to examine benthic life forms of hard
corals based on site and depth factors as well as the interaction between sites and depth. We
also tested for normality using Bartlett's K-squared test and the homogeneity test for diversity
using the Ligner-Killeenmed chi-squared test. PCA wais used to describes the two sites based
on HC and environmental factors.

3. Results
3.1. Shallow Water Habitat (Coral Habitat Distribution)

The total area of shallow water habitat (coral habitat distribution) in Buli Bay was
532,93 ha, and the Termadoreh Islands was 1.313,99 ha (Table 1).
Table 1. Shallow water habitats (ha) and Geomorphic zone type

Shallow water habitats area (ha)

Geomorphic
Site Island Sand Mixed
Sand Coral Seagrass Zones Type
Seagrass
Reef Crest, Reef
Hiri 2,29 139,87 1,5 -
Slope
Reef Crest, Reef
Ternate 58,2 541,77 26,7 20,41
Slope
Termadoreh
Reef Flat, Reef
Maitara 7,83 91,1 18,03 -
Crest, Reef Slope
Reef Crest, Reef
Tidore 10,83 541,25 40,93 1,4
Slope
Total 79,15 1.313,99 87,16 21,81

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Englan 49,59 222,48 236,33 75,68 Reef Flat
Reef Flat, Reef
Lelewi 6,15 68,28 19,06 14,49
Crest, Reef Slope

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Buli Bay Reef Flat, Reef
Plun 7,7 63,49 22,11 18,86
Crest, Reef Slope
Reef Flat, Reef

Total
Pakal 27,69
91,13
178,68
532,93
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336,28 109,03
-
Crest, Reef Slope
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3.2. Percentage of HCC and Aquatic Environmental Factors
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The percentage of coral cover was calculated at different depths for each of the 16
observation sites at the two sites. We analyzed its distribution in different geomorphic zones:
reef flats, crests, and slopes. The percentage cover of HC differed sites and depths. In
Termadoreh, the percentage of HC ranges from 14,09% to 71,60%. The highest HC was
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found at the MaT06 site at 71,60%, and a very high Acropora brancing (ACB) cover was
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dominated by Isopora brueggemanni (Wallace, 1997). In Buli Bay, the highest percentage of
coral cover was found on England Island at the EB02 site (61.04%), dominated by the ACB.
The lowest was found on Lelewi Island at the the LB05 site at 34,74%, with the dominant life
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form being Coral Foliouse (CF) (Figure 2). The distribution of HC in different geomorphic
zones at both sites was described as such that ACB and CM were predominantly found in the
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reef slope zone at both study sites (Figure 3). The CF in Termadoreh was dominant in the reef
slope zone, whereas in Buli Bay, it was dominant in the reef crest and slope. The reef crest
zone at both sites was dominanted by coral submassive..
 Figure 2. Hard coral cover (HCC) distribution map in research sites

The aquatic environment parameters showed that the average value of water visibility
varied between the sites (Table 2). In Buli Bay waters, water visibility ranges from 6-25 m,
whereas in Termadoreh waters, it is 17-25 m. The highest average visibility value was found
in Termadoreh waters (23 m). The temperature difference between the highest sites on Pakal
Island (PkB08) was 27,990C, and the lowest on Ternate Island (TeT03) was 26.230C. Salinity
values at the two study sites ranged from 29.65 to 30.88‰. The highest mean salinity value
was in Buli Bay at 30.63‰ and the lowest eas in Termadoreh (29.95‰). The highest DO
value among the sites was found on Tidore Island (9,19 mg/L) and the lowest on Ternate
Island (7.2 mg/L). The highest pH value was recorded on England Island at site EB01 (8.11)
and the lowest on Lelewi Island at site LB06 (7,27).

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Table 2. Average values of hard coral (HC), diversity Index (H'), and environment parameters (temperature,
salinity, dissolved oxygen (DO), pH, and visibility).

