Science Introduce Your System Paper

Pleasesubmit your detailed outline (2-3 pages + full-text PDF of each of the 10 articles in the references) here follow these instructions:

The outline must have all major sections of the paper and sub topics for each section.

Each statement needs to have a citation. You must include and cite at least 10 peer-reviewed articles, 7 of which must be primary literature. References must be properly formatted: how to format your references Recommended: use reference manager software to handle your citations. There are free services such as MendeleyLinks to an external site..

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Secondary: Main and Better restoration policies..

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Steps in the Preparation of an Annotated Bibliograph

This outline is an overview of the paper that outlines the scope of the paper, describing the topicsto be covered and the order. This outline will contain all the detail you need to write a completepaper. If you prepare your outline correctly, it should be almost as long as the actual paper(don’t freak out, that’s a good thing). Below is a general example of what your outline shouldlook like, except that yours will be much longer. Make sure that your outline includes thefollowing:Topic sentences for each section (marked by Roman numerals)Subtopics:• Major key pointsReferences for each point that you intend to cover.Outline ComponentsI. Title  Should inform the reader of what the paper is about.  When constructing a title, choose informative over cute.II. Introduction: Topic sentence that states the basic idea/premise of your paper. For example,if you are examining the role of neuropeptides in parental behavior, your first sentence mightintroduce parental behavior and its significance in species survival(Reference- see format for in-text citations)
. a. Introduce your system

i.Define the system, its function, types present, etc. (Reference- see format
for in-text citations)

ii. If you are comparing organisms, briefly introduce the organisms
(Reference- see format for in-text citations)

b. What is the main thesis of your paper?
c.
What if your goal with this paper?
d.
Provide the scientific reasoning as to why your topic is interesting/relevant
e.
Be brief and concise

III. Section I.
Topic sentence summarizing the main point of this section (Reference- see
format for intext citations).
For each section you should have about (3 to 4) three to four paragraphs. For this outline, you only need to include a bullet point for each future paragraph, each bullet point should be a sentence describing the main point that each paragraph will cover. f. Statement First paragraph providing background about this subtopic and main thesis for this subsection. g. Sentence providing support for one aspect of this subtopic. Must include at least one citation. h. Sentence providing support for another aspect of this subtopic. Must include at least one citation.i.
Sentence providing support for another aspect of this subtopic (optional). Mustinclude at least one citation.IV. Section II. Same structure as section I but for your next subtopic.V. Section III. Same structure as section I but for your final subtopic.VI. Conclusion j. Summary

k.
Significance

VII. References
(see reference instructions)

Environmental Development 47 (2023) 100895
Contents lists available at ScienceDirect
Environmental Development
journal homepage: www.elsevier.com/locate/envdev
Integrating a conceptual framework for the sustainable
development goals in the mangrove ecosystem: A
systematic review
Indira A.L. Eyzaguirre a, c, d, *, Allan Yu Iwama b, Marcus E.B. Fernandes a, c
a
Mangrove Ecology Laboratory, Federal University of Pará, Alameda Leandro Ribeiro 68600-000, Aldeia, Bragança, Pará, Brazil
Posgraduate Programme in Development and Environment, Federal University of Paraíba, Campus I Lot. Cidade Universitária, 58051-970 Joao
Pessoa, Paraíba, Brazil
c
Sarambuí Association, Perpetuo Socorro, Bragança, Pará, Brazil
d
Resiliencia Innovadora NGO, Lima, Peru
b
A R T I C L E I N F O
A B S T R A C T
Keywords:
Mangrove wetlands
Ecosystem services and threats
2030 Agenda
Ramsar strategic plan
Conservation strategies
Mangrove forests are highly productive wetlands and provide essential ecosystem services for the
well-being of human communities, with the Ramsar Convention being the main international
agreement for planning conservation strategies for these areas of great international relevance.
The present study carried out a systematic review to envision a conceptual framework on the
alignment of these strategies with sustainable development (SD) and its objectives (SDGs), based
on the identification of ecosystem services and their possible threats related to mangrove forest in
the Ramsar classification. The study was carried out using the PSALSAR (Protocol-SearchAppraisal-Synthesis-Analysis-Report) framework and an open-access database, where the search
for studies was not restricted to Ramsar Sites only. Since 1991, interest in questions about sus
tainable development in mangrove areas has increased, almost a decade after the first article was
registered in search databases and repositories on this topic. The main SDGs addressed are related
to SDG 13 (Action on Global Climate Change; 30%) and SDG 14 (Life in Water; 3%), while the
goals with low performance in countries that have mangrove forests are: SDG 1 (No Poverty), SDG
2 (Zero Hunger), SDG 8 (Decent Work), SDG 13 (Climate Change), SDG 14 (Life in Water), and
SDG 15 (Life on Land). However, it is still necessary to fill gaps in knowledge about the role of
mangroves in the SDGs through the systematization of methods and the use of indicators that
capture the socio-ecological dimensions, in order to assist in the evaluation of the SD. This re
quires a conceptual framework with five key elements, knowing the plan of the 2030 Agenda,
SDG implementation based on ecosystem services and threats, collection and monitoring of data
of the SDGs, promoting transparent and decentralized governance, and effectiveness SDGs in all
countries based on the science-policy interface, which address the SDGs in this ecosystem to
comply with the Ramsar Sites Strategic Plan and the 2030 Agenda, both based on the ecosystem
services offered by mangroves, in order to address the identified threats and create a set of in
dicators for the purpose of monitoring the SDGs in relation to this ecosystem.
* Corresponding author. Mangrove Ecology Laboratory, Federal University of Pará, Alameda Leandro Ribeiro 68600-000, Aldeia, Bragança, Pará,
Brazil.
E-mail address: indira.eyza@gmail.com (I.A.L. Eyzaguirre).
https://doi.org/10.1016/j.envdev.2023.100895
Received 17 January 2023; Received in revised form 8 May 2023; Accepted 5 July 2023
Available online 8 July 2023
2211-4645/© 2023 Published by Elsevier B.V.
Environmental Development 47 (2023) 100895
I.A.L. Eyzaguirre et al.
1. Introduction
Mangrove forests cover more than 137,000 km2 around the world (Giri et al., 2011), 90% of which are in developing countries
(López-Angarita et al., 2016). Areas with the greatest extension of mangrove vegetation are located in Indonesia (23%), Brazil (7%),
and Mexico (5%). This ecosystem is highly productive (Alongi, 2012) due to the quality and quantity of the ecosystem services it
provides, such as harvesting wood and the provision of crabs (Duke and Bochove, 2014) for the well-being of coastal communities
(Barbier et al., 2011). The mangrove wetland is a complex socio-ecological system (Dahdouh-Guebas et al., 2021) of worldwide
importance (Duke et al., 2007) that has been suffering various threats around the world (Semeniuk and Cresswell, 2018). The main
pressure vectors have been the loss of mangrove forests to replacement by aquaculture and agriculture (Thomas et al., 2017). These
pressures threaten the maintenance of mangrove ecosystem services (Islam et al., 2018) and their sustainability, since tropical forests
play an important role in contributing to the SDG (Swamy et al., 2018).
Sustainable development (SD) means the use of natural resources without jeopardizing the basic needs of future generations (IPCC,
2021) and designed to achieve a balance of the environmental, economic and social axes (Mensah, 2019). In 2015, the 2030 Agenda
was proposed which involves commitment to the so-called five Ps: People, Planet, Prosperity, Peace, and Partnerships adopted by the
United Nations (UN, 2015). Member countries of the United Nations adopted this Agenda in order to plan a prosperous future based on
17 SDGs, 169 targets, and more than 200 indicators proposed within a strategic, indivisible, and universal plan (Bennich et al., 2020),
in order to solve problems in the world with the main focus on eradicating poverty (UN, 2021a). These objectives stem from the union
of great efforts and treaties made since the Earth Convention in Rio de Janeiro (UN, 1992) to achieve the fulfilment of the Millennium
Development Goals (UN, 2000) and came into force in 2016 to promote economic growth while protecting the environment and
including social participation (Mensah, 2019).
