Murdiyarso 

et al. Carbon Balance and Management

Carbon Balance and Management (2023) 18:12
https://doi.org/10.1186/s13021-023-00233-1

REVIEW Open Access

Deriving emission factors for mangrove blue

carbon ecosystem in Indonesia
Daniel Murdiyarso1,2*, Haruni Krisnawati3, Wahyu C. Adinugroho3 and Sigit D. Sasmito4 

Abstract 
Background  Using ‘higher-tier’ emission factors in National Greenhouse Gas Inventories is essential to improve
quality and accuracy when reporting carbon emissions and removals. Here we systematically reviewed 736 data
across 249 sites (published 2003–2020) to derive emission factors associated with land-use change in Indonesian
mangroves blue carbon ecosystems.
Results  Four management regimes—aquaculture, degraded mangrove, regenerated mangrove and undisturbed
mangrove—gave mean total ecosystem carbon stocks of 579, 717, 890, and 1061 Mg C h ­ a−1 respectively. The largest
biomass carbon stocks were found in undisturbed mangrove; followed by regenerated mangrove, degraded man-
grove, and aquaculture. Top 100-cm soil carbon stocks were similar across regimes, ranging between 216 and 296 Mg
C ­ha−1. Carbon stocks between 0 and 300 cm varied significantly; the highest values were found in undisturbed
mangrove (916 Mg C ­ha−1), followed by regenerated mangrove (803 Mg C ­ha−1), degraded mangrove 666 Mg C ­ha−1),
and aquaculture (562 Mg C ­ha−1).
Conclusions  Using deep layer (e.g., 300 cm) soil carbon stocks would compensate for the underestimation of sur-
face soil carbon removed from areas where aquaculture is widely practised. From a project perspective, deep layer
data could secure permanence or buffer potential leakages. From a national GHG accounting perspective, it also pro-
vides a safeguard in the MRV system.
Keywords  Aquaculture, Carbon stocks, Forest reference emission level (FREL), GHG fluxes, National Greenhouse Gas
Inventories (NGGI) , Mangrove restoration, Nature based climate solutions

Background gases (GHGs). The Intergovernmental Panel on Climate

Emission factors (EFs) are representative values or coef- Change (IPCC) emission factor database contains default
ficients used when calculating anthropogenic emis- data, known as Tier 1, and data from peer-reviewed jour-
sions by sources, and removals by sinks of greenhouse nals and other publications with higher tiers (i.e., Tier
2 and 3). Country-specific data are usually considered
Tier 2, and those values obtained using the most detailed
*Correspondence: methods, like modelling, are considered Tier 3. The IPCC
Daniel Murdiyarso
emission factor database is managed by the IPCC’s Task
[email protected]
1
Center for International Forestry Research – World Agroforestry, Jl. Force on National Greenhouse Gas Inventories, and
CIFOR, Situgede, Bogor 16115, Indonesia supported by the National Greenhouse Gas Inventories
2
Department of Geophysics and Meteorology, IPB University,
Programme (https://​www.​ipcc-​nggip.​iges.​or.​jp/​EFDB/​
Bogor 16680, Indonesia
3
Research Center for Ecology and Ethnobiology, National Research main.​php). The emission factor database becomes the
and Innovation Agency, Bogor, Indonesia main reference for countries where Tier 2 and 3 EFs are
4
NUS Environmental Research Institute, National University of Singapore,
unavailable.
21 Lower Kent Ridge Road, Singapore 119077, Singapore

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Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 2 of 12