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Percent Cover of Hard Coral Life Form (%) Environment Parameter
Area
Sit
e
HC
(%)
H
’

0.
A
C
B
A
C
D
A
C
E
A
C
S
A
C
T
C
B
C
E
C
F-p C
H
L
C
M
C
M
E
C
M
R
C
S
0.
T
(0
C)
S
(pp
t)
DO
(mg/
L)
p
H
8.
Vis
(m)
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Buli EB 55. 43 0. 11 0. 26.
3 0 0 0 0 0 0 0 0 3 30 9 1 4
Bay 01 44 .2 64 .2 08 75
3 2 1
3. 0.
Buli EB 61. 0. 5. 8. 20 8. 1. 2. 1. 7. 0. 27. 30. 7.
0 8 0 8 9.12 4
Bay 02 04 7 7 64 .2 32 92 52 86 12 08 57 68 5
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6 2
Pl 0. 1. 0. 7.
Buli 40. 29 0. 0. 4. 0. 0. 0. 2. 0. 26. 30.
B0 6 8 0 0 4 9.07 8 17
Bay 32 .3 08 04 4 29 16 49 84 37 65 88
3 9 7 8 3
Pl 0. 24 11 1. 1. 7.
Buli 54. 0. 2. 3. 0. 8. 0. 26. 30.
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B0 7 .6 0 .2 4 0 0 1 8.9 7 17
Bay 22 48 5 65 66 25 18 75 67
4 4 6 8 4 2 2
0. 22 0. 7.
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Buli LB 34. 0. 6. 0. 0. 0. 3. 0. 0. 0. 0. 26. 30.

0 4 .5 0 8.82 7 15
Bay 05 74 7 75 08 08 28 44 09 52 04 4 87 58
8 4 4 8
0. 17 0. 24 0. 7.
Buli LB 49. 0. 0. 0. 3. 1. 0. 26. 30.
7 .5 0 8 .9 0 0 0 8.98 2 15
Bay 06 48 24 08 32 08 6 76 76 84
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1 6 4 2 8 7
Pk 0. 2. 10 12 1. 7.
Buli 46. 9. 0. 1. 0. 5. 0. 26. 30.
B0 7 0 3 .7 0 .8 0 6 7.66 5 25
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Bay 36 07 8 24 93 82 98 97 71
7 6 6 2 1 3 5
Pk 0. 10 5. 16 1.
Buli 52. 4. 2. 1. 2. 2. 3. 0. 0. 27. 30. 7.
B0 9 .8 3 .4 0 1 7.8 6
Bay 27 67 27 09 84 67 84 58 57 99 69 6
8 1 4 2 1 7
Term 0. 11 0. 2. 7.
HT 34. 7. 0. 3. 2. 1. 4. 0. 0. 27. 30.
adore 8 0 .4 2 0 4 8.75 5 23
01 91 88 04 74 35 52 04 92 24 18 07
h 5 8 5 5 8
Term 1. 0. 2. 7.
HT 30. 1. 1. 1. 14 1. 5. 0. 0. 26. 30.
adore 1 0 0 0 0 4 7.83 5 24
02 51 4 27 92 .9 73 48 32 92 79 14
h 5 8 9 3
Term Te 0. 1. 31 0. 7.
44. 1. 0. 3. 0. 2. 1. 26. 30.
adore T0 6 0 0 0 0 .6 0 3 8.63 6 23
28 38 57 64 96 67 96 41 08
h 3 9 6 8 6 3
Term Te 0. 0. 3. 7.
30. 6. 0. 0. 6. 1. 1. 8. 0. 26. 29.
adore T0 9 0 7 0 0 3 8.5 7 17
36 32 47 66 52 68 96 46 14 23 65
h 4 3 9 6 3
Term Ma 0. 0. 0. 7.
71. 38 1. 13 8. 6. 0. 1. 0. 0. 26. 29.
adore T0 6 0 4 0 3 6.9 6 23
6 .4 54 .2 08 32 72 68 78 08 26 88
h 5 1 8 2 9
Term Ma 0. 32 4. 7.
58. 0. 1. 0. 0. 26. 30.
adore T0 6 .7 0 0 0 0 18 0 0 6 7.2 3 25
48 24 73 14 96 39 05
h 6 4 2 9 8
Term Ti 14. 1. 2. 0. 0. 0. 0. 0. 3. 1. 5. 0. 0. 26. 30. 7.
0 0 9.16 25
adore T0 57 0 36 04 24 04 32 23 4 68 53 18 5 52 03 6
h 7 8 3 2 4
Term Ti 0. 0. 7.
14. 0. 0. 0. 0. 0. 3. 2. 3. 2. 26. 29.
adore T0 0 2 0 0 8 9.19 6 24
09 8 08 08 16 17 84 68 23 69 56 72
h 8 7 9 7
Note :
HC = Total percentage cover of hard coral life form CF = Coral Folious
DO = dissolved oxygen (mg/L)
H’ = Diversity Index CHL = Coral Heliopora
pH = Potential Hidrogen
ACB = Acropora branching CM = Coral Massive
Visibility = Visibility (m)
ACD = Acropora digitate CME = Coral Meliopora

