The Nutrient and Carbon Dynamics that Mutually Benefit Coral and Seagrass in Mixed Habitats under the Influence of Groundwater at Bise Coral Reef, Okinawa, Japan 1-15

The Miangaran (also called Izeh) marsh located in vicinity (1.5 Km) of Izeh city at Khouzestan province in south of Iran. The wastewater (domestic sewage, urban-ran-off and industrial) of the Izeh city discharge into the south part of the Izeh marsh. The aim of this study was to determine the effect of water quality by comparing the relative number and species richness and diversity of marsh birds in south and north part of marsh, and to determine what landscape variables could be used to predict the relative number and species richness of marsh birds. Determination of species diversity, richness, evenness, similarity, and number of waterbirds in south part (more polluted part) and north part, as a (low-polluted part) of marsh were carried out from July to September 2011. Eighteen species of migratory waterbirds were present in both south (more Polluted) and north (low-polluted) parts of marsh, but total number of waterbirds in north part (4707 individuals) was twice more than south part (2110 individuals) in summer 2011. Maximum similarity between bird communities in south and north part of marsh was 64.57% (0.77 Morista’s index) in September 2011 and Minimum similarity was 13.44% (0.07 Maritsa’s index) in August 2011. Species diversity and richness of north part were more than south part of marsh, and were in range (10, 9, 11) and (14, 15, 15) species in July, August and September respectively. The study revealed that averages of COD, biological oxygen demand, salinity, SO4 and temperature were in range (9.66-102 mg/L), (50-55 mg/L), (0.96-1.6), (0.61-0.78mg/L), (20-21.6 siliceous) in north and south part of marsh in July, August, and September respectively. The pH, EC, Turbidity, DO, BOD, COD, SO4, NO3, salinity and temperature of water in south part were a little more than north part of marsh, but DO was inverse of other chemical parameters, and in north part was more than south part and were in range (4.66 2.90mg/L). A little difference between averages of physicochemical parameters of water in two parts of marsh has been cased significantly in number, species diversity, and richness of waterbirds in summer 2011.


Introduction
Throughout the history birds migrating, many birds migrate in response to biological requirement, such as the need to find a suitable location for breeding and raising their young, and to be in favorable area for feeding at other times of the year [9]. In some cases, these specific requirements are fulfilled in location separated by distance of thousands of Kilometers [10]. In the other hands, several aspects of the ecology of waterbirds make them useful as bio-indicators. Frist, waterbirds have been shown to track environmental variations, at short (months) and long (years) temporal scales, and at both species and community level [1,27]Second, because many species are top predators and several contaminants often accumulate along the tropic chain, such species may be used as indicators of changes occurring at lower tropic level [7,22]. And third, either the waterbirds themselves or their prey is exploited by humans (e.g. hunting and fisheries), so that hunting bags of waterbirds may be indicative of productivity in nesting or wintering areas (Miller et al., 1998) or breeding parameters of birds may inform on fish stock [14]. It is long time in the world that studying on effect of water pollution on species diversity and population of waterbirds is being done. The application of species diversity and number of waterbirds found on beaches as indicators of oil pollution at sea has been reviewed in a number of recent publications [13,20]. Miangaran marsh is among the most important habitats for migratory International Journal of Marine Science 2014, Vol.4, No.54, 1-10 http://ijms.biopublisher.ca waterbirds in south of Iran [15]. South part of the marsh polluted by wastewater of Izeh city directly. Izeh city evacuate the wastewater directly in to the south part of marsh. The pollutant factors of the wastewater effect on waterbirds habitats, number and species diversity, richness and similarity. We aim to determine the effect of water quality in Miangaran marsh on the relative number and species richness and diversity of marsh birds, and to determine what landscape variables could be used to predict the relative number and species richness of marsh birds. This information can be used to develop more effective, long term conservation strategies, because waterbirds are popular subjects for research and monitoring, and long term datasets of waterbirds count often provide a useful resource as indicator of ecological change [18]. However, different waterbird species undergo population fluctuations for different reason, and a thorough knowledge of the ecology of a given species in required if trends are to be interpreted correctly.