Worldwide discussion of wetlands conservation led to the Ramsar Convention, one of the first international agreements designed to
conserve and promote the sustainable use of wetlands, including mangrove forests (RAMSAR, 1971; Kingsford et al., 2021), including
mangrove areas, which are currently represented at 305 Ramsar Sites throughout the world (RAMSAR, 2021). In 2015, the Ramsar
Strategic Plan for 2016–2024 was also defined, proposing four objectives and 19 targets linked to the SDGs to deal with the drivers of
wetland degradation and to conserve, and effectively manage a network of Ramsar Sites (RAMSAR, 2022). There is little evidence of
the real impact of treaties such as the Ramsar Convention, inspection legislation or even conservation legislation (IPCC, 2022) on
mangrove wetlands. Thus, the effective management of these sites is still a challenge, mainly due to the lack of commitment on the part
of the stakeholders and of incentives for legislation to protect these areas (Shah and Atisa, 2021).
In that sense, the first step towards achieving SD in wetlands is to increase the number of Ramsar Sites and implement a conceptual
framework for adaptive management (Kingsford et al., 2021). There is currently no agreement on how SDGs can impact policy through
science (Bennich et al., 2020) but there are global methodologies to assess SDG targets based on metrics that provide data (Fraisl et al.,
2020). Even so, there are gaps in knowledge as to how far SDG goals are being met (Zeng et al., 2020), mainly related to effectiveness
issues and to the lack of contextualized compliance metrics that go beyond statistics (Ordaz, 2019). Thus, to prevent sustainable
development and its goals from becoming a mere fad due to the lack of a precise and exact definition of its advances (Menash and
Enu-Kwesi, 2019), as, for example, in the role of mangrove forests in the 2030 Agenda, it is necessary to carry out theoretical studies in
order to propose a framework whereby these SDG can be better organized. In addition, integrating ecosystem services and their main
threats into SDG assessment studies is of paramount importance (Wood et al., 2018) because this knowledge is still lacking (Bennich
et al., 2020). One of the important ways to expand knowledge on the subject is to fill these gaps with review studies integrated with
open-access databases (Davidson et al., 2019) and it is the first step to take.
The SD, SDG, and Ramsar Sites in the present study, have mangrove forests as a common factor. They are a unique ecosystem that
safeguards biological diversity under the criteria of RAMSAR groups A (rare or unique sites) and B (sites of importance for biological
conservation) (RAMSAR, 2021). For that reason, to assess the SDGs, it is necessary to identify knowledge gaps, relating them to
ecosystem services and threats to the mangrove formations that are linked to natural or anthropogenic pressures (Liao et al., 2019).
Review studies, based on standardized protocols (O’Hagan et al., 2018), have been one of the ways to identify gaps in knowledge (Cook
et al., 2013) regarding the science of SDG studies in the mangrove ecosystem, as they support decision-making (Higgins et al., 2019)
and are the basis for proposing a theoretical framework as some previous studies have already done (Govindan et al., 2021).
Accordingly, this study formulated the following guiding questions: i) what are the topics addressed in the conceptual framework of
the SDG in the mangrove ecosystem (not necessarily declared as Ramsar Sites)? ii) What is the theoretical status of the Ramsar Sites, in
the mangrove category, in regard to the SDG? and iii) What are the challenges and gaps in studies on SDG focusing on the reality
(ecosystem services and threats) of Ramsar Sites that include mangroves? Thus, the present study aimed to propose a conceptual
framework for SDG in relation to the mangrove ecosystem, as a baseline scenario, based on a systematic review relating them to
Ramsar Sites. Specifically, the objectives are 1) to identify the main topics studied that involve the science of the SDG and Ramsar Sites
in the mangrove ecosystem through systematic review and 2) to define a conceptual framework to think about the SD of the mangrove
ecosystem in the context of the SDG, and the main threats to, and services provided by the mangrove ecosystem defined in the Ramsar
Sites that contain it.
2. Methods
The design, search, and analysis of the data obtained followed review study protocols (O’Hagan et al., 2018) such as PSALSAR
(Protocol-Search-Appraisal-Synthesis-Analysis-Report) based on the PIPOC (Population, Intervention, Comparison, Outcome, and
Context) framework, applying steps to perform the systematic review (Mengist et al., 2020) (Appendix A.1). In addition, inclusion and
2
Environmental Development 47 (2023) 100895
I.A.L. Eyzaguirre et al.
exclusion criteria were defined, as follows: i) keywords inserted in the title and abstract sections; ii) type of documents such as article
and review paper; and iii) research carried out in the mangrove ecosystem, and the search was not restricted to those studies involving
Ramsar Sites.
2.1. Data collection
For the present study, the ‘title’ and ‘abstract’ sections of two databases: Scopus and Web of Science (WoS) were searched as it is
more efficient to search for documents in these sections (Mateen et al., 2013). Scopus and WoS were used as the main databases
(Gusenbauer and Haddaway, 2020), without including grey literature. The timeframe was the period between 1945 and 2021. The
search words and phrases were ‘sustainable development’, ‘sustainable Development Goal*’, ‘SDG’ and ‘Ramsar*’ combined with
‘mangrove*’ in order to obtain more accurate documents (Bramer et al., 2017). The first search stage returned 782 documents, from
which scientific documents irrelevant to the guiding questions were eliminated. The second stage returned 262 documents, with 42
scientific documents chosen to be evaluated according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses PRISMA (Fig. A.1), since they were the only documents that directly mentioned some SDG and Ramsar Sites. The low-performance
Table 1
Status of the SDGs in the scientific papers found on the mangrove related to information from the RAMSAR Strategic Plan.
Countries
Indonesia
# Scientific papers (SP)
# Ramsar Sites
Ramsar Site extension (km2)
Mangrove extension (km2)
Main ES
3
2
4
2
6
3
3
5
8
64
6
1
4
7
11,302.76
92,998.34
44,150.68
957.36
6017
5326.40
481.68
27,729.48
10,521.26
7260.03
5554.21
4435.33
3848.50
171.34
educational (7); food (7); hazard (7); inspirational (7); recreation (7); scientific (7); spiritual
(7); tourism (7); biodiversity (6); control (6); detoxification (6); erosion (6); protection (6);
water (6)
water (101); harvesting (100); use (95); agricultural (92); human (91); aquaculture (77);
urban (75); pollution (73); modifications (63); waste (63); settlements (60); tourism (60);
aquatic (59); fishing (59); regulation (55); effluents (54); agriculture (52); conversion (51);
land (51); housing (43); logging (41); forestry (32); household (32); hunting (32); industrial
(32); sewage (32); disturbance (31); garbage (31); intrusions (31); transportation (26);
mining (23); military (22); alien (20)
deforestation (3); aquaculture (2); climate change (2); conversion (2); degradation (2);
erosion (2); disasters (storm, cyclones) (2); logging (2); population (2); corruption (1);
growth (1); cultivation (1); depletion (1); development (1); destruction (1); economic (1);
encroachment (1); farming (1)
SDG 1, SDG 2, SDG 6, SDG 13, SDG 14, SDG 15
Social, Natural, Economic and Productivity
SDG 1, SDG 2, SDG 3, SDG 6, SDG 7, SDG 8, SDG 9, SDG 11, SDG 12, SDG 13, SDG 14, SDG
15
1.5.3, 2.5.1, 3.3.5, 9.a.1, 9.2.2, 9.2.1, 9.1.2, 8.9.1, 7.2.1, 6.a.1, 6.6.1, 6.5.2, 15.c.1, 15.b.1,
15.a.1, 15.8.1, 15.7.1, 15.6.1, 15.2.1, 15.1.1, 14.4.4, 14.1.1, 13.1.3, 13.1.2, 12.c.1, 12.6.1,
11.b.1, 11.4.1, 11.2.1
SDG 1; SDG 2; SDG 3; SDG 4; SDG 5; SDG 6; SDG 8; SDG 9; SDG 10; SDG 11; SDG 12; SDG
13; SDG 14; SDG 15; SDG 16; SDG 17
6.6, 6.5, 15.4, 15.3, 15.2, 15.1, 14.2, 13.1, 12.4, 11.b, 11.a, 11.4, 11.3
11.3, 11.4, 11.a, 11.b, 13.1, 14.2, 15.1, 15.2, 15.3, 15.4, 6.5, 6.6
11.3, 11.4, 11.a, 11.b, 13.1, 14.2, 15.1, 15.2, 15.3, 15.4, 6.3, 6.4, 6.5, 6.6
15.8
11.4, 11.5, 11.6, 11.7, 12.2, 12.6, 14.1, 14.2, 14.3, 14.4, 14.5, 14.7, 14.b, 15.1, 15.2, 15.3,
15.4, 15.5, 15.6, 15.7, 2.3, 2.5, 3.9, 6.3, 6.4, 6.5, 6.6, 6.a, 6.b, 8.4, 9.1, 9.5
6.4, 6.5, 6.6
1.b, 11.3, 11.4, 11.a, 11.b, 13.2, 14.4, 14.5, 14.c, 15.9, 2.4, 6.1, 6.2, 6.5, 8.3, 8.9
6.6, 15.1, 14.5, 11.4
5.a, 14.7, 6.5, 14.c, 11.b, 1.4, 8.4
2.5, 15.c, 2.3, 5.5, 5.a, 6.b, 12.8
15.9, 1.5, 14.7
14.4, 6.6, 15.1, 14.2, 15.2, 15.3
1.b, 11.3, 11.4, 11.a, 11.b, 12.b, 13.2, 14.4, 14.5, 14.c, 15.9, 2.4, 6.5, 8.3, 8.9
17.6, 9.a, 14.5, 9.5, 14.3, 14.4
17.9, 2.5, 6.5, 6.6, 15.1, 17.6, 17.7, 9.1, 11.a, 14.2
6.a, 17.9, 2.4, 11.3, 13.1, 13.3, 4.7, 4.a, 15.7
10.6, 9.a, 15.a, 15.b, 17.3
2.5, 6.a, 17.9, 1.b, 6.5, 6.6, 10.6, 12.4, 14.5, 14.c, 15.1, 15.6, 16.8, 17.6, 17.7
2.4, 2.5, 6.a, 11.3, 13.1, 13.3, 15.c, 17.9
Focus group, Discussions, Household, Surveys, Questionnaire, Interviews, Review, GIS and
RS
management (7); protection (5); conservation (4); information (4); research (4); restoration
(4); awareness (3); community (3); government (3); organizations (3); training (3);
adaptation (2); adaptive (2); ecotourism (2); education (2); effective (2)
Main Threats
Threats in SP
SDGs in SP
Indicator in SP
Relative performances (score) related SDG targets
Ramsar Plan Goals
Targets
Address wetland loss/degradation
1
2
3
4
5
Conserve and manage the RAMSAR site
network effectively
Use wetlands wisely
Enhance implementation
Method contribution in SP
Recommendation in SP
6
7
8
9
10
11
12
13
14
15
16
17
18
19
Brazil
Mexico
3
Malaysia
Bangladesh
India
China
Total
23
95
161,234.22
59,520.15
14
33
18
6
4
12
29
16
13
12
14
1
32
3
16
4
7
7
3
6
15
6
10
9
5
15
8
9
16
Environmental Development 47 (2023) 100895
I.A.L. Eyzaguirre et al.