ACE = Acropora Encrusting CMR = Coral Mushroom

ACS = Acropora Submassive CS = Coral submassive
ACT = Acropora Tabulate T = Temperature (0C)

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CB = Coral Branching ` S = Salinity (ppt)
CE = Coral Encrusting

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Figure 3. Sea bottom topography profile and HCC in the research site
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3.3. Differences in the Distribution of Hard Coral Cover

Before the data were analyzed, we performed a normality test using Bartlett's K-
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squared test and a homogeneity test for diversity using the Fligner-Killeenmed chi-squared
test. We also tested depth and site using a two-way ANOVA. The results of the normality test
showed that the HC data between sites showed no difference or were normal with a p-value
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of 0,8 (p < 0,05), and the results of the homogeneity test showed homogeneous data with a p-
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value of 0,703 (p < 0,05). The ANOVA results showed that the HC differed significantly
between the Teluk Buli and Termadoreh sites differed significantly with a p-value < 0.01 (p
<0.05).

The results of the two-way ANOVA analysis between HC and environmental factor
with site and depth shiw that the bottom HCC and diversity index (H') differ significantly
between sites (Table 3). Acropora branching was significantly different between sites,
however is was not different between depths. However, CF was not significantly different
between sites, however it was significantly different between depths. Corals Heliopora and
Millepora were not significantly different among sites, depths, or interactions between sites
and depths. The diversity of coral life forms (H') was significantly different between sites and
highly significantly different in the interaction between site and depth.
Table 3. Two-Way ANOVA test HCC, H’, and benthic life form hard coral based on site
depth and interaction between site and depth (p <0.05*)

Area Depth Area x depth

Variable
F p-value F p-value F p-value
Hard Coral (HC) 45.858 0.000* 7.172 0.007* 25.080 0.000*
Acropora branching (ACB) 7.430 0.006* 1.218 0.269 4.785 0.028*
Acropora digitate (ACD) 21.666 0.000* 16.083 0.000* 9.254 0.002*
Acropora encrusting (ACE) 4.038 0.044* 0.109 0.741 3.319 0.069
Acropira submassive (ACS) 7.062 0.007* 42.876 0.000* 0.139 0.709
Acropora tabulate (ACT) 9.583 0.001* 0.657 0.417 8.229 0.004*
Coral branching (CB) 14.151 0.000* 11.204 0.000* 1.640 0.200
Coral encrusting (CE) 27.279 0.000* 5.242 0.022* 5.784 0.016*
Coral folious (CF) 0.682 0.408 6.777 0.009* 129.448 0.000*

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Coral heliofora (CHL) 0.188 0.664 2.453 0.117 0.036 0.848
Coral massive (CM) 45.938 0.000* 2.3615 0.124 37.831 0.000*
Coral milepora (CME) 2.888 0.089 0.273 0.060 0.456 0.499

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Coral mushroom (CMR) 8.779 0.003* 0.550 0.458 0.041 0.838
Coral submassive (CS) 18.505 0.000* 19.462 .000* 11.428 .000*
H’ Bentic Life Form 27.982 0.000* 4.405 0.035* 43.198 0.000*
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The results of the ANOVA test on HC, suggested that the HCC was significantly
different between the sites. We then conducted further tests using Tukey‘s Post Hoc tes on
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HCC. The test results showed that sites with the same letters were not significantly different,
whereas sites with different letters showed statistically significant differences. All sites
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differed from the TiT07 and TiT08 sites (Figure 4). Each island had a similar percentage of
HCC, except for Lelewi Island, where the sites on the island were different.
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Figure 4. Result of analysis using Turkey’s Post Hoc test on HCC between sites: the x-axis is
a site, and the y-axis is the HCC presentation.

3.4. Environmental Factors Driving the Distribution of Hard Coral Cover

We analyzed the main environmental factors driving the distribution of hard coral
cover. The analysis showed that the Buli Bay has a high temperatures, salinity, and HC
differntiation (Table 4 and Figure 5). Although Termadoreh is distinguished by its high
visibility and diversity of benthic life forms, DO and pH were not distinguishable between
these two locations. The principal components (Figure 5) of axes 1 was main Component 1
(Dim 1) and main Component 2 (Dim 2) explain 58.7% of data variability. The variables
strongly correlated with (Dim 1) were HC, H, visibility, temperature, and salinity.