Study Area
Miangaran (also called Izeh) marsh is placed in the southwestern foothills of the Zagros Mountains, 125 km east-northern of Ahwaz at the north of Izeh city in Khuozestan province in south of Iran ( Figure 1) [28,29]. Its altitude is 90 meter from sea level and its area fluctuate 571 to 2102 hectare. Lowest depth of marsh is 70 cm with 40 million m 3 of water in summer and its highest depth when it is full of water is 3 meter with 63 million m 3 of water in winter [7]. The wetland is surrounded by foothills and there is no exit way for water. It is a shallow fresh water marsh almost entirely overgrown with emergent vegetation except around of the edges where heavy grazing and trampling by cattle maintain some areas of open water [15]. Size marsh is fed by local runoff and spring at the base of the nearby hills. Also wastewater of Izeh comes directly through the south part of wetland from conduit and it divides wetland to two parts: south part (more-polluted) and north part (low-polluted) ( Figure  1). On the other hand, it is important wintering area for herons, egrets, gooses, Ruddy shelducks, surface feeding ducks, diving ducks, coots, and common crane [15,29]. In summer there is no ducks and number of herons and gulls are dominant. Several species of waterfowl breed in small number, including, Podiceps ctistatus, Himantopus himantopus and about 10-20 pairs of Ciconia ciconia nest in the general area (including over 5 pairs on telegraph poles in Izeh town). Mid-winter waterfowl censuses have been carried out by the Dep.of the Environment, in the most years science 1975 [29], but there is not information about water birds population and species diversity in summer.

Chemical parameters of water
The wetland is polluted by wastewater (domestic sewage, urban ran-off and industrial) of Izeh city, but the south part of the marsh is more polluted because the wastewater discharge into the south part of wetland. For this cause, for water sampling and bird counting, the marsh divided to tow part: north part (31 o 53 ' 41 " N 49 o 51 ' 42 " E) and south part (32 o 52 ' 19 " N 49 o 51 ' 58 " E). Samples of water were collected in July, August and September from each part of marsh immediately before counting of waterbirds. Three replicates of selected physicochemical water quality parameters were recorded directly at the sampling site and included pH, measured by a pH-meter Waterproof Model Testr30, water temperature was measured by a hand-held thermometer, and dissolved oxygen (DO), which was measured by a HACH® Model Sens ION 6 DO meter. Water samples from each collecting part were stored in polyethylene bottles (500 mL) and transferred in ice analyzed in the laboratory. EC, Turbidity, COD, BOD, NO3 and SO4, of sampled water have been measured according to the Standard method 2005 (section 2000-2810) for determination of mentioned parameter by a certified laboratory, (Research Center of Processing Mineral Materials of Iran, Ministry of Industrial and Mineral).

Bird count
Total count method was used for bird's census in summer (in 10th July, August and September 2011), a day in per month. This method is international method and Wetland International (WI) recommits to counts all waterbirds in all inland wetlands in the world. Birds' counting was performed simultaneously with water sampling. The waterbird abundance was estimated by direct count method as described [2,12]. For watching counting and identifying birds, wide-range binoculars, spotting scope and telescopes were used. The birds were identified by studying their characteristic features in accordance with the identification keys evolved by King et al. (1978), Sonobe & Usui (1993) and Grimmett et al. (2001). With the results which we took from birds counting, number of all birds, Density(1) and then with using Ecological Methodology and Past soft wares, the level of indexes of bio-indicator such as Margalef, species richness(2), Shanon-Winer species diversity (3), Simpson Evenness (4) was specified monthly for wetland. Similarity indexes between two parts of wetland (north and south parts), was specified into percentage by using Morista similarity (5) index. With using T-test difference of number of birds average was specified in two north part(low-polluted) and south part (morepolluted) and also with using Pearson tests depending coefficient between physicochemical parameters and number of birds was specified [12]. D = Density, ni = number of species i, A= Area of marsh, Rmg= Margalef's index, S= Number of species, H'=Index of Species Diversity, Nj =∑Xij = total number of individuals in sample j, Pi=proportion of total sample belonging to ith species, Cλ= Morista's index of similarity between sample j and k, Xij, Xik= Number of individuals of species ith in sample j and sample k, Nk =∑ Xik = total number of individuals in sample k.

