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DOI: 10.1166/asl.2017.9155

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Copyright © 2017 American Scientific Publishers Advanced Science Letters

All rights reserved Vol.23 (4), p3277-p3282(6), 2017
Printed in the United States of America

Mangrove Health Index as Part of Sustainable Management

in Mangrove Ecosystem at Karimunjawa National
Marine Park Indonesia

Johan Danu Prasetya1*, Ambariyanto2,3, Supriharyono2, Frida Purwanti2.

1
Environmental Engineering, the Universitas Pembangunan Nasional “Veteran” Yogyakarta. 55283, Indonesia.
2
Faculty of Fisheries and Marine Sciences, Diponegoro University, Semarang 50275, Indonesia
3
Coastal Disaster Rehabilitation and Mitigation Center, Diponegoro University, Semarang 50275, Indonesia.

Abstract
Background: Monitoring the health of marine ecosystems is an integral part of sustainable management of the
ecosystems including mangrove. Distribution and diversity of mangrove ecosystems are two important parameters
in Mangrove Health Index (MHI). The index analyses value of mangrove density, diversity, index of similarity
and the number of mangrove species.
Method: This study investigates mangrove distribution and diversity. Mangrove distribution maps were prepared
using Satellite imagery GEO-EYE. Ecological surveys to analyze the diversity of mangrove at five locations,
namely Legon Cilik, Legon Gede, Kemujan, Karimunjawa and Menjangan Besar. MHI was calculated by
assigning weight for each parameter, multiplied by each parameter score and then summing all of multiplication
results value.
Results: Satellite image interpretation results showed that mangroves were found at island of Karimunjawa,
Menjangan Besar and Sintok. In total, 22 mangrove species identified, 12 species were true mangroves and the
rests were mangrove associates. Rhizophora apiculata dominates three of nine survey locations, while Rhizophora
stylosa was the dominant species in two of nine locations and the rest are dominated by Ceriops tagal, Lumnitzera
racemosa, Rhizophora mucronata and Sonneratia alba. Density of mangrove in the category of tree, mangrove
average density ranging from medium to high, from 230 to 1060 ind/ha. In the category of sapling, dominant
mangrove species was relatively diverse. In general, the Shannon diversity index was low, it means that mangrove
diversity is low, it means that mangrove diversity is low. Mangrove in Legon Cilik 1 and Menjangan Besar had
the highest Shannon diversity index (1,09) while Karimun 1 were the lowest (0,18).
Conclusion: The value of MHI at Karimunjawa was 200, which is in the medium category. The results suggest
that there is a need to improve MHI as part of sustainable management based on the distribution and diversity of
mangrove.

Keywords: Mangrove Health Index, Distribution, Diversity, Sustainable Management, Karimunjawa Islands.

1. INTRODUCTION as provide protection from erosion and flooding,

Mangrove is one of the important coastal
ecosystems which has a great ecological and
economic importance1. Mangrove possess a high
diversity and abundance of organisms2,3.
The ecological function of mangrove are as
nursery and feeding areas of marine fishes4–8, as well
* Email: johan.danu@upnyk.ac.id.
buffer salinity changes and intrusion9.
Indonesia has the highest diversity with 43 true
mangrove species10, however facing various threats
from nature and human9. For example, large areas of
mangrove have been converted into oil palm
plantations in Malaysia and Indonesia 9. Over half of
the mangrove in Indonesia have been converted for
aquaculture11, timber extraction and the expansion of
urban areas12.