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Figure 5. Principal Component Analyisis (PCA) - Biplot : Correlation between Hard Coral
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(HC), Diversity Indix (H’), and environmental factors (Visibility, disolved oxygen [DO], pH,
and temperature) with the main axis

Table 4. Loading vector Principal Component Analysis value

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Variable Dim.1 Dim.2 Dim.3 Dim.4 Dim.5 Dim.6 Dim.7

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HC 0.67 -0.10 -0.70 0.02 -0.06 -0.11 0.17

H -0.57 0.66 0.28 -0.29 0.09 -0.23 0.08
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Temperature 0.65 0.57 0.24 -0.36 -0.02 0.25 0.05

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Salinity 0.66 0.50 0.09 0.40 0.38 -0.06 -0.04

DO 0.13 -0.15 0.88 0.36 -0.19 0.00 0.12
pH 0.18 -0.79 0.34 -0.29 0.38 -0.01 0.05
Visibility -0.87 0.11 -0.28 0.24 0.22 0.21 0.11

4. Discussion

4.1. Spatial Distribution of Hard Coral Cover

Our study of hard coral cover distribution was initiated by studying the spatial
distribution of shallow water habitats using satellite imagery. As rsult, the total area of
benthic coral habitat in the Termadoreh Islands was large than that in Buli Bay. The total area
of benthic coral habitat in the Termadoreh Islands is 1.313,99 ha, whereas in Buli Bay it is
532.93 ha. Based on the results of this analysis and the free-roaming survey, we selected 16
observasion sites to study the distribution of hard coral in the study area. The highest
percentage of hard coral was found in Buli Bay, and the lowest is in the Termadoreh Islands.
 The percentage cover of Acropora branching corals (genus Acropora) was the main
contributor to Buli Bay’s high percentage cover of HC’s. The highest ACB was found on
England Island near the main land and the lowest on Plun Island off the coast. Massive corals
(genus Porites) and folius corals (genus Montipora) were dominate at the Pakal Island site.
Coral development in the Gulf differs markedly between onshore and offshore island owing
to development of basin geology, sea level variation, and climite change. It is dominant by
fringing reefs with high diversity in flat are facing the open sea (Purkis and Riegl, 2012). This
may vary due to the complexity of the aquatic environment. Water areas near land are under
strong pressure from local anthropogenic stressors. Thus, the spatial structure of coral reefs is
directly related to anthropogenic solid pressure originating from local and regional sources
(Baum et al., 2015).
We found hard coral cover in Buli Bay spread across the reef flat, reef crest, and reef
slope zones. Generally, hard corals are found spreading from the reef flat to the reef slope at a
depth of 12 m (Wallace, 2011). The percentage of hard coral cover is higher in the upper part

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of the reef (Fahlevy et al., 2019). Acropora branching is a coral life form that is dominantly
distributed on reef slopes in fringing reef areas. This indicated that geomorphic zones

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influence the composition and structure of coral communities in aquatic environments
(Latypov, 2016; Zawada et al., 2010).
The water of the Buli Bay have unique oceanographic characteristic. The water is
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calm, the current speed is weak, and the topography is sloping, causing the ACB was
dominant (Latypov, 2016). In these waters, there is a nickel exploitation area with a high
level of turbidity (total susvended solids [TSS] 40 mg/L), corals adapt to turbid water
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conditions. CM and CF dominant because they can adapt to these extreme conditions
(Montagne et al., 2013). However, corals experience morphological adaptation. CF forms
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wider leaves, and the CM (Porites species) is large and sturdy. Which is a morphological
adaptation to extreme conditions in the form of limited sunlight due to high turbidity s (Lowe
and Falter, 2015).
The distribution of hard coral life forms varies between water depths on the volcanic
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islands of the Termadoreh Islands. We found differences in coral diversity among