With National Greenhouse Gas Inventories (NGGI), a high turnover of fine root production [9]. As a result,
best practice must abide by certain principles (e.g., trans- together with the two other blue carbon ecosystems—
parency, accuracy, completeness, comparability, and seagrasses and saltmarshes [10]—mangrove is one of the
consistency), specifically in the use of higher-tier activ- ecosystems with the highest carbon burial rates; as much
ity data and EFs for land-based emissions monitoring. To as 20 times more than terrestrial forests [11], contribut-
reduce uncertainties in GHG emission reduction targets, ing to the high proportions of carbon stocks in their soil
countries or project developers may prefer to use higher- carbon pools [6, 12].
tier EFs, as they tend to offer higher levels of accuracy. The source of mangrove soil carbon, especially in the
Therefore, deriving country-specific or even site-specific first meter or top soil, is primarily driven by the tidal
higher-tier EFs can further improve the quality of the transport of allocthonous sediment; while in-situ or
NGGI, and thus the credibility of national measuring, autochtonous sequestration is predominantly recalcitrant
reporting and verification (MRV) processes [1]. carbon [13]. The use of the top 1  m estimate, however,
Since the 2013 Supplement to the 2006 IPCC Guide- may cause a 40% underestimation of TECS [14]. The fact
lines for NGGI for Wetlands was published [2], just that soil carbon dominates TECS by up to 80–90% [6, 15]
a few countries have adopted the guidelines for their suggests that the soil excavation that is generally prac-
national reporting. The Supplement, which was designed ticed in the development of aquaculture should be regu-
to address high-carbon reservoirs in wetlands, includes lated. That said, restoration efforts, such as increasing
peatlands and mangroves. It follows the Agriculture, tree density and basal area, could improve the survival of
Forestry and Other Land Use (AFOLU) sector key cat- stands [16], which in turn promotes effective carbon bur-
egories analysis, under the 2006 IPCC Guidelines and ial [17]. If a large soil carbon pool is sustainably managed,
its predecessor the 1996 IPCC Guidelines. The total eco- permanence is largely secured. Efforts to reduce emis-
system carbon stocks (TECS) is the sum of the following sions from mangrove deforestation and degradation must
carbon pools: aboveground biomass carbon (AGBC), prioritize protecting soil carbon stocks as they contribute
belowground biomass carbon (BGBC), dead organic mat- up to 80% of the mangrove blue carbon ecosystem [18].
ter (DOM), and soil organic carbon (SOC). To estimate Here we present a synthesis of carbon stock and flux
anthropogenic emissions by sources and removals by datasets from 249 mangrove ecosystems in Indonesia,
sinks, the 2006 IPCC guidelines provides two approach and further derive EFs associated with multiple land man-
options; the stock-difference approach and the gain– agement regimes (e.g., aquaculture, degraded mangrove,
loss approach [3]. Both produce comparable estimates. regenerated mangrove, and undisturbed mangrove). We
Although countries such as Australia are interested in used a systematic review approach to address the pri-
including blue carbon in their national emissions reduc- mary question—to what extent does land-use change
tion policy, the use of the guidelines around this is still affect carbon stocks and GHG flux dynamics in Indone-
unclear [4]. Indonesia, meanwhile, has been incorporat- sian mangrove ecosystems? Our synthesis and dataset on
ing mangrove into its improved Forest Reference Emis- mangrove EFs will be useful to support future improve-
sion Level (FREL), which was initially submitted to the ments in Forest Reference Emission Level (FREL), as well
Secretariat of the United Nations Framework Convention as to support emerging mangrove restoration projects
on Climate Change (UNFCCC) in 2016. related to voluntary carbon offset mechanisms.
Indonesia is home to around 3 million hectares of
mangroves—almost a quarter of world’s mangrove area Methods
is found in this archipelagic country with its 900,000 km Literature search
coastline [5]. While Indonesian mangrove is facing tre- The scope and steps of this study followed the proto-
mendous pressure from the development of aquacul- col used in a previously-published systematic review
ture and agriculture [6], this carbon-rich coastal forest is assessing carbon stocks and GHG fluxes associated with
also one of the key ecosystems for nature-based climate land-use and land-cover change in mangrove ecosys-
solutions [7]. Mangroves in Indonesia, which are domi- tems globally [19]. In line with our focus on Indonesia,
nated by Rhizophora spp and are predominantly located we modified the keyword search strings for this review’s
in estuarine and deltaic coastal settings, store consider- literature search (see Table  1). Literature searches were
ably high TECS, with means of 1083 ± 378 Mg C h ­ a−1 [6]. conducted in two main databases (Scopus and Web of
Unlike most terrestrial forests, mangroves are halophyte Science), with additional searches conducted through
coastal vegetation, tolerating high salinity and other Google Scholar. We used both Google Scholar English
harsh conditions in the root environment, making these and Bahasa Indonesia, collecting the first 50 literature
coastal forests strong contenders in a world with rising results, in ‘most relevant’ order. Literature searches were
sea levels [8]. This is probably the reason mangroves have conducted several times, with the final search undertaken
 Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 3 of 12