scores of the SDGs by countries (Table A.1) were obtained from a study based on compliance with the metrics of targets around the
world (Zeng et al., 2020). For that purpose, mangrove information was systematized (Giri et al., 2011) by selecting the
low-performance scores of the countries that contain this forest, based on the calculation of SDG status targets (Zeng et al., 2020). In
addition, the Ramsar Sites, the main ecosystem services and the main threats were obtained from the open access database (RAMSAR,
2021).
2.2. Data analysis
The choice of documents for full-text analysis was based on the application of inclusion and exclusion criteria, in addition to the
relevant search words. The selected studies were classified according to the five principles of the 2030 Agenda (5Ps) and the SDGs
mentioned directly based on the frequency of words in all documents. For the analysis of the data obtained from the scientific papers,
the following software was used: i) Xlstat for the quantitative statistical analysis, ii) Voyant Tools (Sampsel, 2018), Iramuteq v0.7 alpha
2 (Analyses Multidimensionelles de Textes et de Questionnaires) for data visualization and analysis (Ratinaud, 2009), and iii) QGIS
v3.16 for spatial data visualization (GLOBIL, 2021; Natural Earth, 2021).
The documents were classified and analyzed by abstract, keywords, objectives, and conclusions according to their similarity in
semantic networks (Alexander et al., 2018). Likewise, Cluster analysis (Reinert’s method) was used through a Descending Hierarchical
Classification (DHC) of evaluation by textual segments of documents evaluating the association between words (Ratinaud, 2009). The
DHC indicates the proximity and similarity of the words throughout the content analysis of the documents, whereby the dimensions
that make up the SD contextualizing the mangrove were identified.
3. Results
3.1. Space-time distribution of the SDG and mangrove
Of the countries that have mangrove ecosystems, 118 are located in tropical and subtropical regions around the world (GLOBIL,
2021) and ~90% of them are in developing countries (López-Angarita et al., 2016). The scientific papers found referred to research
carried out in 24 countries and 305 Ramsar Sites that have mangrove forests (Fig. 1). The documents mostly address information about
SDG (43%), SD (36%), and Ramsar Sites (21%), most of which are in Asia and Africa, and, to a lesser extent, South America. The
evaluated studies represent 0.3% of the total studies on SD, 0.6% of those on Ramsar Sites and 1.8% of the total studies worldwide on
SDG registered in databases. The study made a full-text analysis of forty-two scientific articles with information on Ramsar Sites (21%)
and the direct relationship between mangrove wetlands and SD (36%) and SDG (43%) for the period between 1991 and 2021 (Fig. 2).
In general, increase of Ramsar Sites in mangrove areas has been somewhat erratic over the last four decades around the world
(Fig. 2). The Ramsar Convention was held in 1971 and the first Ramsar Site was declared in 1974 in the mangrove forests of the
Cobourg Peninsula in Australia (RAMSAR, 1974). Studies on the Ramsar Sites began 33 years later, addressing issues of land use
change such as the introduction of aquaculture in the mangrove ecosystem (Seto and Fragkias, 2007). Although SD was discussed in the
Brundtland Report “Our Common Future” back in 1987 (Mistry et al., 2014), the interest of the academic community in SD and SDG
related to mangrove ecosystems has not been continuous over the last three decades (Fig. 2). The first scientific paper on SD in
mangroves was registered in 1991 (Pons and Fiselier, 1991), a decade after the first registered general study on SD and one year before
the celebration of the Commission on Sustainable Development when Agenda 21 was generated at the Rio 1992 Conference (UN,
1992). The growth of interest in studies relating the mangrove ecosystem to SDG started with the declaration of the 2030 Agenda (UN,
2015), in the same year of the RAMSAR Strategic Plan launch, which began by directly relating SDGs, (mainly 13, 14, and 15), with the
mangrove ecosystem. Those first studies date from 2018 (Fakhruddin et al., 2018a), five years after the first registered study on SDG
addressing climate change issues.
Fig. 1. Spatial distribution of scientific papers, mangrove forests and Ramsar Sites around the world (GLOBIL, 2021; RAMSAR, 2021).
4
Environmental Development 47 (2023) 100895
I.A.L. Eyzaguirre et al.
Fig. 2. Temporal distribution of documents on SD with direct and indirect relation to mangrove ecosystems. CSD: Commission on Sustainable
Development created in Agenda 21 at the Rio 1992 Conference. *First record of data related to SDG in countries with mangrove formations.
Fig. 3. Ecosystem services and main threats declared at Ramsar Sites harboring mangroves.
5
Environmental Development 47 (2023) 100895
I.A.L. Eyzaguirre et al.
3.2. The experience of Ramsar Sites with mangroves: ecosystem services and threats
Although the study did not focus solely on Ramsar Sites, it highlights studies on areas that have mangroves in order to identify the
main ecosystem services and their threats (Fig. A.2). There are currently 305 Ramsar Sites in mangrove wetlands worldwide (see
dataset in (Eyzaguirre, 2023) and nine criteria have been defined to classify these sites, and several criteria can be applied to them at
the same time. They form two groups: Group A: Sites with representative, rare or unique wetlands and B: sites for the conservation of
biological diversity (Fig. 3a). On the one hand, the main threats identified are (non-agricultural) Human settlements (27%), Biological
resource use (22%), and, to a lesser extent, Transportation and service corridors (1%). On the other hand, in some of the ecosystem
services systematized, there were greater numbers of cultural services – recreation and tourism (37%), regulatory services – Erosion
protection (34%), provisioning services – food for humans (28%), and a smaller quantity of supporting services – biodiversity (1%). The
biggest threat to the regulatory services is ‘Human settlements’ (Fig. 3b), affecting, to a greater extent, the sites of group A and the main
threat to the sites of group B is ‘Fishing and harvesting aquatic resources’.