1 Adv.Sci.Lett.Vol.23,No.4,2017 doi:10.1166/asl.2017.9155 1

High density, high diversity, low species
similarity and high number of mangrove species,
describe mangrove ecosystem healthy. Healthy
mangrove ecosystem provides maximum benefits
for biodiversity, therefore, maintaining mangrove in
a healthy condition can be interpreted as sustaining
biodiversity. One of the tool to conserve mangrove
is Marine Protected Area (MPA). Monitoring the
condition of the ecosystems periodically is one of the
important programs, not only in tracking ecosystem
status but also evaluate the effectiveness of MPA13.
The result of monitoring should be the primary
consideration in MPA management. Implementation
diversity based conservation management through
periodically diversity monitoring is important
particularly in the area of the richest biological
diversity14, such as Indonesia which is known as the
center of mega-biodiversity 15,16.
Karimunjawa National Park (KNP) was an
important Marine Protected Areas for the
conservation of marine biodiversity in Indonesia.
KNP consists of 22 islands and some of those islands
are inhabited17, most of the local people rely on
marine resources. KNP has five types ecosystems,
consisting of coral reef, seagrass, mangrove forest,
beach forest and low-land tropical forest18.
Figure 1. Field surveys locations
Mangrove area in KNP is about 400 ha, concentrated
in the Karimunjawa and Kemujan Island.
Monitoring programs which to document
dynamics and generate data are essential for
management and decision-making in conservation
management. Monitoring the status and condition of
2 Adv.Sci.Lett.Vol.23,No.4,2017
RESEARCH ARTICLE
mangrove is an integral part of sustainable
management of the ecosystems. Sustained
monitoring programs will improve our understanding
health status and trends of mangrove. Single value of
monitoring result can describe mangrove health
condition more obvious. This single value approach
from data sets aims to portrayal of mangrove
ecological dynamics. We introduce an index of
mangrove condition that takes into account the
diversity of mangrove ecosystem. The study aims to
investigate mangrove distribution and diversity then
propose single value index based on ecological data,
called Mangrove Health Index (MHI), as a part of
sustainable management of mangrove ecosystem at
Karimunjawa National Park.
2. METHOD
This study mapped the percent cover and
distribution of mangrove using satellite imagery Geo-
Eye and followed by investigation of mangrove
distribution and abundance using ecological surveys
(See Fig. 1).
Satellite image interpretations were done at several
islands at KNP, i.e. Cemara Kecil, Cemara Besar,
Krakal Besar, Krakal Kecil, Cilik, Sintok, Menjangan
Besar, Menjangan Kecil, Tengah and Karimunjawa
with a total area of 3.752 ha. While ecological surveys
of mangrove distribution and abundance were
doi:10.1166/asl.2017.9155 2
 RESEARCH ARTICLE