topographies based on analysis of coral distribution in each coral reef geomorphic zone
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(Kennedy et al., 2021; Medina-Valmaseda et al., 2022). Hard corals were more diverse on
reef slopes areas than reef flat areas. Branching corals are dominantly found on reef flats and
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peaks, while Acropora branching (genus Acropora) and corals massive (genus Porites) are
dominant on reef slopes. The CF was dominant on the reef flats at the TeT03 site, whereas at
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site MaT05 and MaT06, it was dominantly distributed on the reef slope. The highest
percentage of HC was found at the MaT05 location (71.60%), dominated by branching
Acropora (genus Acropora), and at MaT06 (58.48%), dominated by CF (genus Montipora).
The distribution of coral community structures varies depending on topography and wave
exposure areas. In slope areas where wave exposure is low or the waters tend to be calm, it is
dominated by prites with the highest hard coral cover values. ACB and CM dominate the area
exposed to waves. The slopes affected by the dominant waves were found to be isopores.
Areas with low levels of HC are dominated by corals that are tolerant to pressure and are
highly adaptable (Feliciano et al., 2023).
The percentage of Coral Folious cover (genus Montipora) was higher in protected
shallow and deep waters with steep topography. The site factor contributed significantly to
the differences in coral distribution and differences in coral geomorphic zones. Wave
exposure factors also affect coral distribution patterns (Medina-Valmaseda et al., 2022).
Additionally, different types of coral morphologies at the same depth experience
spatiotemporal variations in the hydrodynamics of different waters (Galbraith et al., 2022).
 Benthic hard coral life forms more diverse on the Termadoreh Islands. The hard coral
cover varied with increasing depth, except at the MaT06 site. The pattern of fringing coral
reef habitat zones around volcanic islands is distributed on a seaward sloping topography, and
a coral cover dominates the reef slopes. There are differences between reef flat, crest, and
slopes because they are influenced by hydrological, physical, and biological conditions (Kim
et al., 2022). The topographical and oceanographic factors of the waters encourage the
formation of distribution zones of benthic hard coral life forms based on depth (Done, 1983).

4.2. Correlation of Environmental Factors with Spatial Distribution of Corals

The small islands in Buli Bay are located in a semi-enclosed water area with relatively
calm oceanographic dynamics. The complexity of the archipelago's bathymetry, hydrology,
and geological history indicates the possibility of developing a unique coral community.
(Feliciano et al., 2023).The dynamics of oceanography directly influence this area in the

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Pacific Ocean through the Halmahera Sea. We found that the bottom topography of the small
islands is sloping with a depth of 3 to 7 m, while the slope is at a depth of 8 to 15 m. Reefs
and slopes are dominated by hard coral cover. The life forms ACB, ACS, and CF (Figure 3)

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were dominant on reef flat, while hard coral life forms were more diverse on slopes. The
distribution of hard coral cover is determined by bottom topography and aquatic

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environmental factors. Physical and biological processes in water at various spatial scales are
influenced by the complexity of the topography of the water bottom (Zawada et al., 2010).
The distribution of hard coral cover is influenced by bottom topography and aquatic
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environmental factors at various spatial scales (Zawada et al., 2010). Reef flats are one of the
largest and most distinctive habitats on coral reefs. They are highly vulnerable to predation,
face challenging hydrodynamic constraints, and are covered by sediment. Reef flats are the
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most important habitat for various organisms in shallow waters. Contributing to a ninefold
increase in populations of shallow water organisms from an evolutionary and ecological
perspective (Bellwood et al., 2018).
The average percentage of hard coral cover differed between sites, with the highest
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recorded in Buli Bay and the lowest recorded in the Termadoreh Islands. This difference is
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primarily caused by environmental factors that limit coral growth. The main environmental
parameters that contribute to the high percentage of HC coral cover in Buli Bay are
temperature (26,650C-27,990C), DO (7,66-9,12), salinity (30,00‰-30,88‰), and pH (7,27-
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8,11). The Termadoreh Islands had the lowest percentage of hard coral cover. However, the
highest life form (H') diversity value and the visibility variable contributed to the high
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diversity value in that site. Differences in coral communities are due to environmental
gradients, namely temperature, visibility, and related organic matter upwelling-downwelling
and dynamics from the mainland (Guadayol et al., 2014; McClanahan et al., 2002). Coral
reefs thrive at moderate temperatures (Brandl et al., 2019). In addition, the coral composition
is correlated with sea surface temperature (Veron and Minchin, 1992). Environmental factors
are the main driving forces in ecological processes, where the hardness of the waters is the
main factor for coral growth and development and contributes to the processes of
photosynthesis and calcification, which encourages the creation of coral reef diversity
(Guadayol et al., 2014; Pratchett et al., 2015).
Differences in the spatial distribution of corals and the percentage of hard coral cover
between sites were also caused by anthropogenic activities. The dominant coral life forms
found in both sites were Acropora branching (genus Acropora), Coral Folious (genus
Montipora), and Coral massive (genus Porites). The islands in Buli Bay are uninhabited
islands with low anthropogenic activity, except for Pakal Island, a site for nickel exploitation.
The islands of Termadoreh are inhabited, especially those of Ternate and Tidore, with dense
populations. It was found that there was a damaged coral reef ecosystem in the waters of
Termadoreh, and this damage was allegedly caused by fishing activities using bombs and
potassium cyanide in the past. Anthropogenic activities threaten coral reef ecosystems (Prada
et al., 2019). Human pressure causes habitat degradation, shifts in species composition, and
decreased coral abundance (A. El-Naggar, 2021; Eddy et al., 2021; Hoegh-Guldberg et al.,
2019). Gradient factors influence the condition of the coral reef ecosystem in the aquatic
environment and local stressors. Thus, the response of reef habitats to local stress conditions
will vary widely. Local pressure factors that affect coral reef ecosystems are fishing,
anthropogenic activities in urban areas, and predation by predatory fish. Reef habitats that
experience high stress are those on the slopes of the reef (Houk et al., 2015). This condition
will cause differences in the percentage of coral cover at the research location.
There were differences in the percentage of hard coral cover between sites in the two
study areas. The highest was at Termadoreh site MaT05 at 71.60%; Acropora was the
dominant genus found. This site is a volcanic island located between Ternate Island and
Tidore Island. Visibility and ocean currents are environmental factors that encourage a high