Table 1  Keywords used as search strings in the literature database search

Category Search terms

Populations mangrove* OR Rhizophora OR coast* AND Indonesia

Interventions undisturb* OR clear* OR pristine OR intact OR plantation OR log* OR harvest* OR abandoned
OR anthrop* OR impact* OR aquaculture* OR aquaculture* OR “land use*” OR “oil palm” OR “shrimp
farm*” OR “shrimp pond*” OR “rice cultivation” OR “rice farm*” OR “rice production” OR “rice field*”
OR “rice area*” OR “fish farm*” OR “fish pond*” OR mining OR degrad* OR disturb* OR “land cover*”
OR “urban development” OR deforest* OR conversion OR rehabilit* OR restor* OR pollut* OR ero-
sion
Comparator ecosystem OR sediment* OR biomass OR soil* OR NPP OR productivity OR “root product*”
OR dynamic* OR litter* OR “dead wood” OR emission* OR stock* OR storage* OR respiration
OR efflux OR sequest* OR soil OR forest* OR POC OR DOC OR DIC OR burial
Outcomes carbon OR methane OR “greenhouse gas*” OR GHG OR flux* OR emission* OR CO2 OR CH4 OR N2O

on 24 May 2021. To maintain the quality of literature stocks (aboveground and belowground biomass, woody
data, we included only peer-reviewed publications in our debris, and soil carbon pools) as well as carbon fluxes
systematic review. (biomass productivity, GHG fluxes, aquatic carbon
fluxes, and soil carbon burial) from either and/or both
Literature screening undisturbed and disturbed mangrove ecosystems. At
We conducted three stages of literature screening, which each stage of the literature screening, we developed semi-
included title, abstract and full-text screening. The num- structured questions to assess the relevancy of each lit-
bers of included and excluded literature are described in erature, in terms of the scope of the systematic review.
the Preferred Reporting Items for Systematic Review and
Meta-Analysis (PRISMA) diagram (Table  2). Included Critical appraisal and data extraction
studies needed to meet the predefined scope and inclu- We used three main criteria to assess the quality of the
sion criteria of the previous systematic review on the datasets presented in included literature. Literature
effect of land-use change on mangrove carbon stocks included for data extraction had to meet the follow-
[18]. Specifically, we included only field-based data col- ing criteria: (a) location and land-use types of the study
lection studies from Indonesia that reported carbon site(s) are described; (b) carbon stocks and/or GHG

Table 2  The PRISMA systematic review workflow for literature screening, inclusion, and exclusion
Process Inclusion Exclusion

Literature identification n = 163 (Scopus, cut-off date 27 Feb 2020)

n = 137 (WoS, cut-off date 27 Feb 2020)
n = 45 (Scopus: cut-off date 24 May 2021)
n = 44 (WoS: cut-off date 24 May 2021)
n = 2 (author contact)
n = 691 (all search)
↓
n = 321 (remaining literatures) ⟶ n = 370 (duplicates)
↓
Literature screening n = 98 (title screening) ⟶ n = 223 (irrelevant literatures)
↓
n = 66 (abstract screening) ⟶ n = 32 (irrelevant literatures)
↓
n = 47 (full text screening) ⟶ n = 19 (irrelevant literatures)
↓
Eligibility evaluation n = 45 (critically appraised) ⟶ n = 2 (irrelevant literatures)
↓
Included literature n = 29 studies were eligible for data extraction and analysis ⟶ n = 16 (irrelevant literatures)
Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 4 of 12

fluxes data, obtained from primary field-based collection,

are available; (c) rigorous statistical assessment, such as
sufficient replication. Literature was excluded from data
extraction if not all three criteria were met.
Data extraction focused on the following items: AGBC,
BGBC, DOM, SOC, soil ­ CO2 efflux, soil ­
CH4 efflux,
soil ­N2O efflux, and soil carbon burial. We extracted
all standard data presentations, such as mean, standard
deviation, standard error and sample sizes for each study.
If data were presented in figure format and direct read-
ing was not possible, we retrieved the numbers by using
WebPlotDigitizer Version 4.0 [20]. All data were com-
piled into a single database (see Supplementary Data for
details, including variables and compilation of extracted
data for this review study).