Statistical analyses
Species diversity, similarity, evenness and richness of waterbird communities of two parts of wetland were measured by Shannon-Wiener, Simpson's, Morista's , Menhink and Marghalef's indexes [12]. The bird density, diversity, richness and physicchemical parameters are correlated by the help of SPSS software. Correlation between physicochemical parameters and birds communities were measured by Pearson Test (SPSS Version 16).

Number of waterbirds
Eighteen species of waterbirds, 15 species in south part (more polluted part), and 17 species in north (Low-polluted) part as a controlling belonging to eleven families are found in summer 2011 (Table 1). Among them 4 species nest within the Miangaran marsh (on north part of marsh) (Behrouzi-Rad, 2014;Scott, 1995).The total number of waterbirds in summer (July, August. and September) in north part (4707) was twofold more than south part (more Polluted, 2110). Dominant species were Larus sp. in more Polluted part in summer, the detailed analysis of the result of the summering waterbirds survey has been shown that the number of waterbirds in the polluted part and north part can be estimated to a range of 200-5500 birds over different months. This number can fluctuate more than twice. Apparently, natural fluctuation of waterbirds number depends on weather conditions of a certain year, but in micro-habitats of Miangaran wetland depends on local International Journal of Marine Science 2014, Vol.4, No.54, 1-10 http://ijms.biopublisher.ca 4 environment factors as well as water quality. It was noted that 3 Larus species constitute more than 20.13% of all counted birds. These were Larus genei (8.91%), Larus ridibundus (9.32%) and Larus agentatus (1.90%), Only 2 individuals of Anser anser were observed at north part in 10th July 2011. Average density of birds was 7.40 individuals per hectare at south part of wetland and more the twice (16.80) in north part. Lowest waterbird individuals were found in Sept. in north and south part 187 and 797 respectively, but the bird number in north part was more than four time in north part.

Population trend
Birds are commonly utilized as indicators of ecosystem integrity (Alvin Lopez andTaje Mundkur1994-1996). Population levels and breeding success are monitored at many different geographical scales to assess environmental change and to determine future conservation. Various factors contribute to the extensive usage of birds as bio-indicators, (Furness et al., 1997). Also, birds have proven popular study subjects throughout history. Thus, many lengthy time series of data collections exist such as the Christmas Bird Count [9], and Breeding Bird Census [21,6], as well as a large body of behavioral and ecological research. The availability of established study methods for censuring and monitoring performance and their relative ease of application in the field contribute to the attractiveness of birds as bio-indicators. A total of 6817 birds composed of 18 species were counted during the course of this study. The number of individuals per month varied from 187 to 1273 in south part (more Polluted part) and 797-1576 in Low-polluted part (Table 1). Population trend of waterbirds in both part were declined from July to September 2011 (Figure 2). This trend shows the most waterbirds are summer migratory in the Miangaran wetland, because they leave the region in the September. Declining of number of waterbirds in both part of wetlands was similar (Figure 2). It is much easier to make accurate counts of breeding birds, or nests, than to count all birds in marsh bird populations. Pollution may affect waterbirds in many ways as waterbirds are fresh water top predators that biomagnified contaminants to high concentrations. In some parts of the North Sea monitoring pollutants by seabirds as accumulative indicators occurs already, but should be expanded to other areas of the world, using further species as monitors [11]. To examine population trends from July to September 2011, for two Parts of marsh we calculated liner regression of mean of total birds for July, August and September. We found a significant negative trend in the total number of waterbirds in two parts of wetland (p=0.05, slope= 0.113). Because these two parts closed together and only difference between them is wastewater of Izeh city that released to south part of wetland. These pollutants caused the significant difference between waterbirds number. The results of monitoring from July to Sept. 2011 suggest significant fluctuations in the overall waterbirds population on the wetland. The total number of waterbirds varied from 2110 to 4707 individual ( Table 2). Percentage of water birds species in more polluted and low-polluted part of wetland has been showed on Figure 3 (69% >31%). Population of waterbirds in the more polluted part of wetland in an average was 703.3 individuals belong to 9 family, 17 species (9 of them were waterbirds and the rest were wader and wading birds), and in low-polluted part of wetland the average density of birds population were 16.51 individuals belong to 10 family, from 17 species (9 species were waterbirds and 8 species were wader and wading birds) the reason is caused by wastewater enters into the south part and causes repulsion of birds. In the other hand these wastewater cause aquatic organism not to move a lot and make them easy targets to hunt by aquatic  eating birds, but these polluted aquatic organism will cause diseases and make birds sick and will increase mortality of birds. Some parts of this pollution will be transfer by birds to other habitats of the region.
The most number of bird species in more polluted area of wetland in summer was 15 species (Table1). Phonicopterus ruber, Plegadis falcinellus and botaris stelaris, were seen in north part (low-polluted part) of wetland that has relation with their food. Only 2 Anser anser were seen in south part in August. Laridae species eat everything that they can live in all part of wetland.

