Received: December 03, 2018; Published: December 11, 2018
Corresponding author: Behrouz Behrouzi-Rad, Retired, Department of Environment,Wildlife Ecology specialist, Iran
The research was conducted on Ghabre Nakhoda and Dara islands in Khore Mosa Creek in Persian Gulf on August in 2003, 2009, 2012, and 2016. Total count method was used to obtain the census of the nests and breeding population of terns and Western Reef Heron on Islands. Five species of terns and Western Reef Heron had bred on Ghabre Nakhoda and Dara islands in 2003, 2009, 2012, and 2016. Average breeding pairs of Lesser Crested Tern Thalasseus bengalensis, Swift Tern Thalasseus bergii, Bridled Tern Sterna anaethetus, White-cheeked Tern Sterna repressa, Caspian Tern Hydroprogne caspia and Western Reef Heron Egretta gularis were 1368, 63, 217, 71, and 13 pairs on Ghabre Nakhoda and 127, 7, 54, 4, 9, and 6 pairs on Dara, respectively. Thirty-one species from ten families belonged to two order of water birds recorded on August in 2003, 2009, 2012, and 2016 on both islands. Total number of counted water birds was 26303 individuals on Ghabre Nakhoda and 17404 individuals on Dara Island in 2003, 2009, 2012 and 2016. Maximum species richness on Ghabre Nakhoda was in 2016(31 species), but on Dara island was in 2009(18 species).
Keywords:Breeding population; Terns; Western Reef Heron; Khore Mosa; Persian Gulf; Iran
The detailed knowledge of general seabird ecology and of the numbers and productivity of many populations makes them particularly appropriate as a choice of bio-monitor or bio-indicator [1,2]. The colonial nature of breeding seabirds has several benefits. It allows numbers to be tracked for less effort than if the breeding populations were dispersed, and it allows large quantities of data to be collected from a particular site in a relatively short period of time. However, to be useful, a bio-monitor must respond in a sensitive way to changes in the variable for which it is a proxy measure [1,2]. It is widely accepted that the number of water birds using a site is a good indicator or that site’s biological importance, and they are also important indicator of the ecological condition of their habitats . Terns are colonial breeding in Persian Gulf islands [ 4-7], and are bio-indicators to monitor the status of the environment of Islands . There are 34 islands on northern part of Persian Gulf belong to Iran, six of them located in Khore Mosa in Khuzestan province . Ghabre Nakhoda located in Middle of Khore Mosa and Dara at mouth of Khore Mosa (Figure 1).
The creeks and islands in the Khore Mosa are suitable sites for fishing and harvesting of shrimps and other aquatic species . Terns, Herons, Gulls and Waders form important animal group heavily dependent on the islands for their continued existence . There are many species of these seabirds in the Persian Gulf, [10,11] but the Ghabre Nakhoda and Dara Islands is important breeding site for terns, three in particular nest in vast number on the islands, these are the Lesser Crested Tern Thalasseus bengalensis,, Swift Tern Thalasseus bergii and Birdled Tern Sterna anaethetus. These three species of terns are dominant breeding in most islands of Persian Gulf [5,6] Herons notably Western Reef Heron Egretta gularis Little Egret Egretta garzetta and some wader species especially Crab Plover Dromas ardeola breed on this island [5,7,9,11,12]. Although the islands still support substantial water bird foraging and nesting populations, recent surveys suggest that population size has been reduced from historic levels. On the other hand, one of the aims of monitoring is to provide information for ecological assessment, which can provide early warning of changes that could negatively affect species or ecosystems . For these reasons and protecting the sensitive habitats of water birds in Persian Gulf, also to awareness of breeding population changes for protecting the sensitive habitats, present study was carried out to count and compare the present population of colonial breeding tern’s species on Ghabre Nakhoda and Dara islands in Khore Mosa Creek in Persian Gulf in the breeding season.
Khore Mosa Creek (30o11’01”N49o01’56”E) is consisted of several estuaries, creeks, and a main canal and is an important place for fisheries and aquaculture activities. All creeks around it are most important intertidal habitats of the Persian Gulf shoreline. There are a lot of small islands in Khore Mosa, but two of them (Ghabre Nakhoda and Dara) are important habitats for water birds (Figures 1 & 2). These islands are flat, sandy and Shelly, 70-90% of area of the Ghabre Nakhoda Island covered by vegetation in Feb and March, but More than two third of Dara island surface covered by water by a small branch of creek. All around of the islands are sandy beach (Figures 1 & 2). Area of the Ghabre Nakhoda Island is 3 hectares in high tide and more than 800 hectares in ebbs. There is a Grave in the middle of island, named Ghabre Nakhoda (Ghabr mean is Grave and Nakhoda meaning is Captain). Area of the Dara Island is 160 ha. Main plant species of both islands are Atriplex leucoclada, Stipa capensis, Suaeda fruticosa, Halostachys belangeriana, Calanderula persica, Malva sp, and Cistanche tubolusa. Cistanche tubolosa is vulnerable specie, Calendula persica is an endemic species [5,6,8].