Data analysis
We summarized datasets by using the descriptive statisti-
cal approach for carbon stock pools and flux pathways, Fig. 1  Geographical distribution of 249 studies’ locations
across four different land-use types (e.g., aquaculture, in Indonesia (not to scale; the coordinates of the sites are indicated
degraded mangrove, regenerated mangrove and undis- in the individual publication). The top panel shows study locations
turbed mangrove). The meta-analysis was applied to categorized by land management types, i.e., aquaculture (21 studies),
degraded mangrove (18 studies), regenerated mangrove (57 studies),
calculate the effect-size, mean, standard error, and con- and undisturbed mangrove (153 studies). The bottom panel presents
fidence interval of data obtained from multiple studies, study locations categorized by the type of compiled dataset, i.e.,
before these were summarized according to carbon pool, carbon stocks (184 studies), GHG fluxes (37 studies), and carbon
flux pathways, and land management regime, by using stocks and GHG fluxes (28 studies)
metafor R package in R statistics [21].
The percentage of change in biomass and DOM car-
bon pools, comparing between undisturbed mangrove in number over the last decade, suggesting a growing
and disturbed mangrove classes (i.e., aquaculture and interest in the topic by the scientific community, particu-
degraded mangrove), was calculated using the car- larly after 2012 (Additional file  1: Fig. S1). Most of the
bon stock difference approach, while the percentage of collected data focused on undisturbed mangrove (61%),
change in soil carbon was quantified using a meta-anal- followed by regenerated mangrove (23%), aquaculture
ysis approach (e.g., by comparing with ratio effect size). (8%), and degraded mangrove (7%) study sites.
The meta-analysis was run using OpenMee open-access It is interesting to note that field sampling was under-
software for ecology and evolutionary biology meta- taken across the archipelago (Fig.  1), representing the
analysis [22]. Data that reported carbon stocks and GHG four main management regimes (e.g.,  aquaculture,
fluxes across regenerated mangroves were not included degraded mangrove, regenerated mangrove, and undis-
in the stock change and meta-analysis; these were instead turbed mangrove). While carbon stock studies are more
analyzed and presented separately to examine the rate of widespread, interest in flux studies is growing, allowing
carbon storage recovery according to revegetation stage us to make more analyses and improve gaps in knowl-
(e.g., restoration, rehabilitation). edge and information availability. Widely available car-
bon stocks data suggests that using a stock difference
Results approach may be more readily available way to derive
Data availability and distribution EFs compared to gain-loss approach [3].
With the geographical distribution of our systematic
review only focusing on Indonesia (Fig. 1), we compiled
736 relevant data collected across 249 study sites from 29 Carbon stocks and GHG fluxes
peer-reviewed publications, to derive EFs in mangrove Tier 2 TECS in Indonesian mangrove ecosystems ranged
ecosystems (Table 3). We observed that 85% of the data between 579 and 1061  Mg C h ­ a−1 depending on their
related to carbon stocks, while just 15% related to GHG associated land uses (Fig. 2 and Table 4). TECS increased
and soil carbon fluxes. The records also indicate that in line with rehabilitation status, with the smallest
publications on this subject have increased significantly TECS observed in aquaculture, followed by degraded
Table 3  List of included publications, along with their number of studies across different carbon stock pools and GHG fluxes
No. Publicationa Carbon pool Soil ­CO2 Soil ­CH4 Soil ­N2O Soil C burial
efflux efflux efflux
AGBC BGBC DOM SOC

1 Alongi et al. 12 4
[33]
2 Alongi et al. 4 4 4 4 4
[34]
3 Ardhani et al. 3 3 3 5
[35]
4 Arif et al. [36] 5 5 5
5 Arifanti et al. 18 18 18
[27]
6 Asadi 7 7
and Pambudi
Murdiyarso et al. Carbon Balance and Management

[37]
7 Asadi et al. 2
[38]
8 Asadi et al. 1 1
[39]
(2023) 18:12

9 Cameron et al. 13 13 13
[28]
10 Cameron et al. 13 13
[40]
11 Chen et al. 9 9 9
[41]
12 Dharmawan 3 3 3
[42]
13 Hanggara 11 11 10 9 6
et al. [17]
14 Hapsari et al. 1
[43]
15 Hidayah 1
and Andriyani
[44]
16 Jennerjahn 2 2
[45]
17 Kangkuso 2
et al. [46 ]
18 Kusumaning- 4 4 3
tyas et al. [47]
19 Malik et al. [48] 3 3
Page 5 of 12
Table 3  (continued)
No. Publicationa Carbon pool Soil ­CO2 Soil ­CH4 Soil ­N2O Soil C burial
efflux efflux efflux
AGBC BGBC DOM SOC

20 Murdiyarso 39 39 39 39
et al. [6]
21 Murdiyarso 6 6 3 23 4
et al. [18]
22 Nehren 3 3 3
Murdiyarso et al. Carbon Balance and Management

and Wicak-
sono [49]
23 Rudiastuti 1
et al. [50]
24 Sasmito et al. 49 49 39 49
[15]
(2023) 18:12

25 Sasmito et al. 2 2
[51]
26 Sidik 2
and Lovelock
[52]
27 Sidik et al. [53] 2 2 2 2
28 Slamet et al. 2 2 2
[54]
29 Weiss et al. 12
[55]
Total studies 177 169 94 192 45 30 9 20
AGBC, aboveground biomass carbon; BGBC, belowground biomass carbon; DOM, dead organic matter; SOC, soil organic carbon
a
The full citations are listed in the Supplementary Information
Page 6 of 12
 Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 7 of 12