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percentage of hard coral cover. Water visibility, pH, and DO are the best environmental
conditions for coral growth (Zamani and Januar, 2020). Corals of the genus Acropora grow

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and develop around volcanoes, exhibit low spatial competition, and are influenced by nutrient
enrichment (Takahashi and Shoji, 2002; Tomascik et al., 1996). The main environmental
factors that contribute to the spatial distribution of hard corals in Buli Bay are temperature
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and brightness. ACB is dominantly found at this location. The spatiotemporal distribution of
ACB corals is influenced by water temperature conditions (Anderson et al., 2017). Hard
corals (HC) have different abilities between species in responding to changes in water
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temperature (Carballo-Bolaños et al., 2020).
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4.3. Research Implications

The mapping describes the spatial distribution of benthic habitats, including coral reef
habitats. This information is important for policymakers because it informs them of the
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distribution of benthic habitats in the waters of the small islands of Halmahera and can be
used as a reference for formulating management plans for coastal resources and small islands.
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This information can be used as initial data to determine the conservation areas for coral reef
ecosystems in the waters of the small islands of Halmahera.
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The distribution of hard corals, the percentage of hard coral life form cover, and their
diversity values provide important information that describes the current condition of coral
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reef ecosystems. The results of this study can be used as a reference for assessing the
condition of coral reef ecosystems and predicting future conditions. This information
determines whether coral reef ecosystems must be restored or rehabilitated. Restoration is an
approach to restoring coral reef ecosystems to their natural condition. The rehabilitation of
coral reef ecosystems is an approach for repairing damaged coral reef ecosystem areas
through coral transplantation activities and artificial reefs..

5. Conclusion
Hard corals are distributed in the geomorphology of volcanic islands and atolls around
Halmahera Island, the center of the coral reef triangle. The Termadoreh Archipelago is a
volcanic island, and the islands in Buli Bay are a coral island. Differences in the topography
of different island types affect hard coral cover distribution in coral geomorphic zones.
The spatial distribution of hard coral cover was influenced by bottom topography and
aquatic environmental parameters, and the reef slope was the reef geomorphic zone with the
highest distribution of hard coral cover. The Coral Folious cover was higher in the protected
shallow and deep waters. The highest percentage of coral cover for Acropora branching
(genus Acropora) is found in Buli Bay and was influenced by environmental factor values,
such as temperature and salinity. The highest value of diversity (H') was found in the
Termadoreh Islands, which are influenced by the high value of the water's visibility. There
were differences in the percentage of hard coral cover and environmental factors between
Buli Bay and the Termadoreh Islands. Differences in water characteristics, geographical
location, geomorphology, and bottom topography were found to be related to water quality,
coral habitat complexity, and differences in coral distribution.

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.

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Author Statement

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All persons who meet authorship criteria are listed as authors, and all authors certify that they
have participated sufficiently in the work to take public responsibility for the content, including
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participation in the concept, design, analysis, writing, or revision of the manuscript. Furthermore,
each author certifies that this material or similar material has not been and will not be submitted
to or published in any other publication before its appearance in the Regional Studes In Marine
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Science.

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