The countries with the highest number of Ramsar Sites and their main threats are the following: 1) Mexico with 64 sites, 4,415,068
km2, threatened by Agricultural and forestry effluents and (non-agricultural) Human settlements; 2) Australia with 12 sites, 2,969,423
km2, and threatened by Dams and water management/use, Energy production and mining, Mining and quarrying, 3) Honduras with 9
sites, 2177.98 km2, and threats such as Urban wastewater and Agriculture & aquaculture and 4) Brazil with 8 sites, 9,299,834 km2, and
with threats stemming from Logging and wood harvesting, Fishing and harvesting aquatic resources, Housing and urban areas and
Marine and freshwater aquaculture. In this last country, there is the largest Ramsar Site in the mangrove category in the world, No 2337
’Amazon Estuary and its Mangroves’, 38,502.53 km2 declared in 2018, and the main threats are (non-agricultural) Human settlements
and Housing and urban areas (RAMSAR, 2018). Both information about ecosystem services and threats are relevant as part of the
construction of the framework proposed here for the conservation of this wetland.
3.3. Mangrove wetland and the 2030 Agenda
There are fewer SD studies of the worldwide review type being presented here (20%), with the majority being studies carried out in
Asian mangrove forests (60%). Most of the scientific papers addressed the SD theme in general (67%), few directly addressed the SDGs,
and the studies that did address those objectives directly were on SDG-13 (30%) and SDG-14 (3%). In addition, climate change (19%),
development (16%), human well-being (13%) and gender (13%) were SD-related themes found in studies that addressed mangrove
ecosystems indirectly, that is, establishing no direct relationship with the SDGs, but that discussed the topic in a general way. Sus
tainable development in the mangrove is mainly related to two aspects: management (n = 27) and conservation (n = 22). These guide
the approaches of the respective studies, addressing aspects such as ecosystem services, climate change, restoration, blue carbon
associated to Greenhouse Gas capture by marine ecosystems (Macreadie et al., 2019), and local communities. For example, conser
vation is linked to management through decision-making by local communities that depend on mangrove ecosystem services, and
mangrove management is addressed through participatory management models.
The main themes of the studies according to the 5Ps of the 2030 Agenda were planet (40%), people (38%), prosperity (21%), and
partnership (1%) (Fig. 4). The SDG science on the mangrove ecosystem, for the most part, mentions the SDG in a general way, with few
Fig. 4. Themes of the 2030 Agenda and themes related to the SDG.
6
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I.A.L. Eyzaguirre et al.
studies that directly address them (e.g., availability of quantitative data directly related to their goals). The main SDGs addressed in the
scientific articles were those related to gender equality (SDG5), poverty eradication (SDG1), action against climate change (SDG13),
and other SDGs (SDG9, SDG4, SDG8, SDG14, and SDG12). The Peace theme was not addressed by any scientific paper in this study.
Studies on the Planet theme mainly addressed studies on management, conservation, ecosystem services, climate change, and blue
carbon. Similarly to the People theme, where studies on conservation, management, and threats relating to gender issues and com
munities were addressed, on the Prosperity them, threats to, and conservation in mangrove formations were addressed, and finally, in
the Partnership aspect, monitoring was the main topic addressed.
The DHC shows six classes that make up the scientific papers on SD in regard to the mangrove ecosystems (Fig. 5). Classes 3, 4, and
5 include words related to the environmental pillar of the SD found in scientific papers, such as climate change directly related to SDG
13 and human activities in class 3, which is closer to class 4 because they are studies about the challenges to the sustainability of the
mangrove forest. These two classes are close to class 5 which addresses studies on blue carbon and land use with pressures from
aquaculture and agriculture. In the social pillar of the SD, studies related to ecosystem services and their economic value related to the
livelihood of communities are part of class 6, which is close to class 2, as it addresses topics such as mangrove management effec
tiveness. Class 1 is close to the environmental pillar and refers to the economic pillar through the socioeconomic benefits generated for
the communities, including preferences and decision-making. The main topics addressed in the science of SDGs based on the 2030
Agenda and the SDG targets are presented in this subsection (3.3. The, 2030 Agenda and mangroves) and below (Section 3.4. The SDG
targets and mangroves) as key elements serving as theoretical basis for the construction of the proposed conceptual framework.
3.4. The SDG targets and mangroves
The countries with the largest extensions of mangrove forests are Indonesia, Brazil, and Mexico, and the first two have the largest
Ramsar Sites. The countries where more scientific papers were found are Bangladesh and Mexico (Table 1). The commonest ecosystem
services among these countries are cultural services (e.g., educational, inspirational, recreational, and scientific services), provisioning
service (e.g., food), and regulatory services (e.g., hazard reduction, detoxification, and pollution control). Among the most common
threats found in scientific papers and Ramsar Sites were those associated to water management, harvesting aquatic resources, agri
culture and aquaculture, and (non-agricultural) Human settlements. Likewise, the key element ‘recovery’ retrieved papers highlighting
corruption and power conflicts linked to REDD + projects in mangrove ecosystems (Rahman et al., 2018) thus signaling the need for
further studies to understand the relationship between projects for recovery and restoration in the face of ‘contracts’ with a bias of
corruption.
The SDGs addressed in the scientific papers were mainly SDG 1, SDG 2, SDG 13, SDG 14, and SDG 15, that is, the mangrove is
directly related to these SDGs. The only SDG not covered by the Ramsar Sites Strategic Plan is SDG7 (Fig. A.3). Although the data on the
targets of these objectives are national, they could be a reflection of the reality of the status of the mangrove formations. In that sense,
the targets with low SDG performance scores were 1.5.3 (disaster risk reduction); 2.5.1 (number of resources earmarked for food and
agriculture protected and those under long-term conservation); 13.1.3 (local government action on disaster risk reduction strategies);
Fig. 5. Pillars of studies on SD in the mangrove ecosystem (DHC): Environmental (classes 3, 4 and 5), Social (classes 6 and 2), and Economic
(class 1).
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I.A.L. Eyzaguirre et al.
14.4.4 (data on illegal overfishing); 15.a.1 (assistance for the sustainable use of biodiversity); 15.b.1 (funding for biodiversity con
servation); 15.c.1 (proportion of wildlife traded or illicitly trafficked); 15.1.1 (Forest area as a percentage of total land area); 15.2.1
(progress in forest management); 15.6.1 (countries adopting equitable social and environmental legislation); 15.7.1 (urgent measures
to curb wildlife trade and poaching); and 15.8.1 (countries adopting legislation on resource use and control of invasive alien species)
(Zeng et al., 2020). In addition, other scientific papers systematized methods and tools, such as Geographic Information Systems and
Remote Sensing, interviews, focus group discussion, and social indicators, such as knowledge transfer, perception; natural indicators
such as coastline stabilization, water levels, sea-level rise, soil characteristics; economic indicators such as socioeconomic data; and
political indicators such as extant legislation related to conservation, all of which helps in the evaluation of the SDGs and their targets
in the mangrove ecosystem.
See the complete table in Table S1. Scientific Paper (SP) has been compiled and summarized (Bahinipati and Sahu, 2012; Chak
raborty et al., 2019; Chow, 2017; Duangjai et al., 2013; Fakhruddin et al., 2018b; Garcia et al., 2013; Hardin et al., 2019; Jia et al.,
2021; Liao et al., 2019; Magalhães et al., 2007; Ottoni et al., 2021; Quintero-Morales et al., 2021; Rahman et al., 2018; Razali et al.,
2020; Razzaque, 2017). Targets are from the RAMSAR Plan (numbers in bold) of low-scoring in mangrove countries (Zeng et al., 2020).
3.5. Conceptual framework for SDG assessment in the mangrove context
A conceptual framework for the assessment of SDGs in relation to the mangrove ecosystem is needed to fulfil the Ramsar Sites
Strategic Plan and the 2030 Agenda based on their ecosystem services in order to address the identified threats (Fig. 6). In that sense,
the inclusion of key actors, the definition of clear objectives, risk assessment, and the inclusion of co-management (Kingsford et al.,
2021) based on the investment in science in order to generate data (Burford et al., 2013), are all indispensable to ensuring the sus
tainable future of mangrove ecosystem. The main challenge to complying with the targets of the SDGs is the statistics included in the
targets (Ordaz, 2019), that is, to get beyond the numbers merely questioning the direction of the SD. Although the conceptual
framework is not a finished recipe, it can offer support to fill gaps present in mangrove ecosystem science associated with SDGs (A).
One of the goals of the Ramsar Strategic Plan for the Sustainable Use of Mangrove Forests embodies the need to carry out studies that
identify (biotic and abiotic) ecosystem services in a holistic way while using methodologies that avoid any disconnection. Therefore,
studies on ecosystem services and threats should use scientific and traditional knowledge in a complementary way (B) combining
methods (Borges et al., 2021).