Table 4 Carbon stocks in various pools across Indonesian

mangrove ecosystems under different management regimes
Carbon Unit Mean n Standard 95% CI
stocks error

Aquaculture
AGBC Mg C ­ha−1 11.01 10 3.86 2.29–19.73
BGBC Mg C ­ha−1 2.64 7 1.30  − 0.54 to 5.81
DOM Mg C ­ha−1 3.39 2 2.72  − 31.15
to 37.93
SOC Mg C ­ha−1 259.08 6 90.53 26.37–491.8
0–100 cm
SOC Mg C ­ha−1 562.36 10 50.20 448.81–675.91
0–300 cm
Degraded mangrove
AGBC Mg C ­ha−1 20.98 8 6.05 6.68–35.28
Fig. 2  Carbon stocks in various pools across different management BGBC Mg C ­ha−1 6.01 6 1.43 2.34–9.67
regimes (Aqua, aquaculture; DegM, Degraded mangrove; RegM, DOM Mg C ­ha−1 24.34 7 6.67 8.03–40.65
regenerated mangrove; and UndM, Undisturbed mangrove; AGBC, SOC Mg C ­ha−1 215.66 13 38.07 132.7–298.62
aboveground biomass carbon; BGBC, belowground biomass carbon; 0–100 cm
DOM, dead organic matter; SOC, soil organic carbon) SOC Mg C ­ha−1 665.59 6 132.49 325.02–1006.15
0–300 cm
Regenerated mangrove
AGBC Mg C ­ha−1 58.06 31 8.17 41.38–74.75
mangrove, regenerated mangrove and undisturbed man-
BGBC Mg C ­ha−1 15.80 26 3.77 8.04–23.55
grove respectively. By contrast, soil carbon stocks in the
DOM Mg C ­ha−1 13.49 18 2.52 8.18–18.81
first 100 cm of depth remained similar across all manage-
SOC Mg C ­ha−1 296.41 27 20.11 255.07–337.75
ment regimes, ranging between 216 ± 38 and 296 ± 20 Mg 0–100 cm
C ­ha−1. Overall, the soil carbon pool contributed the SOC Mg C ­ha−1 803.03 15 48.76 698.45–907.61
highest proportion of TECS, with 86% found in undis- 0–300 cm
turbed mangroves, 93% and 90% in both degraded and Undisturbed mangrove
regenerated mangroves, and 97% in aquaculture. AGBC Mg C ­ha−1 101.67 114 4.79 92.18–111.16
Table  5 shows that the greatest soil ­CO2 efflux was BGBC Mg C ­ha−1 28.70 98 1.65 25.42–31.98
observed in aquaculture—as much as 23.8  ± 
7.6  Mg DOM Mg C ­ha−1 14.47 63 1.22 12.03–16.9
­CO2 ­ha−1  ­yr−1—followed by regenerated and undis- SOC Mg C ­ha−1 258.44 34 32.40 192.53–324.36
turbed mangroves with 13.5 ± 4.5 and 7.9 ± 1.4  Mg ­CO2 0–100 cm
­ha−1  ­yr−1, respectively. Degraded mangrove gener- SOC Mg C ­ha−1 916.42 75 47.60 821.57–1011.28
0–300 cm
ated the largest soil C ­ H4 effluxes (4.2 ± 1.5  Mg C
­ O2-eq
­ha−1  ­yr−1), followed by aquaculture (2.0 ± 0.7 Mg C ­ O2-eq The plots of mean, standard error, and confidence interval for all carbon pools
calculated using a random-effects model are shown in Additional file 1: Figs.
­ha−1  ­yr−1) and undisturbed mangrove sites (1.0 ± 0.7 Mg S2–S22
­CO2-eq ­ha−1  ­yr−1). By contrast, the largest mean for AGBC, aboveground biomass carbon; BGBC, belowground biomass carbon;
soil carbon burial occurred in undisturbed mangrove DOM, dead organic matter; SOC, soil organic carbon; n, number of study
(3.2 ± 2.2 Mg C ­ha−1  ­yr−1) followed by regenerated man-
grove (1.7 ± 0.3 Mg C h ­ a−1  ­yr−1) and degraded mangrove
(1.2 ± 0.4 Mg C ­ha  ­yr−1).
−1 were approximately 64% and 52%, due to aquaculture
and degradation respectively. Biomass carbon stocks
experienced the greatest loss following land-use change,
Change of carbon stocks and GHG fluxes between 84 and 95%, while soil carbon pool loss was 74%.
following land‑use change By contrast, DOM carbon stocks were 36% greater when
We found that land-use change overall generated sub- the area was impacted by land-use change, compared to
stantial TECS loss, relative to the undisturbed mangrove undisturbed mangroves. This indicates that woody debris
baseline (Fig. 3). By using paired datasets of undisturbed may have substantially accumulated due to disturbance
mangrove and land-use change impacted sites, however, regimes.
we further observed that the degree of carbon stock loss In the context of carbon gains and losses and GHG
within each carbon pool varied depending on the land- fluxes, Table  3 shows that soil C­ O2 fluxes in land-use
use type or management regime (Fig.  3). TECS losses
Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 8 of 12