conducted at Karimunjawa Island and Menjangan 3. RESULTS

Besar Island, consist of nine sampling location i.e.
Composition & Average Density of Mangrove
Legon Cilik 1 & 2, Legon Gede 1 & 2, Kemujan 1 &
2, Karimunjawa 1 & 2 and Menjangan Besar. Total of 22 mangrove species were identified in the
Field measurement used line transect and study site. In which 12 species were true mangroves
vegetation transect plot method 19. There were were identified, i.e.: Rhizophora apiculata,
transects-line, vertical against the coastal line Rhizophora mucronata, Rhizophora stylosa,
landward. Nine vegetation transects plot in nine Avicennia marina, Sonneratia alba, Sonneratia
sampling location were applied. Vegetation transect caseolaris, Xylocarpus granatum, Xylocarpus
plot of 10x10 m (100 m2) were applied in each muloccensis, Lumnitzera racemosa, Ceripos tagal,
locations. Field measurements in the field were Ceriops decandra, Bruguiera cylindrica. Whereas 3
designed with 1x1 m, 5x5 m and 10x10 m plot size. species were minor mangrove, i.e.: Acrostichum
In each 100 m2 vegetation transect plot, the total aureum, Excoecaria agallocha, Pemphis acidula and
number of mangrove tree species and associated 7 species were mangrove associates i.e.: Acanthus
vegetation as well as the number of individual of ilicifolius, Calophyllum inophyllum, Pandanus
each species were determined. Field measurements tectorius, Scaevola taccada, Sesuvium
are trunk diameter, tree height and mangrove portulacastrum, Ipomea pes-caprae, Hibiscus
species. The species composition was identified tiliaceus.
based on the species of mangrove found in the study Identified species were also categorized into true
site. Species identification was done based on mangrove trees, saplings, seedlings and mangrove-
Kitamura et al. (1997)20. associated species. The number of species founded in
Mangrove mapping was done through several each sampling location ranging from 2 to 5 species per
processing stages i.e. image restoration, sampling location. The highest mangrove tree
enhancement and classification. Image restoration category was R. apiculata with 2200 individu/ha. The
was done by correcting the image radiometrically n most abundant generating species were R. mucronata
geometrically21. Radiometric calibration were done and R. stylosa in sapling category whereas in seedling
by converting digital numbers to radiance values22. category was R. stylosa. (See Table 1).
Geometric corrections were done in order to adjust Table 1. The Mangrove Average Density
the coordinates to geographic coordinates. Image
enhancement was carried out after disruption TLS AD (in 1000)
Species
radiometric and geometric adjusted. While image A B C A B C
classification using supervised classification done by S. alba 3 1 0 0.23 0.40 0.00
using training area that represents each of the
R. mucronata 4 3 6 0.63 3.07 80.00
required information. Determination of the number
and types of land cover was done based on color R. stylosa 5 3 4 0.90 2.40 360.00
variations. Supervised classification is the most R. apiculata 5 6 4 1.06 2.03 22.50
proper approach versus non-supervised C. tagal 3 4 3 0.60 0.80 56.67
approaches23. X. granatum 3 2 1 0.47 0.40 20.00
The value of mangrove density was calculated L. racemosa 2 1 0 0.25 0.80 0.00
based on formula used by Mueller-Dombois and