Similarity of waterbirds communities
Similarity of waterbirds communities between south part (more polluted) and north part (Low-polluted) of Miangaran marsh in summer 2011 has been shown in (Table 2 and Table 3). Maximum similarity was 72.78%,=0.88 Morista's index in July-Sep. between north and south part, and minimum similarity (53.55% = 0.56 Maritsa's index) was in August and Sep. in sumer 2011.

Species diversity, richness and evenness
Eighteen waterbirds species were present in both part of wetland in summer 2011. Four species of the birds were wadding, two species of wading birds ,Botaurus stellaris and Plegadis falcinellus, observed only in north part and two species Ardea cineara and Bubulcus ibis in both parts of wetland.
Species richness of north part was more than south part. Species richness ranged from 9-11 in south part and 14-15 in north part. Population was ranged from 187-1273 in south part and 797-1576 in north part. Species diversity, richness and Evenness of birds have been shown in Table 4 and Figure 4.

Physicochemical parameters of water
Physicochemical parameters pollutants introduced to the environment can impact on ecosystems, and can be found in the whole biosphere. Physicochemical contamination may affect ecosystems, causing changes in the functions of particular organisms. In the last few years, investigations have focused on searching for bio-indicators (both plant and animal organisms) that accumulate toxic substances. The aim of the present study was to discuss selected methods of water quality assessment based on waterbirds used as bio-indicators, paying special attention to water ecosystems, because the Izeh city releases the wastewater with various chemical compositions into  the south part of Miangaran wetland, which more effect on chemical compounds of water in south part than in north part. PH, EC, Turbidity COD, BOD, NO3, SO4 and temperature of water for both Part (south and nourt) of wetlands were measured in 10th July, August and September 2011 (Table 5) by Standard Methods 2005 (part 2000-2810). All Physicochemical parameters of south part (more polluted) were higher than north part (Table 5), except DO was inverse (4.66 mg/L in north part>2.9 mg/L in south part) (Table 5). A little difference between average of these parameters of water at two parts of marsh have been cased significantly in number, species diversity and richness of waterbirds in south and north part of marsh in summer 2011. Pollutants both directly and indirectly threatened birds [10]. For example, Nutrients and sediments from agriculture, urban, runoff, industries and other sources entering Chesapeak Bay, have increased alga bloom, decreased oxygen levels and invertebrate populations. This has decreased sea grasses and population depended upon sea grasses [26]. There were negative correlation between physicochemical parameters of water and number of birds in marsh (Table 6). Biodiversity indexes were also more in north than in south part of marsh (Table 4).