Table 5  Greenhouse gas fluxes and soil carbon burial across Indonesian mangrove ecosystems under different management regimes
Carbon fluxes Unit Mean n Standard error 95% CI

Aquaculture
Soil ­CO2 effluxes Mg ­CO2 ­ha−1 ­yr−1 23.81 30 1.40  − 0.40 to 48.02
Soil ­CH4 effluxes Mg ­CO2-eq ­ha−1 ­yr−1 2.02 20 0.68  − 1.11 to 5.16
Soil ­N2O effluxes kg ­CO2-eq ­ha−1 ­yr−1 NA 9 0.16 NA
Soil carbon burial ­ a−1 ­yr−1
Mg C h NA 7 2.24 NA
Degraded mangrove
Soil ­CO2 effluxes Mg ­CO2 ­ha−1 ­yr−1 NA 4 7.61 –
Soil ­CH4 effluxes Mg ­CO2-eq ­ha−1 ­yr−1 4.18 3 0.73  − 0.63 to 8.99
Soil ­N2O effluxes kg ­CO2-eq ­ha−1 ­yr−1 NA NA NA –
Soil carbon burial ­ a−1 ­yr−1
Mg C h 1.22 NA NA 0.39–2.05
Regenerated mangrove
Soil ­CO2 effluxes Mg ­CO2 ­ha−1 ­yr−1 13.49 NA NA 2.39–24.6
Soil ­CH4 effluxes Mg ­CO2-eq ­ha−1 ­yr−1 NA 4 1.51 –
Soil ­N2O effluxes kg ­CO2-eq ­ha−1 ­yr−1 NA NA NA –
Soil carbon burial ­ a−1 ­yr−1
Mg C h 1.67 8 0.35 0.87–2.46
Undisturbed mangrove
Soil ­CO2 effluxes Mg ­CO2 ­ha−1 ­yr−1 7.87 7 4.54 5.00–10.74
Soil ­CH4 effluxes Mg ­CO2-eq ­ha−1 ­yr−1 0.98 NA NA  − 0.44 to 2.4
Soil ­N2O effluxes kg ­CO2-eq ­ha−1 ­yr−1  − 0.12 NA NA  − 0.48 to 0.25
Soil carbon burial Mg C ­ha−1 ­yr−1 3.20 5 0.29  − 2.28 to 8.69
The plots of mean, standard error, and confidence interval for all GHG fluxes calculated using a random-effects model are shown in Additional file 1: Figs. S23–S31

Fig. 4  Aboveground and belowground biomass carbon stock

recovery according to mangrove regeneration age. UndM denotes
Fig. 3  Carbon stock loss and gain (in per cent) following two undisturbed mangroves
major land-use changes (aquaculture and mangrove degradation)
across the main four carbon pools. AGBC, aboveground biomass
carbon; BGBC, belowground biomass carbon; DOM, dead organic
matter; SOC, soil organic carbon

326%). The carbon burial dataset also suggests a substan-

tial difference between undisturbed and degraded man-
impacted mangroves were between 71 and 202% greater
groves. When mangroves were degraded, approximately
than those seen in undisturbed mangroves. A similar
48–62% of carbon burial rates were reduced.
increase was seen in soil C
­ H4 effluxes in mangrove eco-
Mangrove regeneration or rehabilitation may not be
systems following land-use change (between 106 and
able to fully recover the loss of TECS, which may have
taken place in a relatively short period. Soil carbon
stocks in land-use change impacted mangroves were
 Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 9 of 12