On the one hand, threats to mangrove swamps should be monitored and related to the advancement of SDG targets (Zeng et al.,
2020), mainly those addressing mangrove degradation/loss. On the other hand, to comply with the two pillars of SD, conservation and
management, the generation of data in a contextualized way must be strengthened through diagnoses and systematization of the
Fig. 6. Conceptual framework to integrate SDGs in mangrove.
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science produced, addressing SDG themes in mangrove ecosystems or listing the results of science with the targets situated in context.
There are SDGs with low-performance scores in countries with mangrove formations where it is recommended to include the objective
associated with renewable energies (SDG7) in traditional communities that depends on mangrove ecosystem services as part of the
path towards sustainability. This is one of the SDGs that is not included in the Ramsar Plan. Conservation and management, key el
ements in this systematic review, towards mangrove forest sustainability must be supported by education (SDG 4) including
science-based stakeholder participation (SDG 17) to develop and update plans and jointly implement actions (C). Designing a sus
tainable future for the mangrove (planet) must include the populations that depend on it (people) considering its ecosystem services
(prosperity and peace) in a joint and participatory way (partnership) towards achieving the 2030 Agenda.
4. Discussion
4.1. Mangrove on sustainable development science
The first SD studies were reported in the 70s (Fig. 2) and in the 80s the Brundtland Conference released its report for our common
future (UN, 1983). Although the first studies on mangrove ecology were recorded in the late 1940s in WoS (Davis and Williams, 1950;
Lawrence, 1949), only a single study on mangroves directly addressed the SD in the 1990s (Pons and Fiselier, 1991). The 2030 Agenda
was adopted by the UN in 2015, when the 17 SDGs were defined (UN, 2021a), and from that date on studies on the mangrove
ecosystem related to the SDGs have increased. In general, however, scientific interest in this area is still incipient, leaving gaps to be
filled (Bennich et al., 2020).
The main purpose of the SDG is to eradicate poverty, protect the planet and guarantee peace, and prosperity to all people,
comprising the 5Ps of the 2030 Agenda (Mensah, 2019); these objectives are formally listed and are indivisible (Leal Filho et al., 2019).
The only P not addressed in a direct way by any scientific paper in this study was ‘peace’, although the feeling of peace is part of the
mangrove cultural services in their provision of human well-being and prosperity (Hsieh et al., 2015). In that respect, including
cultural services in decision-making is indispensable (de Souza Queiroz et al., 2017), since it is related to the feeling of peace that the
mangrove forest offers to its populations (Knowlton et al., 2021) and through its maintenance and subsistence they enjoy the ecosystem
on a day-to-day basis.
Most of the documents retrieved by this paper were reports of studies located on the Asian continent, although similarities were
found in ecosystem services and threats identified in Ramsar Sites among other countries that have mangrove forests such as Indonesia,
Mexico, Australia, Honduras, and Brazil. The Ramsar strategic plan lists 16 of the 17 wetlands SDGs, although the mangrove wetlands
could also be included in SDG7 since, in addition to these forests being used in some countries as renewable energy (Numbere, 2020),
they can be a path to generate sustainable development through access to clean energy in traditional communities, that depend on
mangrove ecosystem services (Kerr et al., 2015).
The mangrove forested Ramsar Sites mainly provide cultural services, also linked to recreation and tourism. That service can
become a conservation action because it is a Nature-based Solution (NbS) related to sustainable tourism linked to SDG11 (Musa
vengane et al., 2020). Provision of services such as food security through resource use (Fernandes et al., 2018) can be directly linked to
SDG2 (Mensi and Udenigwe, 2021). Furthermore, fishing in mangrove areas supports food security and human well-being related to
SDG1, SDG2, SDG3, SDG6, SDG8, SDG12, SDG14, and SDG15 (De Cock et al., 2021; Fakhruddin et al., 2018b; Seary et al., 2021).
Among the regulatory services, the main one is coastal protection, which is linked to SDG13, SDG14, and SDG15 (Chow, 2017).
Furthermore, regulation of climate change (Chakraborty et al., 2019; Simard et al., 2019) and blue carbon capture (Chow, 2017; Rovai
et al., 2022; Wang et al., 2021) are services related to SDG-13 (Chow, 2017; Fakhruddin et al., 2018b).
The SD’s main need is to face threats, including anthropogenic ones (Mensah, 2019) such as the threat that urban expansion
represents for mangrove forests in Asia (Chen and Shih, 2019). Indonesia was the country where the highest number of studies on SD
was found and, where the main threats to its mangrove formations are logging exploitation (Yudha et al., 2021) and aquaculture
(Fitzgerald, 2000; Malik et al., 2015). Countries like Brazil and Malaysia, with fewer studies on this topic, present the threats posed by
housing and urban areas (Hayashi et al., 2019; Kanniah et al., 2015; Moschetto et al., 2021), and agriculture and aquaculture activities
(Alongi et al., 2003; Guimarães et al., 2010). Various topics are addressed in the SDG context in studies on mangrove forests but the
great challenge is still how to better direct them in a contextualized way in order to assess the role of this ecosystem and go beyond the
statistics. In other words, studies that glimpse the challenges and gaps in SGDs and their targets must be carried out in order to prevent
the SDG from serving as a mere ‘smokescreen’, while environmental degradation continues throughout the decade (Zeng et al., 2020).
In addition, attention should be paid to low-performance targets in mangrove harboring countries, such as the SDG6 targets, since
mangrove wetlands and the supply of drinking water are closely linked (Sanford, 2009) due to the filtering function performed by the
trees in this ecosystem (Lin and Dushoff, 2004). At the same time, the mangrove forest formation plays an important role in SDG1 in
strengthening the resilience of vulnerable populations (Berke et al., 2008; Soanes et al., 2021). SDG8 is also related to mangrove forests
and is underperforming in countries that have mangrove wetlands, but sustainable tourism, such as community-based tourism, can be
a way to generate employment and economic growth in communities that depend on them (Ahmad and Suratman, 2021; Marasinghe
et al., 2021). Thus it is necessary to understand how essential it is to propose and effectuate sustainable management and conservation
strategies for these wetlands that envisage their rehabilitation (Chen and Shih, 2019) as, for example, in aquaculture activities (Pons
and Fiselier, 1991) where the strategy mentioned is recovery with the inclusion of stakeholders (Chakraborty et al., 2019; Chow, 2017;
Fakhruddin et al., 2018b; Menéndez et al., 2018). In addition, knowledge of ecosystem services including human well-being can be the
basis for forming policy for the conservation and management of mangrove forest resources (Menéndez et al., 2018).
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4.2. Pillars of mangrove sustainable development: management and conservation
Conservation and sustainable management are important issues for mangrove wetlands (Chen and Shih, 2019) and are two
essential pillars of SD in general (Mensah, 2019). Management is closely linked to conservation through local actions together with
communities (Ladia et al., 2019), and for decision-making (Sangchumnong, 2018) that includes their participation (Mensah, 2019).
Sustainable tourism, through actions in education and creative economy (Garcia et al., 2013) can serve as an important tool for a
sustainability model for mangrove wetlands (Ladia et al., 2019; Sukuryadi et al., 2021), and should include the cooperation of local
stakeholders (Garcia et al., 2013). The inclusion of these stakeholders through community training, strengthening participatory
techniques, and carrying out projects with sustainability over time (Sangchumnong, 2018) is essential to the planning of a sustainable
future for the mangrove ecosystems. In that sense, the protection of mangrove resources with future generations in mind makes it
possible to guarantee equity and access to food for people, based on provision services, and generating prosperity and inclusion.
Furthermore, apart from promoting fair and inclusive societies in the mangrove ecosystem, its governance must be established
(Yonvitner et al., 2020) in fulfilment of those principles (Eyzaguirre and Fernandes, 2018) and with sustainable management in mind.
Therefore, mangrove ecosystem management with a focus on SD should be approached through collaboratively based management
models addressing governance dimensions, as has been done in Indonesia together with coastal communities (Sukuryadi et al., 2021).
The ecological, social, economic, and institutional indicators support the assessment of mangrove forest sustainable development
(Sangchumnong, 2018; Sukuryadi et al., 2021). That can be done from a perspective that addresses important SD issues like gender,
since too few studies assess the relationship between gender and mangrove forest conservation (Ladia et al., 2019), ecosystem services
(Menéndez et al., 2018), and climate change (Chow, 2017).