Ellenberg24. While diversity, similarity, and relative TLS : Total Location Sampling
dominancy were calculated using the formula of AD : Average Density
Shannon-Wiener, Pielou, and Simpson, A: Trees; B: Saplings; C: Seedlings
respectively25. Mangrove Health Index was
calculated by assigning weight for each parameter Diversity, Similarity & Relative Dominancy
based on expert judgment. Parameter weights are
determined by expert judgment based on the Legon Cilik 1, has the highest diversity indices with
importance of a parameter to the mangrove 1,091, while Menjangan Besar has the lowest with
ecosystem health. Each weighted parameter was 0,191. Legon Cilik and Kemujan, location that have
multiplied by each parameter score and then high mangrove density, was located in Karimunjawa
summing all of multiplication results value to get Island. Overall, mangrove density was higher in the
Mangrove Health Index. Parameters that be used in Karimunjawa Island than in the Menjangan Besar.
MHI calculation are mangrove density, diversity R. apiculata was the most abundance species that
index, index of similarity and the number of dominated in several location (See Table 2).
mangrove species.

3 Adv.Sci.Lett.Vol.23,No.4,2017 doi:10.1166/asl.2017.9155 3
 RESEARCH ARTICLE

Table 2. Diversity, Similarity, Relative Dominancy Mangrove Health Index

Station H' E' DS RD (%) The index analyses value of mangrove density,
Legon Cilik 1 1.09 0.41 R. apiculata 72,73 diversity index, index of similarity and the number of
mangrove species. MHI calculated from total
Legon Cilik 2 0.47 0.16 R. apiculata 88,48
multiplication of Weight n Score of each parameters.
Legon Gede 1 0.99 0.31 C. tagal 45,02 MHI value of KNP is in the medium category (200)
Legon Gede 2 0.64 0.21 X. granatum 50,29 (See Table. 4).
Kemujan 1 1.00 0.30 S. alba 54,67 Table 4. Mangrove Health Index
Kemujan 2 0.99 0.34 R. stylosa 59,09 Parameter Weight Score Weight X Score
Karimun 1 0.18 0.06 R. apiculata 96,11
Density of trees 30 3 90
Karimun 2 0.89 0.34 S. alba 84,93
Diversity Index 25 1 25
Menjangan Besar 0.19 0.06 R. stylosa 98,17
Index of Similarity 25 1 25
DS: Dominant species
Mangrove Species 20 3 60
RD: Relative dominancy
MHI 200
Mangrove Distribution Mapping
Results of mapping study indicate that 4. DISCUSSION
mangroves are found only in a few islands i.e.
Karimunjawa, Menjangan Besar and Sintok (See fig. The field survey identified 21 mangrove species
2, 3 & 4). The highest and the lowest percent area in the study site, including 11 species true mangroves
occupied by mangrove ecosystems were found at and mangrove associates for the rest, dominated by R.
island of Sintok (29,67 %) and Karimunjawa (12,73 apiculata and R. stylosa, family of Rhizophoraceae.
%). Total research area is 3752 Ha while mangrove The number of mangrove species was different
area is 475 Ha (12,66 %) (See table 3). from that found by Balai Taman Nasional
Table 3. Area occupied by mangrove Karimunjawa (BTNKJ), the agency responsible for
marine park management in Karimunjawa. In 2013,
Karimunjawa Menjangan Besar Sintok BTNKJ identified 22 mangrove species in
Area
Ha % Ha % Ha % Karimunjawa Island, dominated by R. apiculata and
Land 3501.62 87.27 77.46 71.04 22.75 70.33 C. tagal and 22 mangrove species in Kemujan
26,27
Mangrove 445.91 12.73 22.43 28.96 6.75 29.67 dominated by B. cylindrica and C. tagal .