12–39% lower than in undisturbed mangroves. Accord- Stock‑difference and gain–loss approaches

ing to the biomass dataset, however, recovery did occur The majority of currently available publications reported
in aboveground and belowground biomass carbon data on carbon stocks, rather than GHG fluxes, in Indo-
stocks (Fig.  4). In fact, biomass carbon can be consid- nesian mangrove ecosystems. This provides a greater
ered to be fully recovered after 25  years of regenera- opportunity to apply a stock-difference rather than a
tion, when compared with undisturbed mangrove. gain–loss approach for the Indonesian National Green-
house Gas Inventory. This stock-difference approach has
Discussion been proven to produce considerably smaller estimates
Tier 2 emissions factors for land‑use change in mangroves of uncertainty in estimating forest carbon emissions for
Our study provides a synthesis of carbon stocks and aboveground biomass pools [26].
fluxes from 249 mangrove ecosystems in Indonesia and A comparison of sites suggests that carbon stock losses
therefore, these datasets are suitable and useful to sup- due to aquaculture conversion lead to different emis-
port the development of Tier 2 EFs. On comparing the sions factors. For example, aquaculture reduced car-
baseline EFs between the Tier 1 default in the 2013 IPCC bon stocks at the largest scale (75%) when compared to
Wetlands Supplement [2] and our findings, we found that forest logging (27%) and regenerated forest (17%) [15].
the default value for the AGBC pools for tropical wet Aquaculture conversion in Mahakam and Tanakeke, in
mangrove (86  Mg  ­ha−1) is lower than that found in this the island of Kalimantan and Sulawesi, generated lower
study (102  Mg  ­ha−1). Meanwhile, the value for top 1  m carbon stocks loss at just 48% and 36% respectively [27,
soil carbon in this study (296 Mg ­ha−1) was found to be 28]. These findings imply that emissions factors, fol-
lower than the IPCC default value of 471 Mg ­ha−1. lowing mangrove conversion into other land-uses, are
It is worth noting, however, that the population of the unique depending on geographical location and thus on
datasets differs substantially. The default value for the site-specific hydrogeomorphic characteristics, as well as
AGBC was calculated using 49 studies, while this meta- the type and duration of new land use that has replaced
analysis used 114 studies only for Indonesia. For soil car- mangroves. It is also possible that local practices and
bon, sample size for the default value was 43 (presumably culture determine how fish and shrimp ponds are estab-
from all climatic zones and multiple countries), while lished (e.g., different soil excavation depth) and managed,
for the Indonesian value it was 27. This suggests that the hence, the resulting GHG emissions.
proposed Tier 2 AGBC is highly reliable and indicates
the potential to maintain long-term conservation man- Future refinement
agement efforts rather than extensive rehabilitation and While Tier 1 default EFs mostly provide the absolute
restoration efforts, given the evidence that mangrove mean values for carbon stocks and fluxes, their accuracy,
plantations are inadequate to recover long-term carbon and whether these EFs are consistent enough to be used
capture and storage, and the result of regeneration may for multiple key categories, land representations and geo-
not resemble the structure and species diversity of undis- graphical locations, remains unclear. Aquacultural land
turbed mangrove [23–25]. carbon stocks, for example, can differ between countries
The Tier 2 soil carbon data proposed here were all depending on the initial carbon stocks prior to conver-
collected from the same climatic zone (tropical-wet), sion  as well as soil excavation depth. Following carbon
and were impacted by very dynamic land-use changes, stock and flux change analysis previously conducted
including highly destructive soil excavation during on a global level [29], in this study we also calculated
aquaculture development. The deeper layer (i.e., up to the relative change of carbon stocks for each pool  (pro-
300 cm) soil carbon dataset reached an optimum baseline vided as percentage of change), in response to land-use
of 916 Mg ­ha−1. This suggests the potential permanence change  specifically for Indonesia (i.e., degraded man-
that blue carbon mangrove projects have; as well as the grove and aquaculture, Fig.  3). These relative changes
safeguarding they offer to national carbon accounting are particularly useful to understand carbon loss impacts
under the existing MRV system, when it comes to further between types of land use change, if countries or projects
leakage or emission displacement in wetland ecosystems. have calculated carbon stocks based upon undisturbed
With the large soil carbon dataset that exists from 300 cm mangrove alone. Relative carbon stock changes can also
deep cores (n = 75), it has been proposed that a deeper be used to support more advanced analysis, such as the
layer baseline (rather than the standard 1-m depth) could modelling of emissions and removals projections [30].
be used in areas where aquaculture is rampant [6]. Further refinement of the soil carbon data is required,
so as to improve consistency when calculating carbon
emissions by using stocks different approach. In the
studies and data analyzed here, soil carbon stocks were
Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 10 of 12