Discussion
Wetlands provide ecological functions such as protective nursery habitat for fish and shellfish, erosion prevention, flood protection, and water filtration [13,31]. They also provide vital feeding, resting, and breeding habitat for resident and migrating birds [31]. Marsh birds and colonial waterbirds face threats to the habitats and sites on which they depend. Conservation of marsh birds and colonial waterbirds is a local matter. Nesting and roosting marsh birds and colonial waterbirds are particularly affected by local conditions. Diversity and number of waterbirds indicate environmental pollution [13]. Inland wetlands are essential parts of wetland systems and provide breeding and foraging habitat for many marsh birds in Iran. The Miangaran wetland is one of the important marsh in the southwestern foothills of the Zagros Mountains, and south part of the marsh directly received domestic, industrial and agricultural wastewater from Izeh city. The border between more polluted and north part (low-polluted) is not very clear, but the water color in more polluted part is darker than low-polluted ( Figure 1). Water pollution was identified as the main threats at polluted part, because the wastewater of Izeh runoff to south part of marsh. The Miangaran wetland is the most important habitat for waterbirds in south of Iran [7,28]. The distribution and population of waterbirds in Miangaran wetland, especially in its shores and around has become better understood in recent years (7,27,28]. More information has been gathered through waterbirds count. Over 86 bird species occur in Miangaran wetland in winter (7,28], of these, about 90% are waterbirds, of these 30% are present in summer (Table 1). Along the south part coast survey on July 2011, most of the waterbirds habitat were polluted (Table 1), and therefore unavailable as feeding grounds (Killing of invertebrate and aquatic vertabrate food supplies). Census data counted less than half of the expected number of waterbirds at south part (Table 1). Many species of marsh birds spend the winter feeding on benthic invertebrates on wetlands coasts. Many species of gulls are highly opportunistic feeders, and exploit a wide range of habitats as well as taking many kinds of food [17]. In tow part of Miangharan wetland waterbird numbers correlated over month with salinity, EC, COD, BOD, NO3, SO4. (Table 6). The marsh bird's community influenced by water quality because, the Average of Shannon-Weaver Index of diversity was greater (H' =2.20 in north part and 1.16 in south part) Shannon-Weaver Index values in north part revealed that this part had the greater diversity in terms of both species richness and evenness. Average Simpson's Index of dominance revealed that south part of marsh was greater dominance (C =0.49 in south and 0.14 in south) Simpson's dominance varies inversely with diversity which is in consonance to the present observations. Marglef's richness Index was greater and varied between 1.23-1.72 with average 1.85 in south and 1.90-1.97 with average 1.94 in north. Evenness in bird communities was greater (E = 0.58) in north and (E = 0.32) in south ( Figure 4 and Table 4). Number, species diversity, evenness and richness in north part of marsh was more than south part, inversely the physicochemical parameters in south were more than north part, except dissolved oxygen ( We need to plan and promote marsh birds monitoring on a national basis and to strive for cooperation of seabird specialists throughout the region. Ideally, a few widespread species should be monitored throughout their ranges in the region, which requires a nationally coordinated effort. Identification of essential roosting and nesting habitat is required to sustain marsh bird populations in a given region of conservation concern. Conservation problems and threats faced by seabirds in the region have been discussed [3], but briefly these are included offshore pollution, commercial exploitation of prey on which seabirds feed, incidental take, human disturbance, habitat reduction, and releasing wastewater in water bodies. Marsh bird conservation is mostly a matter of wetlands conservation. Wastewater chemical related activities are [4,18] major environmental threats to marsh species. Threats include platform construction, drilling in wetlands and offshore, shipping and spillage, and chronic, low-level seepage from surface runoff or subsurface sources. Marsh birds are commonly injured by wetlands pollution and hazardous material releases, that affected birds numbering in the hundreds to thousands in some cases. Injuries can lead directly to mortality or indirect effects through habitat degradation, lost reproductive success, or contaminated food supplies. As upper trophic level feeders, marsh birds rely on a healthy wetland environment to provide the prey base necessary for reproduction, migration and general maintenance. Study on waterbirds biology is useful to indicate environmental quality. Protection, and management of colonial waterbirds and marsh birds can help conserve the broader landscape in which they occur in summer and other non-nesting habitats are critical to the long-term conservation of marsh birds and colonial waterbirds.

Conclussion
This study revealed, In the Miangharan wetland, the water quality affected on number, species diversity, density and richness of birds, because the local environmental factors were the same during the study period on all parts of wetland (south and north part, except releasing the wastewater of Izhe city into south part of marsh). For this reason the physicochemical parameters in south were more than north and inversely the number of birds bio-indexes (Species diversity, richness and evenness were less in south part than in north part of Miangharan marsh.

Suggestion
To get a better understanding of relationships between waterbird population and species diversity and water physicochemical parameters further study is needed to increase the sampling frequencies and periods and to examine more water quality parameters in four season of year.