The nests of terns and Western Reef Heron were counted directly on Ghabre Nakhoda and Dara Islands on August 2003,2009,2012 and 2016. The nests of Lesser Crested, White Cheeked, Caspian, and Swift terns (on sandy place of islands without any vegetation) and Western Reef Heron (on short bushes) were counted easily, because they were visible, (Figure 2). The nests of Bridled Tern were under the short bushes and were counted by looking under the bushes. Observation was done on August 15th, every year, which all breeding species had made nests and finished egg-laying. All birds observed and counted on mudflat of around of both islands, Ghabre Nakhda in morning (08:00Am to 12:00PM) and Dara at 14:00PM to 18:00PM. The existing birds were counted directly by total count methods at low tide. For accurate birds counting and determination, binocular 40×10 and telescope 15×60 was used. The birds were identified by studying their characteristic features in accordance with the identification keys evolved by Porter et al. , Colin , Baharat et al. , Sonobe & Usui  and Grimmett et al. .
Species diversity, similarity percentage, evenness and species richness between water birds’ communities, in 2003, 2009,2012, and2016 were measured by Simpson’s, Shannon-Wiener, Menhinnink, Margalef and Brilouin indexes as fallow .
Simpson’s index diversity:
1-D = Simpson’s index of diversity, Ni = Number of individual of species i in the sample, N = Total number of individuals in the sample = Σni, S = Number of species in the sample
Shannon-Wiener index as:
H ' = Σ ( pi)(log2 pi)
H’ = Index of species diversity, pi=proportion of total sample belonging to ith species
S= Number of species and N= total number of all individuals
S= Number of species and N=total number of all individuals in sample.
H=Brilouin index, N= Total number of individuals in entire collection, n1=Number of individuals belonging to species 1, n2= Number of individuals belonging to species 2, and
D = Observed index of species diversity, Dmin = minimum possible index of diversity given S and N., Dmax = Maximum possible index of diversity given S species and N individuals
P = Percentage similarity between sample 1 and 2, P1i = Percentage of species i in community Sample 1, P2i = Percentage of species i in community sample 2.
Density analysis: The individual and total water bird densities for different years on Ghabre Nakhoda and Dara islands were calculated as numbers per hectare (Krebs 2001).
Five species of terns and Western Reef Heron had bred on Ghabre Nakhoda Island in 2003, 2009, 2012, and 2016 (Table1). Average nests number of Lesser Crested Tern Thalasseus bengalensis were, 1200 nests (69.04%), (one egg on each nest, 1200 pairs), Swift Tern Thalasseus bergii 60 nests (3.4%) (one egg in each nest, 60 pairs) mixed with Lesser Crested Tern Sterna bengalensis, Bridled Tern Sterna anethetus 154 nests((8.86%) under the short bushes with154 pairs, small colony of White-cheeked Tern Sterne repressa, 4 nests(0.23%), and Caspian Tern Hydroprogne caspia 49 nests(2.82%) with 49 pairs had been bred in four years. Lesser Crested Tern and Swift Tern had bred on sandy ground on the islands. The Western Reef Heron breed on short bushes of Atriplex leucoclada, on the islands. The breeding population of terns and Western Reef Heron declined from3134 pairs in 2003 to 868 pairs in 2016. Reduction was 27.70% (Figure 3).
Figure 3: Number of nests of terns and Western Reef Heron on Ghabre Nakhoda Island on August 2003, 2009, 2012 and 2016.
Table 1: Comparison of number of nests of terns and Western Reef Heron on Ghabre Nakhoda Island on August 2003, 2009, 2012 and 2016.
The mudflats around Ghabre Nakhoda hold many hundreds of shorebirds and water birds in winter, also in summer, including large number of Numenius arquata, Numenius phaepus, Caldris minuta, Tring stegnatlis and Laridae species (Table 2). Thirty-one species of water birds belonged to eight families were identified on this island from 2003 to 2016. (29 species in 2003, 30species in 2009, 30 species in 2012 and 31 species in 2016) (Table 2). Counting was done at low tide and the area of the island was about 800 ha. Out of 31 species, the Crab Plover, Lesser crested Tern consisted more than 74.27 % of bird’s community in four years (Table 2). Five species were more than one percent and 24 species were less than 1%. Maximum birds were counted in 15 August 2016(8353 individuals 31.75%) and minimum birds were counted on15 August in 2003(5657 individuals 21.50 %). Number of counted birds increased from 2003-2016, 5657<5941<6350<8353 (Figure 4), but the number of species was approximately stable (29-31 species). Comparing these numbers, it can be shown that the number of water birds increased (10.25%) (Figure 4), but the breeding pairs declined from 2003-2016(Figure 3).