obtained from diverse soil depths; for example, soil car- Conclusions
bon in Mahakam was obtained from a depth of 300 cm, The derived Tier 2 EFs for mangrove blue carbon ecosys-
while in other areas, sampling was undertaken from tems in Indonesia were derived from a systematic review
depths of up to 100  cm only (see Supplementary Data). of 29 peer-reviewed publications are geographically
The depth of soil organic matter is the main factor con- well distributed across the archipelago. Following IPCC
trolling variation in soil carbon stocks between sites and Guidelines, the EFs were separated into carbon pools, i.e.,
particularly hydrogeomorphic settings [15]. As seen in aboveground, belowground, dead organic matter and soil.
mangrove carbon stock assessments elsewhere, the soil They are readily useable for Indonesia’s National Green-
carbon pool contributes the most (> 50%) toward TECS. house Gas Inventory and the reporting of climate change
As deeper soil coring also implies cost effectiveness, the mitigation measures. The ecosystems are categorized by
modelling of deeper layer carbon stocks value should management regime: aquaculture, degraded mangroves,
be pursued, since this will introduce fewer uncertain- regenerated mangroves, and undisturbed mangroves.
ties, compared with estimating soil carbon based upon Using deeper layer (e.g., 300  cm) soil carbon storage
AGBC, as is widely-practiced currently [31]. The inclu- values would compensate for the underestimation in car-
sion of the DOM carbon pool in carbon emissions and bon losses from coastal ecosystems where aquaculture is
removals reporting may also improve accuracy. Despite widely practised. From a project perspective, this deeper
this carbon pool only contributing up to 1.4% of TECS layer data could secure permanence or buffer potential
in undisturbed mangrove (Fig.  2), it is often neglected leakages; while from a national GHG accounting per-
and reported rarely by most studies [14]. Changes in spective, it also provides a safeguard in the MRV system.
the DOM carbon pool are reported to be significant,
particularly when mangroves experience direct bio- Supplementary Information
mass removals, through logging, for example [15, 17]. The online version contains supplementary material available at https://​doi.​
The inclusion of DOM will certainly improve accuracy org/​10.​1186/​s13021-​023-​00233-1.
in emissions and removals reporting, particularly where
Additional file 1. Trends of publications on mangrove blue carbon in
forest management is applied for wood resource extrac- Indonesia and random effects model results by carbon pools and land
tion. The highest DOM found in degraded mangrove of management types.
24.34 ± 6.67  Mg  ­ha−1 is comparable with those found in
Kenya of 29.92 ± 36.72 Mg ­ha−1 [32]. Acknowledgements
This work was funded by the Norwegian Ministry of Foreign Affairs through
the Norwegian International Climate and Forest Initiative (NICFI) to the Center
Implications for Indonesia’s national greenhouse gas for International Forestry Research (CIFOR), Agreement No. INS 2078–19/0010.
inventory DM thanks partial support from the United States Agency for International
The results of this study reflect TECS for Indonesia’s blue Development (USAID). The authors thank the Indonesian FREL team for pro-
viding constructive comments and inputs on the manuscript.
carbon mangrove ecosystems, categorized into four site
conditions—undisturbed mangroves, regenerated man- Author contributions
groves, degraded mangroves and aquaculture. These DM: conceived the conceptual framework, interpreted the data, wrote the
initial draft and final manuscript, and secured the funding; HK: contributed
allow us to understand the factors driving carbon stock to the discussion and reviewed final manuscript; WCA: contributed to the
changes. As recommended by IPCC best practice, coun- discussion and reviewed final manuscript; SDS: wrote the initial draft and
try-specific EFs should be developed for each ecosystem, final manuscript, conducted the literature survey, interpreted the data, and
prepared the diagrams.
in its various conditions. Our results offer the opportu-
nity to improve the accuracy and reduce the uncertainty Funding
of country-scale accounting for emissions associated Not applicable.
with land-use change in mangrove ecosystems. Data availability
The EFs derived in this study are essential, not only for The dataset presented in this paper is available at the following link: https://​
the estimation of GHG emissions, but also for evaluating doi.​org/​10.​6084/​m9.​figsh​are.​23660​085.
the progress made by mitigation programs in reducing
emissions. Application of these EFs in Indonesia’s GHG Declarations
emission accounting  under both jurisdictional and pro- Ethics approval and consent to participate
ject carbon financing schemes should be straightforward. Not applicable.
The results can also be adopted by the IPCC emission
Consent for publication
factor database, allowing countries to use EFs that are All authors have approved the manuscript and agree with its submission to
suitable for their specific mangrove situation, thus help- Carbon balance Management.
ing to improve the quality of GHG inventories in a cost-
Competing interests
effective way. The authors have no competing interests to declare.
 Murdiyarso et al. Carbon Balance and Management (2023) 18:12 Page 11 of 12

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