Figure 2. Mangrove distribution in Menjangan Besar island

4 Adv.Sci.Lett.Vol.23,No.4,2017 doi:10.1166/asl.2017.9155 4
 RESEARCH ARTICLE

Figure 3. Mangrove distribution in Karimunjawa island

Figure 4. Mangrove distribution in Sintok island

This number of species encompass all growth
category i.e. tree, sapling and seedling. The field
survey found that mangrove from family
Rhizophoraceae was the most dominant in the KNP,
accordance with the result of BTNKJ (2013). The
most abundant species in tree, sapling and seedling
category was R. apiculata, R. mucronata and R.
stylosa respectively.
R. mucronata was found in 4 of 9 sampling
locations while R. apiculata and R. stylosa in 5 of 9
sampling locations. The highest average density was
R. apiculata. The highest average density in sapling
and seedling category was R. mucronata and R.
stylosa respectively. The sapling and seedling
abundance data reflect the degree of natural mangrove
regeneration28. Overall, mangrove density was higher

5 Adv.Sci.Lett.Vol.23,No.4,2017 doi:10.1166/asl.2017.9155 5

in the Karimunjawa Island than in the Menjangan
Besar.
R. apiculata and C. tagal, dominant species in
this study, is true mangrove species that dominated
in many location. The level of dominance may reach
90% of the vegetation that grows in a location29. R.
apiculata community distributed on deep, soft,
muddy soils that are flooded by normal high tides,
occur on stable sediments. C. tagal life in areas
inundated by spring tides with well-drained soils and
prefers clay substrates12.
Satellite image interpretation results showed
that mangrove were found at the island of
Karimunjawa, Menjangan Besar and Sintok.
However, mangrove was also found in in Parang
Island30. Karimunjawa island has the highest
mangrove area cover with 445,91 ha, however was
the lowest in percentage. Karimunjawa was also the
most densely island in the KNP, around 9000
resident population, concentrated on the islands of
Karimunjawa, Kemujan, Parang and Nyamuk.
Mangrove ecosystems are globally affected by
anthropogenic impacts, an increasing human
activities in islands, can increase threat to ecosystem.
Heavily populated coastal zones have spurred the
widespread clearing of mangrove for coastal
development, aquaculture, or resource use31. For
example, mangrove area in the Parang Island, one
island in the KNP that has high intensity human
activity, has declined from 46,80 ha in 1997 to 38,36
ha in 2011, decreased by 8,44 ha or 18,03 % 30. The
condition of these resources is strongly influenced by
how people use these resources.
This study investigated single value index
called Mangrove Health Index (MHI) to obtain
obvious understanding of mangrove ongoing trends
in KNP. The value of MHI at Karimunjawa was 200,
in medium category. The index analyses the value of
mangrove density, diversity index, index of
similarity and the number of mangrove species.
Weigh of each parameter was determined based on
expert judgments. Parameter weights are determined
by expert judgment based on the importance of a
parameter to the mangrove ecosystem health The
present results provide new method to obtain obvious
understanding of ongoing mangrove trends. The
obtained results can also be integrated with
mangrove distribution data and thus directly
contributing to MPA management. MHI allowing
managers to define management scenarios to obtain
more optimal value of MHI that portray mangrove
ecological dynamics. Continuous monitoring that
resulted of MHI will improves our ability to analyze
ineffective collection of multidisciplinary
information also avoid ineffectual transfer of
6 Adv.Sci.Lett.Vol.23,No.4,2017
RESEARCH ARTICLE
information from scientist to end-user in sustainable
management of mangrove ecosystem.
5. CONCLUSION
The value of Mangrove Health Index (MHI) at
the Karimunjawa National Park was 200, which is in
the medium category. The results suggest that there is
a need to improve MHI as part of sustainable
management based on distribution and diversity of
mangrove.
ACKNOWLEDGEMENTS
The authors would like to the thank Balai Taman
Nasional Karimunjawa for data support and M.
Helmi, Head of Ocean Remote Sensing Laboratory,
Diponegoro University for satellite imagery and
significant contribution to the maps analysis.
Ecological survey team, M. Iqbal H.P., Arifismail
E.R., Teo Andri. S., Siti. N.A. and Rendy P.P.
Mapping team Tegar R.K.P. and Rio R.
REFFERENCES
1. Bhatt S, Shah DG, Desai N. The mangrove
diversity of Purna Estuary, South Gujarat, India.
Trop Ecol. 2009;50(2):287-293.
2. Nichols WJ, Seminoff JA, Etnoyer P.
Biodiversity, Function, and Interconnectedness:
A Revolution in Our Understanding of Marine
Ecosystems and Ocean Conservation. In: Grafton
RQ, Hilborn R, Squires D, Tait M, Williams MJ,
eds. Handbook of Marine Fisheries Conservation
and Management. Vol New York: Oxford
University Press; 2010:43-59.
3. Nagelkerken I, van der Velde G, Gorissen MW,
Meijer GJ, van’t Hof T, den Hartog C.
Importance of mangroves, seagrass beds and the
shallow coral reef as a nursery for important coral
reef fishes, using a visual census technique.
Estuar Coast Shelf Sci. 2000;51(1):31-44.
doi:10.1006/ecss.2000.0617.
4. Primavera JH. Mangroves as Nurseries: Shrimp
Populations in Mangrove and Non-mangrove
Habitats. Estuar Coast Shelf Sci. 1998;46:457-
464. doi:10.1006/ecss.1997.0275.
5. Kneib RT, Lee SY, Kneib JP. Adult-juvenile
interactions in the crabs Sesarma (Perisesarma)
bidens and S. (Holometopus) dehaani
(Decapoda:Grapsidae) from intertidal mangrove
habitats in Hong Kong. J Exp Mar Bio Ecol.
1999;234(2):255-273. doi:10.1016/S0022-
0981(98)00149-X.
doi:10.1166/asl.2017.9155 6

