Reforestation of grey mangroves (Avicennia marina) along the northern coasts of the Persian Gulf

Every ecosystem supports the living organisms by providing direct and indirect benefits and services. Among these areas, mangrove forests are one of the most fertile ecosystems in the intertidal zones. These natural forests are one of the coastal ecosystems that not only provide a source of food for humans and animals, but also play a major role in protecting and stabilizing coastlines and controlling climate. Mangroves are a breeding ground and a safe habitat for a variety of marine vertebrates and invertebrates. This study explains the experienced methods of propagation and foresting of Avicenna marina species. For the first time in the Persian Gulf, we reported a 5-year evaluation of reforestation method of grey mangrove. Reforestation in the highest latitude of natural forests in the Persian Gulf did not have any side effects on growing of Grey mangrove in the selected sites. As a result, increasing the area of Grey mangrove forests in the Persian Gulf improves the ecosystems of the tidal area. Increasing the chances of fishing and improving the economic conditions of the local communities around this bay will be some of the results of mangrove forestation. Furthermore, this is the first report of a simple method to train all the steps of grey mangrove reforestation.

of propagation and foresting of Avicenna marina species. For the first time in the Persian Gulf, we reported a 5-year evaluation of reforestation method of grey mangrove. Reforestation in the highest latitude of natural forests in the Persian Gulf did not have any side effects on growing of Grey mangrove in the selected sites. As a result, increasing the area of Grey mangrove forests in the Persian Gulf improves the ecosystems of the tidal area. Increasing the chances of fishing and improving the economic conditions of the local communities around this bay will be some of the results of mangrove forestation. Furthermore, this is the first report of a simple method to train all the steps of grey mangrove reforestation.

Introduction
Mangroves include shrub and tree species grow in the coastal intertidal zone (DeYoe et al. 2020). The adaptation of mangrove species enable them to withstand variable environmental conditions such as floods and salinity stresses (Cahoon et al. 2021). Mangroves protect the coast from cyclones, floods, sea level rise, coastal erosion, and wave action (Gijsman et al. 2021). Mangroves as a shelter protect species living underneath from the solar ultraviolet radiation (Lovelock et al. 1992). Mangrove forests have a tremendous ability to trap atmospheric CO 2 and produce oceanic carbon (Maher et al. 2018;Richards and Friess 2016) and also they can absorb carbon to reduce greenhouse effects (Sumarmi et al. 2021).
Mangrove protects coasts. The root networks of the mangroves contribute to stability of the coast lands by keeping the substrate firm, prevent soil erosion and sinking the nutrients (Kathiresan 2012;Pramanick et al. 2020). This process provides clean water and nutritious food to the surrounding ecosystems (Kathiresan 2012;Mishra and Manish 2020). However, in areas where the mangroves are not grown, such as the most coastal lands of the north Persian Gulf in Bushehr province, Iran, the sediments become loose and increase turbidity of the tidal and subtidal zones (Haghshenas et al. 2019). Due to the loss of mangroves, floating sediments deposit on the associated marine ecosystems such as corals or seaweeds and destroy them (Zulkifli et al. 2017). Thus, mangrove plants provide protection to other aquatic environments. They also provides breeding grounds, sources of food, and nursery sites for many species of shellfishes and fishes (Haghshenas et al. 2019). They also provide substrate to the flora and fauna associated with the ecosystem (Carugati et al. 2018). In addition to the mentioned ecological benefits, it seems that the extract of mangrove seeds/fruits, leaves and stems also have pharmaceutical importance used for human, animal and plant pathogens (Carugati et al. 2018).
Despite the wide range of socio economic and ecological benefits provided by mangrove ecosystem, their populations have been decreasing over the past decades (Valiela et al. 2001). Although mangrove loss occurs in all countries, it occurs at a rate of about 90% in developing countries (Carugati et al. 2018). Mangrove forests are being lost due to urbanization, agricultural land reclamation, industrialization, timber and charcoal production, coastal landfills, or are decaying due to the indirect effects of upstream land use and pollutions (Alongi 2002;Valiela et al. 2001). Their biodiversity is likely to be significantly reduced, as the number of species in the mangrove plants is directly related to the extent of the forest (Duke et al. 1998;Ellison 2002).
The supports that mangrove forests provide to marine food webs would be destroyed, mangrovedependent fauna would be lost, and human communities around them would lose their benefits (Duke et al. 2007). On the other hand, coastal industrial developments associated with sea level rise and climate change require the conservation, protection and restoration of tidal wetlands (Barbier et al. 2008;McLeod and Salm 2006). Government laws and regulations, and basic educational structures are needed to communities that can reverse the process of mangrove extinction and ensure that future generations will benefit from these valuable resources (Duke et al. 2007). Mangrove ecosystems, especially in developing countries, are still decreasing at such an alarming rate that they may be completely extinct within the next 100 years (Carugati et al. 2018). During the last 20 years, the area of mangrove ecosystems in the world has decreased by 35% (Feller et al. 2017). However, the global rate of mangrove deforestation has slowed, with annual loss rates ranging from 0.2 to 0.7 percent (Carugati et al. 2018).
The genus Avicennia has been named in honor of the Iranian polymath Avicenna (980-1037) by Carl von Linnaeus (1707-1778) (Austin 1993;Linnaeus 1764). Eight species of genus Avicennia are usually recognized (Table 1). Avicennia marina is distributed in Egypt to South Africa, Madagascar, Seychelles, Aldabra, Comoro Island, Persian Gulf to Pakistan, South India, Sri Lanka, Andaman Island, Malay Peninsula, Indochina, Philippines, North Borneo, Sarawak, Mainland China, Japan, Australia, New Zealand, New Caledonia, and Solomon Island (Fig. 1). On the northern coasts of the Persian Gulf and Oman Sea, natural mangrove forests are estimated to be about 90 km 2 (Zahed et al. 2010) (Fig. 2). In these forests two mangrove species A. marina and Rhizophora mucronata belonging to in the Persian Gulf that has natural mangrove forest is in the protected area of Mel-e-Gonzeh (latitude 27.846732 and longitude 51.581421) (Zahed et al. 2010) (Fig. 3). The oldest available document and report on the protection of mangrove forests in Iran dates back to 1975 and the Mangrove War of Qeshm Island (Harrington 1975). These natural forests are currently protected and reforested by local communities, Department of Natural Resources, and Environment Department (Ghasemi et al. 2010). Beside the natural forest protection, reforestation of mangrove wetland has several applications and benefits including sea water treatment (Wu et al. 2008), municipal wastewater treatment (Ghasemi et al. 2010), mitigating coastal floods and adapting sea-level rise (Takagi 2017(Takagi , 2018. To the best of our knowledge, methodology for A. marina propagation and its reforestation has not been described. Therefore, we tried to share our 5-year experience of reforestation of A. marina on the north coasts of the Persian Gulf.