Management and conservation strategies need to be strengthened, and in the SDG in general, it is necessary to include education
(Shah and Atisa, 2021), and communication for holistic, sustainable development of the mangrove wetlands, applying Education for
Sustainable Development (EDS) advocated by the United Nations (UN, 2019) that connects the SDG4 with other SDGs to think about
the sustainable development, for example for the mangrove ecosystem. Recently, the United Nations Ocean Decade initiated the Ocean
Literacy program (UNESCO-IOC, 2021) in order to build science around marine-coastal ecosystems (UN, 2021b), such as mangroves
(Lecours et al., 2021). In addition to education, it is also expected that scientific interest can give more visibility to the role of
mangroves in the decade of action, listing the SDGs in order to fill in the knowledge gaps.
Sustainability does not mean avoiding or ceasing to carry out activities such as forestry, aquaculture or agriculture, on which many
people and communities depend, but rather, it is carrying out these activities in a more sustainable way considering the environment,
people, and well-being (Pons and Fiselier, 1991). Thus, the economic pillar of SD means that these activities should be better planned,
thinking about creative production, with sustainable tourism linked to the development of local populations (Sangchumnong, 2018).
This can be done by joining efforts to carry out this activity in a way that respects human health, human rights, and gender equality
(SDG5), and generates decent work for neighboring communities (SDG8) (Mensah, 2019).
The main way to successfully link management and sustainability is the identification of major problems and social conflicts that
affect the mangrove forest, in addition to including ecological, social, economic, and institutional indicators when addressing them
(Sangchumnong, 2018). It is necessary to join forces to contribute information and carry out actions in partnerships to ensure the
successful conservation of this ecosystem (Sangchumnong, 2018) and to face the main threats to the mangrove ecosystems’ contri
butions to SD. For example, restoration and sustainable tourism are valued approaches to mangrove forest management and con
servation around the world. However, it is important to think about management beyond restoration and reforestation efforts, which
are often unsuccessful (Garcia et al., 2013), since there are still gaps in conservation strategies, mainly related to the responsibility and
commitment of stakeholders involved in the rehabilitation of mangrove forests (Garcia et al., 2013).
4.3. Key elements of the framework for the sustainable development of mangroves
The framework is proposed based on the literature that directly addresses the SDG experience and recommendations, in addition to
the Ramsar Sites database with mangroves in order to promote the SD of this ecosystem in a contextualized manner:
a. Knowing the plan of the 2030 Agenda (UN, 2015) to go beyond theory: a process of raising awareness regarding the meaning of the
SDG, their impact, and importance, and an assessment of the applicability of SDG targets is necessary and urgent. That will only be
possible through investment in science, technology, and above all, equitable and inclusive education (Leal Filho et al., 2019) in
order to strengthen the management and conservation of the mangrove ecosystems. Not only the academic community should be
aware of the SDG, but also all organizations, especially those that work collecting data from primary sources and that can
contribute with contextualized information and situated in the geographic place.
b. SDG implementation and the mangrove: the information provided by the Ramsar database on ecosystem services available in the
mangroves and their threats (Fig. 3) can be a guide to start research that diagnoses and identifies priority SDGs for this ecosystem in
a contextualizes manner. In addition, relating the role of ecosystem services to the SDG is necessary to reduce the knowledge gaps
(Wood et al., 2018). Cultural services, for example, are the most neglected due to the lack of sociocultural valuation in one of the
countries with the most mangroves in South America, which is Brazil (de Souza Queiroz et al., 2017). The implementation of the
SDGs must be horizontal and focus on the main threats as drivers of preventive strategies to conserve mangroves and promote
sustainable development in the communities that depend on them, for example, through the formulation of public policies arising
from the definition of existing problems (Allen et al., 2018). There is no doubt that this implementation process is a great challenge,
leaving a relevant question about the second principle of the 2030 Agenda: how far are we to “Leave No One Behind” in mangrove
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areas? mainly in coastal communities and countries that have the largest mangrove areas such as Indonesia (Martinez-Alier, 2001),
Brazil (Gillam and Charles, 2019), and Mexico (Rodríguez Aguilera, 2022), which still suffer from environmental racism.
c. Collection and monitoring of data on the SDGs: The environmental, social, and economic spheres of SD are complex, therefore,
studies on the SDGs in relation to mangrove forests need to be evaluated in a contextualized way, since the lack of contextualization
will lead to failure, especially when producing statistical information for decision making, management (Pons and Fiselier, 1991),
and conservation. Likewise, it is considered that the literature does not directly address the SDGs and has many gaps (Del Río Castro
et al., 2021), as well as considering its data source and level of confidence in these data (data quality) to be fundamental. On the one
hand, the source can come from different social actors and through the use of different tools (Fritz et al., 2019), such as those
mentioned in Table 1. Citizen science, together with techniques such as Artificial Intelligence (McClure et al., 2020), for exemple,
can be a fundamental link to narrow information gaps on SDG data in a contextualized manner, including monitoring (Fritz et al.,
2019), such as Mangrove Watch in Australia (Duke, 2009). On the other hand, data quality is certainly the most challenging and
complex factor to be obtained, as it involves monetary and human efforts. In addition, data coverage on SDGs is higher in Europe
compared to other continents such as Africa and Oceania (Fritz et al., 2019), but this depends on the level of adaptation that each
government has regarding the digitization process (ElMassah and Mohieldin, 2020).
d. Transparent and decentralized governance: Open and transparent data governance, although still emerging (Wirtz et al., 2022) in
populous countries with large territorial extensions, is a way to promote the decentralization of monitoring and access to SDG data
in the digitization process (MacFeely, 2019), as is practiced in Brazil (Tinoco et al., 2022). A global example is UN Data (http://
data.un.org/), which makes SDG targets available, although it is still necessary to contextualize and monitor them. This can be done
by prioritizing the SDGs in order to promote data collection more effectively and according to the context (Schmidt-Traub et al.,
2017), as in the case of SDG 1, 13, and 14 regarding mangrove ecosystem (Figs. 4 and 5).
e. Effectiveness of the SDGs in countries that have mangroves: The science-policy interface through dialogue is the basis for enforcing
the 2030 Agenda (Del Río Castro et al., 2021) and implementing wetland conservation and management processes (Clare and
Creed, 2022). On the one hand, the exchange of knowledge at the science-policy interface with coastal communities that includes
the involvement of communities in the management, planning, and zoning of this ecosystem (Garcia et al., 2013; Pons and Fiselier,
1991) is also indispensable, since in many coastal countries marine spatial planning is still incipient (Borges et al., 2020). On the
other hand, the involvement of stakeholders such as government, civil society, academia, citizen, and business (Rashed and Shah,
2021) is essential to meet the goals of the 2030 Agenda. Consequently, this makes the SDGs indispensable, not in isolation but in an
integrated manner (Del Río Castro et al., 2021), especially with the use of a transdisciplinary approach to address
socio-environmental issues related to mangroves and the use of data from primary sources such as data repositories. UN Data
(http://data.un.org/), for example, is a data repository that offers an overview of the indicators, although it is still necessary to
contextualize and monitor such information.
5. Conclusion
Mangrove wetlands are complex socio-ecological systems that provide important ecosystem services. In that sense, planning
conservation strategies is necessary to insert SDG science and promote the 2030 Agenda. The first study on mangrove wetlands from an
SDG perspective was not until 2018 and mainly concerned climate change, development, human well-being, and gender, thus directly
related to SDG 13 and SDG 14. Studies on SDGs must be related to the Ramsar Sites that harbor mangrove forests and must include
ecosystem services such as recreation and science production, food provision, and regulation, such as hazard reduction. They must also
address threats associated to water management, harvesting aquatic resources, agriculture and aquaculture, and (non-agricultural)
Human settlements. The SDG targets with the most deficiencies in countries that have mangrove forests and low score performances in
relation to the SDG metrics, according to the study consulted, are those of: disaster risk reduction, the number of resources earmarked
for food and agriculture protected and under long-term conservation, local government action on disaster risk reduction, data on
illegal overfishing, assistance for the sustainable use of biodiversity, funding for biodiversity conservation, ensuring proportion of the
forest area under conservation in relation to the territory as a whole, progress in forest management, countries adopting equitable
social and environmental legislation, urgent measures to curb wildlife trade and poaching, and countries adopting legislation on
resource use and control of invasive alien species. The database review and analysis studies are a relevant basis for proposals for a
conceptual framework, and in the case of the mangrove wetlands, they are indispensable for identifying the main gaps and challenges
related to the conservation of this world-renowned ecosystem. Conservation and management are related to decision-making by the
social groups such as communities that manage this forest, as they depend on its ecosystem services and are the main ones affected by
threats to it. In that sense, the conceptual framework proposed here envisions the importance of: key actors, the definition of clear
objectives, the inclusion of co-management in addition to the production of information, based on scientific and traditional knowledge,
to fill gaps in the scientific knowledge of mangrove wetlands. Finally, in order to comply with the environmental agendas in favor of
the sustainable development of mangroves, it is essential to know the 2030 Agenda plan in order to adhere to the SDG in a contex
tualized way, reduce the gaps in its implementation by decision makers, rethink the methodology for collecting and monitoring in
dicators, defining a decentralized plan for data governance and sovereignty, and, above all, including stakeholder participation.