Figure 4: Total number of birds recorded in Ghabre Nakhoda Island on August in2003, 2009, 2012, and 2016.
Table 3 shows the similarity between birds within 4 years on Ghabre Nakhoda Island. Similarity of breeding species was more than 70% within four years. The lowest similarity was between 2012 and 2016(70.12). The similarity between birds observed within four years were more than 70%. Highest similarity was 86.15 % (between 2009 and 2012) and lowest similarity was 58.01% between 2003 and 2016.
Ecological Methodology software by Krebs 2001 was used to determine and compare the diversity of the water birds on Ghabre Nakhoda Island. The total bird species richness (No. of species present Table 2) was maximum in 2016(31 species) and minimum in 2003(29 species). Shannon Wiener index (H´) (Table 3) for total birds on Ghabre Nakhoda Island was on higher side with maximum during August 2016(1.82) and minimum in 2009(1.401) The evenness for total birds was maximum in August 2016 (0.199) and minimum in August 2009(0.1353). The value of evenness was found highest (0.199) in 2016 and lowest (0.1353) in 2009. The Simpson’s index of dominance was highest in 2003 (C=0.3451) and lowest in 2012 (C=0.2742). Marglef’s richness Index varied between 3.24 (2003, 3.337 in, 2009, 3.312 2012 and 3.322 in 2016), (Table 4).
Dara Island is Greater than Ghabre Nakhoda, with a chain of high vegetated dunce along its western and eastern margins and around the southern end. The central part of island covering by water during high tide is without plant (Figure 2). Western part of island covered by vegetation is a suitable place for breeding of Bridled Tern. Nests of the breeding birds were counted at high tide and the area of island was 160 ha (Figure 1). Five species in 2003 six species in 2009, four species in 2012 and four species in 2016 had been bred on this island (Table 5). Breeding bird’s population increased from 164 pairs in 2003 to 347 pairs in 2016 (Figure 5). Breeding pairs of birds increased about two times. The Lesser Crested Tern was the dominate breeder species and breeding population of this species increased from 110 pairs in 2003 to 506 pairs in 2016. 142 pairs of Bridled Tern had bred in 2016 but had not bred in 2003. White-cheeked Tern had not bred in 2012 and 2016, but had bred in 2003 and 2009 (Table 5). In general, the total breeding population increased from 2003 to 2016 (Figure 5). Eighteen species of water birds were identified on the island in 2003, 2009, 2012, and 2016, (Table 6). Population of these 18 species increased from 4007 in 2003 to 5083 individuals in 2016 (Figure 5). Counting was done at low tide and the area of the island was about 500 ha.
Figure 5: Total number of nests of terns and Western Reef Heron on Dara Island on August in 2003, 2009.2012 and 2016.
Diversity is a major aspect of species structure in avian community. Ecological Methodology software by Krebs 2001 was used to determine and compare the diversity of the water birds on Dara Island. Table 7 shows the diversity of water birds on Dara Island in 2003-2016.The Shannon’s index of diversity was found highest (H =1.66) in 2016 and lowest (H =1.078) in 2003. The value of evenness was found highest (0.3186) in 2012 and lowest (0.196) in 2003. The Simpson’s index of dominance was highest in 2003 (C=0.5519) and lowest in 2012 (C=0.3196). Krebs (2001) stated that this index gives relatively less importance to rare species and more to common species . The value of Simpson’s Index in the 2012 was 0.6804 i.e. closer to ‘1’, thus, having higher dominance as compared to the value 0.4481 (closer to 0), indicating the lower dominance in August 2003. Simpson (1949) opined that dominance varies inversely with diversity which is in consonance to the present observations) . Marglef’s richness Index varied between 1.641-2.05 (1.688 in, 2003, 2.05 in 2009, 1.672 in 2012 and 0.1.641 in 2016).
The similarity percentage of water bird’s community among four years on Dara Island has been showed in Table 8, it shows there is some difference between breeder species (5 species in 2003 and 4 species in 2016) and breeding population of water birds (164 to 347 pairs) in August 2003 and 2016. These two numbers show that the number of water birds increased (21.17%) in 2016 (Table 6). Despite the differences in the populations of water birds, the similarity between observed species and population were more than 70%. Highest similarity was between 2009 and 2016(79.68%) for breeding birds, the lowest similarity was between 2003 and 2012 (57.55%). Highest similarity was between 2009 and 2016 for observed birds and lowest similarity was between 2003 and 2016.