A. marina reforestation site and soil selection
Choosing a planting site is very important because good planting depends on choosing the best place (Table 2). Knowing the details needed to choose the best location saves time and money on the project. According to previous studies, mangrove forests are found on the lower slopes of coastal drainage basins around the world (Kjerfve 1990). Mangroves also prefer to grow on gentle and high slopes above sea level. (Lewis III 2005). To select the appropriate planting site, water characteristics such as tidal conditions, water salinity, water pH, soil characteristics such as slope, soil texture and type as well as the region's climate such as average rainfall, temperature and humidity of the region should be considered. Due to these cases, several suitable places for mangrove forestation was considered in project in Bushehr province including Khor-e-Soltani (latitude 28.933059 and longitude 50.896734), Khor-e-Shekasteh (latitude 28.823673 and longitude 50.983015), Jainak coast (latitude 28.790090 and longitude 51.025520), and Chah-Talkh coast (latitude 28.826171 and longitude 51.015950) (Fig. 4).
Mangroves usually grow in areas near to forested areas, lands with good soils and streams, and areas where dead leaves accumulate (Sandilyan and Kathiresan 2012). However, the selected locations did not meet most of these criteria, rather they were all firth from which local seasonal floods flow into the Persian Gulf. Mangroves do well in areas where there is a combination of muddy and gravel sediments (Madkour et al. 2014). Planting in areas that are not vulnerable to winds and waves is the single most important factor for high mangrove survival. Mangroves grow in areas where they are shielded from these harsh conditions (Arihafa 2016). More regular flooding stresses mangroves and causes them to die (Lewis III 2005). These mud and gravel sediments and shielded conditions can be found in firth of the Persian Gulf, which is locally called Khur. A. marina can grow on muddy flats with a high tidal level and high salinity, as well as periodic wave and wind impacts (AboEl-Nil 2001). Avicennia sp. has a spike-shaped aerating root (or pneumatophores) system that rises 20-30 cm above the ground. They can withstand the events with this root system (Hoai 2011).
Different soil factors, such as soil erosion, sedimentation rates, salinity, nutrient inputs, and soil quality, are said to have a significant impact on the occurrence, development, and structure of mangroves (Perera et al. 2013). On the drier side of the high salinity margin, A. marina may be planted (Kairo et al. 2001). Since Avicennia sp. shows the best growth response to approximately half the concentration of sodium chloride in seawater, it indicates that the normal habitat of this species is more likely to reflect its tolerance to high sodium levels rather than its optimal adaptation (Connor 1969). A. officinalis, A. alba, and A. marina are the three species. Among them A. officinalis is found growing along rivers in richly organic muddy soil or in inner areas submerged in salt water. A. alba and A. marina can grow on muddy flats with a high tidal level and high salinity (25-30 ppt), as well as periodic wave and wind impacts.