Ethical standards
None.
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Formatting of funding sources
I. A. L. Eyzaguirre thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship
(88882.444921/2019–01) and Rufford Small Grants Program (grant number 28236-1) for funding the doctoral fieldwork.
Authors contributions
Conceived and designed this study: I.A.L.E. and M.E.B.F. Collected and analyzed the data: I.A.L.E. and M.E.B.F. Wrote original
draft: I.A.L.E., AYI, and M.E.B.F. Wrote, reviewed & edited: I.A.L.E., M.E.B.F., and AYI.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to
influence the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgments
I. A. L. E. thanks the Laboratório de Ecologia de Manguezal (LAMA/UFPA), Associação Sarambuí, and Resiliencia Innovadora NGO
for providing logistical support and the Rede Internacional de Promotores ODS (RIPO) Brazil for providing an opening to new ideas
from the debates held by the RIPO Brazil team.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.org/10.1016/j.envdev.2023.100895.
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DOI 10.1007/s00468-001-0152-4
O R I G I N A L A RT I C L E
Yoav Bashan · Gina Holguin
Plant growth-promoting bacteria:
a potential tool for arid mangrove reforestation
Received: 10 July 2001 / Accepted: 12 November 2001 / Published online: 24 January 2002
© Springer-Verlag 2002
Abstract Although a few countries protect mangroves
(USA, some states in Mexico), the systematic destruction of these ecosystems is increasing. Deforestation of
mangrove communities is thought to be one of the major
reasons for the decline in coastal fisheries of many tropical and subtropical countries. Although mangroves in the
tropics can regenerate themselves or be restored using
low-technology propagule planting, arid mangroves
(areas having limited or no access to fresh water) can
seldom regenerate, and if they do, it happens very
slowly. To conserve arid tropical mangrove ecosystems,
maintenance and restoration of the microbial communities is required. There is sufficient published evidence to
propose a close microbe–nutrient–plant relationship that
functions as a major mechanism for recycling and conserving essential nutrients in the mangrove ecosystem.
The highly productive and diverse microbial community
living in tropical and subtropical mangrove ecosystems
continuously transforms dead vegetation into sources of
nitrogen, phosphorus, and other nutrients that can later
be used by the plants. In turn, plant-root exudates serve
as a food source for the microorganisms living in the
ecosystem, with other plant material serving a similar
role for larger organisms, such as crabs and detritusfeeding fish. This speculative synthesis of recent work
on growth-promoting bacteria proposes that mangrove
rhizosphere bacteria be used as a tool to enhance reforestation with mangrove seedlings. This can be done by
inoculating seedlings with plant-growth-promoting bacteria participating in one or more of the microbial cycles
of the ecosystem.
Keywords Detritus · Mangrove · Nitrogen fixation ·
Phosphate solubilization · Photosynthetic bacteria
Y. Bashan (✉) · G. Holguin
Environmental Microbiology,
The Center for Biological Research of the Northwest (CIB),
P.O. Box 128, La Paz, Baja California Sur 23000, Mexico
e-mail: bashan@cibnor.mx
Tel.: +52-112-536-33 ext. 3663, Fax: +52-112-54710
Nutrient recycling by bacterial communities
in the mangrove ecosystem
Mangrove ecosystems are rich in organic matter; however, in general, they are nutrient-deficient ecosystems,
especially of nitrogen and phosphorus (Sengupta and
Chaudhuri 1991; Holguin et al. 1992; Alongi et al.
1993; Vazquez et al. 2000), which are indispensable for
plant growth. In spite of this, on a global scale, mangroves are among the most productive ecosystems. This
paradox can be explained by a very efficient recycling
that keeps the scarce nutrients within the system. Microbial activity (bacteria and fungi) is responsible for major
nutrient transformations within a mangrove ecosystem
(Alongi et al. 1993; Holguin et al. 1999, 2001). In tropical Australian mangroves, bacteria and fungi constitute
91% of the total microbial biomass, whereas algae and
protozoa represent only 7% and 2%, respectively
(Alongi 1988, 1994; Bano et al. 1997). However, these
protozoa data, based on cell C conversion factors taken
from the literature, are probably drastically underestimated considering that extraction of protozoa using a
Percoll-sorbitol mixture can yield significantly greater
densities of organisms than most of the other extraction
methods (Alongi 1986).
In terrestrial environments, bacteria colonizing the
surface of plant roots induce root exudation, which
stimulates microbial activity by providing the bacteria
with a source of food (Lynch and Whipps 1990). In
mangroves, root exudates fuel the microbial community
in sediments (Alongi et al. 1993; Nedwell et al. 1994).
Mangrove trees can alter the characteristics of the soil.
For example, mangrove trees can oxidize the soil by
supplying oxygen to the otherwise anaerobic subsoil
transporting oxygen through their aerial roots (Sherman
et al. 1998) and thereby ameliorate the detrimental
effects of hydrogen sulfide in the soil (Thibodeau and
Nickerson 1986; Mckee 1993). These edaphic changes
induced by the plants could influence the proliferation
of certain groups of bacteria in the rhizosphere (Holguin
et al. 2001).
160
Table 1 Bacterial species isolated from mangrove ecosystems with potential as plant-growth-promoting bacteria for arid mangrove
reforestation
Bacterial species
Beneficial property
Azospirillum sp., Azotobacter. sp.,
Rhizobium sp., Clostridium sp.,
and Klebsiella sp
Nitrogen fixation
Vibrio campbelli, Listonella anguillarum,
Vibrio aestuarianus,
and Phyllobacterium sp
Nitrogen fixation
Rhizophora mangle,
Avicennia germinans,
and Laguncularia racemosa
Holguin et al. 1992;
Rojas et al. 2001
Microcoleus chthonoplastes
Nitrogen fixation
Avicennia germinans
Toledo et al. 1995a
Staphylococcus sp
“Helper” bacterium
Avicennia germinans
Holguin and Bashan 1996
Bacillus amyloliquefaciens
Bacillus atrophaeus
Paenibacillus macerans
Xanthobacter agili
Vibrio proteolyticus
Enterobacter aerogene
Enterobacter taylorae
Enterobacter asburiae
Kluyvera cryocrescens
Phosphate solubilization
Avicennia germinans
Vazquez et al. 2000
B. licheniformis
Chryseomonas luteola
Pseudomonas stutzeri
Phosphate solubilization
Languncularia racemosa
Vazquez et al. 2000
Families: Chromatiaceae (purple
sulfur bacteria) and Rhodospirillaceae
(purple nonsulfur bacteria)
Photosynthetic anoxygenic
sulfur bacteria
Not specified
Vethanayagam 1991;
Vethanayagam and
Krishnamurthy 1995
Genera Chloronema, Chromatium,
Beggiatoa, Thiopedia,
and Leucothiobacteria
Photosynthetic anoxygenic
sulfur bacteria
Not specified
Dhevendaran 1984;
Chandrika et al. 1990
Chromatium sp
Photosynthetic anoxygenic
sulfur bacteria
Avicennia germinans
Zuberer and Silver 1978
Genera Rhodobacter and
Rhodopseudomonas
Photosynthetic anoxygenic
sulfur bacteria
Avicennia marina
Shoreit et al. 1994
Plant growth-promoting bacteria
in arid mangrove ecosystems
Plant growth-promoting bacteria (PGPB), studied mainly
in association with crops, can be of various types: nitrogen fixers, phosphate solubilizers, phytohormone producers, siderophore synthesizers, mineral uptake enhancers, root development enhancers, proton extrusion
enhancers, and biocontrol of phytopathogens (Kloepper
et al. 1980; Glick 1995; Bashan and Holguin 1997; Glick
and Bashan 1997). They belong to various genera and
each species might be used singly or together with other
strains to inoculate the plants and enhance their growth.