6. Laegdsgaard P, Johnson C. Why do juvenile fish
utilise mangrove habitats? J Exp Mar Bio Ecol.
2001;257(2):229-253. doi:10.1016/S0022-
0981(00)00331-2.
7. Suryono CA. Ekologi Perairan Delta Wulan
Demak Jawa Tengah : Distribusi Kepiting (Infra
Ordo Brachyura dan Anomura) di Kawasan
Mangrove. Ilmu Kelaut. 2006;11(4):210-215.
8. Redjeki S. Komposisi dan Kelimpahan Ikan di
Ekosistem Mangrove. 2013;18(1):54-60.
9. Clough B. Continuing the Journey Amongst
Mangroves. Vol 1. 2013.
10. FAO. The World’s Mangroves 1980-2005. Vol
153. FAO; 2007. doi:978-92-5-105856-5.
11. van Oudenhoven APE, Siahainenia AJ, Sualia I,
et al. Effects of different management regimes
on mangrove ecosystem services in Java,
Indonesia. Ocean Coast Manag. 2015;116:353-
367. doi:10.1016/j.ocecoaman.2015.08.003.
12. Giesen W, Wulffraat S, Zieren M, Scholten L.
Mangrove Guidebook for Southeast Asia.
Dharmasarn Co., Ltd; 2007.
doi:10.1086/346169.
13. Roca G, Alcoverro T, Krause-Jensen D, et al.
Response of Seagrass Indicators to Shifts in
Environmental Stressors: A Global Review and
Management Synthesis. Ecol Indic.
2016;63:310-323.
doi:10.1016/j.ecolind.2015.12.007.
14. Short FT, Coles R, Fortes MD, et al. Monitoring
in the Western Pacific Region Shows Evidence
of Seagrass Decline In Line with Global Trends.
Mar Pollut Bull. 2014;83:408-416.
doi:10.1016/j.marpolbul.2014.03.036.
15. Ambariyanto. Kebijakan Pengelolaan
Organisme Laut Dilindungi: Kasus Kerang
Raksasa. Semarang: Undip Press; 2010.
16. Barber PH, Ablan-Lagman MCA, Ambariyanto,
et al. Advancing Biodiversity Research in
Developing Countries: The Need for Changing
Paradigms. Bull Mar Sci. 2014;90(1):187-210.
doi:10.5343/bms.2012.1108.
17. Campbell SJ, Kartawijaya T, Yulianto I, Prasetia
R, Clifton J. Co-Management Approaches and
Incentives Improve Management Effectiveness
in the Karimunjawa National Park, Indonesia.
Mar Policy. 2013;41:72-79.
doi:10.1016/j.marpol.2012.12.022.
18. Nababan MG, Munasik, Yulianto I, et al. Status
Ekosistem Di Taman Nasional Karimunjawa
2010. Wildlife Conservation Society-Indonesia
Program; 2010.
7 Adv.Sci.Lett.Vol.23,No.4,2017
View publication stats
RESEARCH ARTICLE
19. Menteri Negara Lingkungan Hidup. Kriteria
Baku dan Pedoman Penentuan Kerusakan
Mangrove. 2004.
20. Kitamura S, Anwar C, Chaniago A, Baba S.
Handbook of Mangroves in Indonesia; Bal &
Lombok. ISME; 1997.
21. Valle M, Palà V, Lafon V, et al. Mapping
estuarine habitats using airborne hyperspectral
imagery, with special focus on seagrass
meadows. Estuar Coast Shelf Sci. 2015;164:433-
442. doi:10.1016/j.ecss.2015.07.034.
22. McCarthy MJ, Merton EJ, Muller-Karger FE.
Improved coastal wetland mapping using very-
high 2-meter spatial resolution imagery. Int J
Appl Earth Obs Geoinf. 2015;40:11-18.
doi:10.1016/j.jag.2015.03.011.
23. Lillesand TM, Kiefer RW, Chipman JW. Remote
Sensing and Image Interpretation. Vol (Stanley
D, Pigliucci NM, Powell D, Flahive R, eds.).
John Wiley & Sons, Inc. All; 2004.
doi:10.1017/CBO9781107415324.004.
24. Mueller-Dombois D, Ellenberg H. Aims and
methods of vegetation ecology. John Wiley Sons.
1974;(September):93-135. doi:10.1016/0304-
3746(75)90017-7.
25. Odum EP. Dasar-Dasar Ekologi. Gadjah Mada
University Press; 1993.
26. BTNKJ. Laporan Inventarisasi Mangrove Di
SPTN II Karimunjawa.; 2013.
27. BTNKJ. Laporan Inventarisasi Mangrove Di
SPTN I Kemujan.; 2013.
28. Ashton EC, Macintosh DJ. Preliminary
assessment of the plant diversity and community
ecology of the Sematan mangrove forest,
Sarawak, Malaysia. For Ecol Manage.
2002;166:111-129. doi:10.1016/S0378-
1127(01)00673-9.
29. Noor YR, Khazali M, Suryadipura INN. Panduan
Pengenalan Mangrove Di Indonesia.; 2006.
30. Hartoko A, Hendrarto IB, Widiyanti AMD.
Perubahan Luas Vegetasi Mangrove di Pulau
Parang, Kepulauan Karimunjawa Menggunakan
Citra Satelit. J Manag Aquat Resour.
2013;2(2):19-27.
31. Polidoro BA, Carpenter KE, Collins L, et al. The
loss of species: Mangrove extinction risk and
geographic areas of global concern. PLoS One.
2010;5(4):1-10.
doi:10.1371/journal.pone.0010095.
doi:10.1166/asl.2017.9155 7