Collecting and planting A. marina seeds
Mangrove seeds are called "propagules" because, unlike most other plant seeds, they germinate when still attached to the tree (Van der Stocken et al. 2019) ( Fig. 5A-C). This is an adaptation that allows them to grow quickly until they fall to the soil below once mature. Grey mangroves are relatively easy to plant in restoration sites. According to many local reports, harvesting Grey mangrove seeds from trees and directly planting them in the soil of areas without the shade of mother star trees has had very little seedling success. Although this method can work, it has a much better chance if the seeds are first rooted and growth at least 50 cm before planting. Picked and dried propagules in the shade can be kept in dry and cool air for up to 2 weeks before peeling and planting.
After the seeds have been collected during August (lower latitude zones of the Persian Gulf) to September (higher latitude zones of the Persian Gulf), they were moved to prepared site with covered green shade net. Propagules were placed in plastic fresh water buckets and soaked with fresh water in the shade. To avoid overcrowding effects, buckets water   was replaced every 12 h. Self-remove the pericarps of propagules done during 5 days and the peeled seeds were separated to cultivate based on the modified previous method (Purnobasuki and Utami 2016) (Fig. 5B). Black polythene bags (10 cm opening diameter × 12 cm height) were filled with soil and arranged in plastic basket (610 × 420 × 330 mm). The baskets were put in 10 cm deep fresh water pond allowing sands to be saturated with water prior to planting. The pericarp-peeled seeds were green in color without black marks and were placed vertically on the medium, the tips of the seeds were upside and the primary root side was pushed into the medium (Fig. 5C, D). Half of the seeds were above the medium surface. This method simulated natural germination conditions before sprouting their first leaves (Alleman and Hester 2011). Fresh water, drying of the pond, salt water and drying of the pond were used periodically to irrigate the seedlings. The pond water depth kept 5 cm during the nursery and let it dry 1 day per week. During November tip of the mangroves were cut and removed to let their stem grow widely, thickened and branched (Fig. 5E). Plants were moved to planting site between February to April. An initial growth phase in a nursery improves seedling survival, especially the presence of shade and indirect light during growth prevents it from drying before four leaves are formed in the seedling. When setting up a greenhouse, these items should be considered: (i) Place the nursery where it has access to both saltwater and fresh water. Set it up by the sea, where it would be flooded by the tides or a river on a regular basis, but away from areas prone to severe flooding. (ii) Build a nursery where water, materials, and mangroves are easiest to come by. (iii) Take into account the distance between where the nursery is planted and the homes of those who work there. The closer the nursery is to the buildings; the more likely regular events would occur. However, ensure that the nursery is closely supervised, since the closer it is to homes, the more it would be exposed to threats from children and animals. (iv) In order to avoid cutting trees, if necessary, the nursery site should be established in an open area. It's ideal to have several trees in the nursery to provide shade in some areas. (v) Choose a location that drains well and is relatively flat and shallow for good drainage. If plants are constantly immersed in water, they will die.

Daily activities at A. marina nursery site
Here's a rundown of things to do every day: I. The act of watering. A. marina seedlings must be watered with freshwater and saltwater to keep the interval of 3 days' wet pool and 1 day's dry pool. Watering should be performed to acclimate seedlings until 4-6 months old. II. In order to protect the newly potted seedlings from direct sunlight, they were placed in a shaded area. A greenhouse shade net was used for permanent mass production of nurseries. III. At least once a week, the nursery was weeded.
Any plants that were not mangroves was removed. IV. We did not use any pesticides or rodenticides.