The study of PGPB in mangroves ecosystems is in its infancy; however, several studies demonstrate the potential
for using rhizosphere bacteria isolated from mangrove
roots as PGPB. Table 1 summarizes potential PGPB in
mangrove ecosystems.
Isolated from various
mangrove species
Reference
Sengupta and
Chaudhuri 1990, 1991
Nitrogen fixation in mangrove ecosystems
Nitrogen (N2) fixation is common in mangroves. High
rates of nitrogen fixation were detected in association
with dead and decomposing leaves, pneumatophores
(aerial roots), the rhizosphere, tree bark, cyanobacterial
mats covering the surface of sediments, and in the
sediments themselves (Gotto and Taylor 1976; Zuberer
and Silver 1978, 1979; Potts 1979; Uchino et al. 1984;
Van der Valk and Attiwill 1984; Hicks and Silvester
1985; Holguin et al. 1992; Mann and Steinke 1992;
Toledo et al. 1995a).
Nitrogen-fixing bacteria identified as members of
the genera Azospirillum, Azotobacter, Rhizobium, Clostridium, and Klebsiella were isolated from the sediments,
rhizosphere, and root surfaces of various mangrove species (Sengupta and Chaudhuri 1990, 1991). In an arid
mangrove in Mexico, several strains of diazotrophic bacteria were isolated from the rhizosphere of the mangroves Rhizophora mangle, Avicennia germinans, and
Laguncularia racemosa. Some of these strains were
identified as Vibrio campbelli, Listonella anguillarum,
161
Vibrio aestuarianus, and Phyllobacterium spp. (Holguin
et al. 1992; Rojas et al. 2001). The amount of nitrogen
contributed by these free nitrogen-fixing bacteria in this
ecosystem is unknown, although we know that the capacity of these bacteria to fix nitrogen is similar to that
for diazotrophic bacteria from the terrestrial environment, such as Azospirillum spp. (Holguin and Bashan
1996; Rojas et al. 2001).
Nitrogen-fixing and non-nitrogen-fixing cyanobacteria, diatoms, green microalgae, bacteria, and fungi were
found colonizing the surface of pneumatophores (aerial
roots) in black mangroves (Potts 1979; Toledo et al.
1995a) (Fig. 1 A–C). Year-round in situ measurements
of nitrogen fixation associated with the aerial roots of
A. germinans in a Mexican mangrove showed rates up to
ten times higher during the summer than during autumn
and winter. The main factors influencing nitrogen fixation were light intensity and water temperature (Toledo
et al. 1995a). Similar results were obtained with aerial
roots of A. marina in South Africa (Mann and Steinke
1992).
Six days after inoculation under controlled conditions
of black mangrove seedlings with the diazotrophic filamentous cyanobacterium, Microcoleus chthonoplastes,
the roots were completely colonized by the cyanobacterium and embedded in a mucilaginous sheath (Fig. 1D, E).
Nitrogen-fixation activity and total nitrogen concentration in inoculated seedlings was significantly higher than
in uninoculated plants (Toledo et al. 1995b). Subsequent
15N-labeling studies showed that the nitrogen fixed by
M. chthonoplastes was assimilated mainly in the plant
leaves, but was also present in other plant tissues
(Bashan et al. 1998). These results imply that the interaction between cyanobacteria and mangrove plantlets is
mutualistic, and suggest the use of cyanobacteria as
inoculants for reforestation programs.
Phosphate-solubilizing bacteria
In marine sediments, phosphates usually precipitate
because of the abundance of cations in the interstitial
water, making phosphorus largely unavailable to plants.
Phosphate-solubilizing bacteria (PSB), as potential suppliers of soluble forms of phosphorus, would provide a
great advantage to mangrove plants.
Almost no research has been focused on this group of
bacteria found in coastal environments, either in temperate or tropical regions (Craven and Hayasaka 1982;
Promod and Dhevendaran 1987) and even less in mangrove ecosystems. In an arid mangrove ecosystem in
Mexico, 12 strains of phosphate-solubilizing bacteria
were isolated from mangrove roots (Vazquez et al.
2000). The phosphate-solubilizing activity of one strain,
B. amyloliquefaciens, had an average solubilization capacity of 400 mg of phosphate per liter of bacterial suspension (108 cfu/ml). This amount could theoretically
supply a small terrestrial plant with its daily requirement
of phosphate. The mechanism involved in phosphate
solubilization was probably the production of organic
acids (Vazquez et al. 2000).
Photosynthetic anoxygenic bacteria
Members of this group of bacteria include purple sulfur
bacteria and green and purple nonsulfur bacteria. Sulfurrich mangrove ecosystems, which have mainly anaerobic
soil environments, would provide favorable conditions
for the proliferation of these bacteria. Only a few papers
have reported the presence of anoxygenic photosynthetic
bacteria in mangrove environments. Nevertheless, representatives of the families Chromatiaceae (purple sulfur
bacteria) and Rhodospirillaceae (purple nonsulfur bacteria) were found in sediments of a mangrove community
in India (Vethanayagam 1991; Vethanayagam and
Krishnamurthy 1995). The predominant bacteria in the
mangrove ecosystem of Cochin (India) were members of
the genera Chloronema, Chromatium, Beggiatoa, Thiopedia, and Leucothiobacteria. Between 4% and 20% of
the total anaerobes isolated were phototrophic sulfur
bacteria (Dhevendaran 1984; Chandrika et al. 1990).
Large populations of Chromatium grew in enrichment
cultures containing sediments from a mangrove community in Florida. This bacterial species was seen with the
naked eye as a coating on submerged leaves in mangrove
pools (Zuberer and Silver 1978).
Two morphotypes of purple sulfur bacteria were isolated from the submerged part of the pneumatophores of
A. germinans in a semiarid mangrove in Baja California
Sur, Mexico. Initial characterization of the two strains of
purple sulfur bacteria showed typical profiles of the pigments bacteriochlorophylls a and b (Holguin G, unpublished data). In another arid mangrove on the coast of the
Red Sea in Egypt, 225 isolates of purple nonsulfur bacteria
belonging to ten species, representing four different genera, were identified. The strains were isolated from water,
mud, and roots of A. marina specimens. Nine of the ten
species of purple nonsulfur bacteria inhabited the rhizosphere and the root surface of the trees. The most common
genera were Rhodobacter and Rhodopseudomonas, detected in 73% and 80% of the samples (Shoreit et al. 1994).
Although there is yet no published evidence, one can
hypothesize that photosynthetic anoxygenic bacteria, the
predominant photosynthetic bacteria in mangrove communities, in addition to cyanobacteria, may contribute to
the productivity of the mangrove through carbon fixation
(Day et al. 1989).
Conceptual models for microbial transformation
in mangrove sediments
The importance of microbially generated detritus as the
major substrate for bacterial growth in mangrove ecosystems was outlined in a conceptual model (Bano et al.
1997). This model stated that detrital particles loaded
with bacteria channel essential elements through the
162
Fig. 1 Scanning electron microscopy of the lower part (A, B) and
middle part (C) of a pneumatophore of black mangroves
(Avicennia germinans) showing the complete coverage of these
surfaces with microorganisms. A The surface of the pneumatophore colonized by bacteria, filamentous cyanobacteria and
Anabaena sp. B An enlarged view of part A. C The middle part of
a pneumatophore showing colonization by filamentous cyanobac-
teria, bacteria and diatoms. D Artificial inoculation of roots of a
black mangrove seedling with the cyanobacteria Microcoleus
chthonoplastes (arrows). E Filaments of M. chthonoplastes embedded in a thick biofilm layer produced during the plant–bacteria
interaction 4 days after inoculation (a Anabaena sp., b bacteria,
Bf biofilm material, d diatom, Fc filamentous cyanobacteria, m the
cyanobacterium M. chthonoplastes, RS root surface)
163
Fig. 2 Legend see page 164
164
food web by providing nitrogen and phosphorus to protozoa and metazoa, which eventually provide nutrients to
commercially important higher-trophic-level organisms,
such as fish and shrimp. The primary producers, being
light limited, play a lesser role in introducing N and P
into the biomass. However, the energy needed to channel
N into the microbial biomass appears to be derived
largely from the mangrove productivity (Bano et al.
1997). A more recent model (Holguin et al. 2001) focuses on the role of several bacterial groups (nitrogen fixers,
phosphate-so…

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