Choose a planting pattern for A. marina
A. marina grows year-round; however, transferring the seedlings to the planting site in the wet season is better. Planting was avoided during high winds and/ or high tides. If there was a flood, we did not plant anything. After the flood, waited a few days before planting.
Mangroves can be planted using a variety of planting patterns, each with its own set of advantages. Most mangrove planting activities spread the mangroves evenly across the site. In this project, we combined the first and third planting patterns to increase the chances of seedling viability. The survival rate of seedlings after the first year was 90-95%. The following are the three most common patterns (Video S1).
I. Planting in strips. Both types of sites may benefit from the conventional method of planting mangroves. Plant seedlings in rows with equal spacing between them. Plant with regular spacing if the site is covered from waves and wind.
Reduce the spacing between seedlings if the site is exposed with medium to high winds or waves. Some seedlings may need to be transplanted to increase the space between shrubs or trees if they were planted close together and are doing well after 2 years. II. Planting in an inverted V. This is appropriate for locations with moderate waves or winds. Seedlings should be spaced 25 to 50 cm apart in V-shaped groups of about 11 seedlings each. To deflect wave effect, plant so that the V's point faces the sea. Place each V between 1 and 1.5 m apart. After 2 years, if all seedlings in the V pattern are developing well, plant new seedlings in the empty spaces. III. Planting in clusters. This is ideal for locations with high waves or winds. Plant seedlings in small clusters 25 cm to 50 cm apart, with around 10 seedlings per cluster. Each cluster should be spaced between 1 and 1.5 m apart.

Correct planting depth for A. marina
In the muddy selected sites, the seedling with oneside teared bags were pushed into the holes made by foot. Lower the seedling into the hole until the root collar is level with the top of the hole. This will require one people per seedling. The hole was filled with mud substrate with one hand while the other held the seedling at the same height. The substrate around the newly planted seedling was compacted.
Since mangroves do not grow in straight lines in nature, don't worry about spacing your seedlings too closely. Depending on the function and natural conditions, the applied density on aggraded beaches ranges from 1600 plants/ha (2.5 m × 2.5 m) to 5000 plants/ha (2 m × 1 m). The spacing can range from 1 to 1.5 m.
Ensure that the tops of these plants are at least 25 cm above the water level while planting. Within the field of mangrove planting, no fishing or navigation is permitted during the plantation for several years afterward. Cattle or camels should also be kept away from these mangroves to protect their growth.

Discussion
During field the areas that have been introduced is susceptible to biological restoration mainly include with a slope close to zero, coastal estuaries and tidal areas with an average depth of one meter in full mode. Based on this, most of the areas prone to reforestation had optimum growth and survival rate more than 90 percent. Furthermore, all reforested trees started propagule production after age four. The stabilization of the forest was observed in all places after the 4th year, which can be mentioned in the indicators of reproduction, growth of new seedlings and survival of the wetland. In general, mangrove ecosystems are very vulnerable to various types of environmental disturbances and stresses. Mangrove plants are sensitive to the formation of sludge, heavy sedimentation, waterlogging and most importantly, oil and industrial pollution (Jimenez et al. 1985;Nardin et al. 2021;Tam et al. 2005). These activities reduce the absorption of oxygen through respiration and increase the mortality rate of mangroves. Salinity above 90 PSU as a result of reducing the flow of fresh water, evaporation and changing water level patterns due to the construction of dams, dredging, etc. causes the destruction of mangroves (Santini et al. 2015).
The most important natural factors affecting the development of mangrove forests are tidal regime, fresh water sources, bed type, drainage, water salinity, land slope, land use, climate, latitude, soil texture, soil humidity, the concentration of organic, mineral substances and the electrical conductivity of the soil (Safiari 2017). Three criteria and nine sub-criteria for the For the process of locating mangrove forest development areas three identified criteria and nine subcriteria by using the Delphi method after screening the physical properties of the bed (shaphe and characteristics of the beach) and chemical properties of the bed (tides, air temperature, water quality, climate type and rainfall) have been introduced (Andon Petrosian et al. 2013).
In land identification, the most important factors affecting the growth and development of mangrove forests in the Qeshm Island, The Persian Gulf, Iran are tidal factors, soil saturation percentage, soil electrical conductivity, pH and soil texture, soil minerals (magnesium, calcium, sodium etc.), absorption ratio and amount of their exchange (Dehghani et al. 2010). (Nagelkerken et al. 2008). Moreover, longitude and latitude, air humidity and temperature, easy access to permanent fresh water, soil type (soil texture and its constituent elements, salinity and acidity) are the other factors affecting the formation of mangroves (Kamali and Hashim 2011). A map of suitable lands for planting mangrove species was prepared considering the above mentioned criteria and land use pattern and weighting each criterion (Hossain et al. 2003).
In the land rehabilitation guide for mangrove cultivation that soil parameters including texture, density, percentage of rock formation, pH, electrical conductivity, amount of iron sulfide, amount of organic matter and mineral nutrients, ratio of carbon to nitrogen and soil moisture are very important in the successful establishment of this species in an area (Friess 2017). Reviewing the benefits of using low-cost principles in the re-establishment of mangrove forests in America showed that the important determining factors in the successful re-establishment and introduction of mangrove species in an area include the frequency and depth of inundation, wave energy, salinity and water and soil pH, soil type and texture, soil nutrients and slope (Gilman and Ellison 2007). Investigating the habitat of mangrove species in the coasts of India showed that while pointing out the importance of the elements in the soil in the success of planting mangrove trees, the physico-chemical of soil and water are the most important parameters affecting mangrove communities (which have a large percentage of mangrove species) (Bhalla et al. 2008).
For the establishment of mangrove species regulating parameters (soil and water salinity, sulfide level and pH), resource parameters (soil nutrients, light and space) and periodic parameters of water (the duration, abundance and depth of waterlogging) are the most important parameters (Berger et al. 2008). Regarding mangrove planting in order to rehabilitate saline and saturated agricultural lands, physical and chemical parameters of water and soil including pH, electrical conductivity, total dissolved solids, dissolved oxygen and salinity percentage in natural mangrove habitat in Pakistan have been considered (Nazim et al. 2010). Despite the difference in water and soil characteristics, there is no significant difference in vegetation parameters in the two environments and in areas with high salt, saturated with water and unbearable for other species, mangrove is one of the few species that survives (Nazim et al. 2010).
The breakwater installation in an area with an almost regular tidal regime and with a maximum span of 2.3 m, a gentle slope of 1% and in direct contact with waves with a height of less than one meter has led to the re-establishment of mangrove forests with a high percentage of mangrove species (Kamali and Hashim 2011). The temperature factor as one of the factors that affect mangroves in nature showed that mangroves face with a temperature of less than 15 degrees Celsius through the decrease in the rate of photosynthesis and the decrease in seedling growth indicated sensitivity (Simard et al. 2019). The results showed that the best conditions for the establishment of this species are in the range of water pH between 0.9 and 3.8, the pH range of the soil is between 7.4 and 8.5 and the water salinity range is between 3.5 to 17.5 PSU and the type of soil is sandy loam, loamy clay (Bhalla et al. 2008;Santini et al. 2015). Mangroves become more dense under low salinity conditions and settle at salinities between 5 and 30 PSU (Joshi and Ghose 2003). Mangroves spend more energy to maintain water and proper ion concentration at high salinity conditions, so less energy is left for growth and primary production (Joshi and Ghose 2003). Also, high salinity reduces the leaf surface, increases the osmotic pressure of plant sap, increases the ratio of surface area to leaf weight and decreases the amount of potassium, nitrogen, and phosphorus (Gilman and Ellison 2007).
The most important reason for the increase in the size of unsuitable areas for the growth and creation of mangrove forests in the areas planted in this study can be seen as the increase in construction, including the construction of roads, nearest to the entrances of fresh water, and estuaries by increasing the area of shrimp breeding ponds or related channels with them, the construction of wharves and its destructive effects such as sedimentation or dredging, the destruction of the tidal zone by creating walls in these areas. The development of industries without taking into account the characteristics of the mangrove wetland ecosystem can cause the lack of flooding and the formation of a complete lagoon and increase of soil salinity, which can be considered as a limiting factor in establishment and planting of mangroves.
The benefits of rehabilitating mangrove wetlands in these places include increasing shelter for migratory birds, preventing coastal/ estuaries erosion during high tides and sea storms, increasing local fishing due to the increase in demand of fisheries for food with the expansion of wetlands, increasing tourist visits pointing out the places to plant mangrove trees, preventing the expansion of future industries due to the existence of laws restricting the presence of forest and also creating local and rural jobs for the residents around the wetland, from the production of saplings to the protection of the wetland. The services provided by mangrove forests are of significant importance to coastal communities and contribute to the sustainability and resilience of local economies (Hussain and Badola 2010). The costs and benefits of mangrove expansion with those created by aquaculture and forestry can achieve the goals of sustainability and equity as well as economic efficiency in coastal communities (Ron and Padilla 1999).

Conclusion
The need to increase the area of forests in the world due to increasing concerns about global warming causes non-governmental organizations to collaborate with governments to plant trees and expand forest areas. Mangrove tree as a species resistant to heat, salinity and adverse environmental conditions and with minimal need for maintenance or irrigation during growth is a useful choice for spreading on the shores of the Persian Gulf. In addition to the environmental benefits of mangrove forest expansion, its social benefits have prompted local coastal communities to expand mangroves. Based on our findings, A. marina is a useful species for increasing the area of mangrove forests on the northern shores of the Persian Gulf due to its characteristics and simplicity of propagation.