Dominance results when one or several species control the environment and conditions that influence associated species . A total of 31 species were observed and recorded in and around islands covering both, waders and wading birds. The results indicate that overall 5 bird species dominated the area in terms of relative abundance (Tables 2 & 6). It was revealed that Bridled Tern Sterna anaethetus was the most dominant (46.23%) fallowed by Crab Plover Dromas ardeola (33.90%), Slender–billed Gull Larus genei(4.08%), Black Headed Gull Larus ridibundus (3.01%) on Dara Island, but on Ghabre Nakhoda, Crab Plover (37.57%) flowed by Lesser Crested Tern (36.70%) and Bridled Tern were dominant species (Tables 2 & 6). Two species Bridled Tern (12.48%) and Lesser Crested Tern (78.71%), were dominating breeders on Ghabre Nakhoda Island in 2003-2016 (Table 1), but on Dara Island Lesser Crested Tern (49.60%) and Bridled Tern (21%) were dominant species (Table 5).
Ghabre Nakhoda and Dara islands located in Khore Mosa, which is part of Shadegan marsh and this wetland is Ramsar site and wildlife refuge [5,11,21]. Wildlife refuge of 296000 ha, encompassing all the main wetland areas and the coastal mudflats in the south was established in 1972 and has remained since then . The central and southern portions of Shadegan marsh and the mudflats of Khore–Al-Omayeh and Khore Mosa (a total of 400000 ha.) were designated as a Ramsar site on 23 June 1975[9,11,21]. The site has been identified as an “Important Bird Area” by Birdlife International . Egg-collecting, chick and female harvesting when the females sited on eggs, roosting and staying of fishermen on island (Figure 6), illegal hunting, Pollution of water bodies by chemical compounds of oil Tankers, motor boats and factories are serious treats to the breeding population of birds . Poaching is practiced particularly in the waters around islands. Oil pollution has been reported on the beaches around Bandar Imam in the southeast . The breeding success of the species is sensitive to food availability, predator presence, and human disturbance and oil pollutions in Khore Mosa .
Khore Mosa is an economically and environmentally strategic creek in Persian Gulf. There are six sandy offshore islands in Khore Mosa. Khore Mosa and the southern estuaries of the Shadegan marshes are among the most important intertidal habitats of Persian Gulf shoreline. It holds considerable commercial and noncommercial aquatic species and populations. The creeks and islands in Khore Mosa are suitable habitats for fishing and harvesting of shrimps and other aquatic species. The specific conditions of the Khore Mosa, combined with high nutrient content of this water body, provide attractive conditions for many fish, shrimps and birds’ species to use it as, nursery, breeding and feeding habitat . Terns, waders and gulls form main animal group heavily dependent in the Persian Gulf islands for their continued existence. There are many species of these seabirds on the islands and also on Ghabre Nakhoda and Dara, but six species in particular nest in vast number on the islands. These are the Western Reef Heron Egretta gularis, Lesser Crested Tern Thalasseus bengalensis, Whitecheeked Tern Sterna repressa, Swift Tern Thalasseus bergii, Bridled Tern Sterna anaethetus and Caspian Tern Hydroprogne caspia. All six species occur together on Ghabre Nakhoda and Dara Islands, but each has distinctive nesting habitats, (Figure 1). Ghabre Nakhoda is ecologically extremely important for breeding and wintering of many migratory water bird species, as well as a breeding site for Marine Turtles . Ghabre Nakhoda island is habitat for breeding birds, including at least 2 pairs of Egretta garzetta in 2003 (this species did not breed in 2009, 2012, and 2016), five terns’ species, all together more than3134 pairs in 2003, 1953 pairs in 2009, 997 pairs in 2012 and 868 pairs in 2016, (Table 1) and (Figure 2). Tuck (1974) reported, Mudflats around of this island are important staging and feeding habitat for a wide variety of shorebirds, Gulls and Terns  (Table 2), including up to 744 Larus ridibundus, 1368 Larus genei, 169 Larus fuscus, 9882 Dromas ardeola, 75 Naumenius arquata, 105 Naumenius phaopus. Ghabre Nakhoda, south most island and furthest offshore, is c.3 ha, almost elliptic, and composed mainly of sand with some rocky shores in the south and west. It is fringed with low dunce who encircles a central basin almost completely covered in dance, low scrub. Main plant community of the island is Atriplex+Stipa+Suaeda+Halostachys. Lesser Crested Tern and Swift Tern often make their nests on the bare ground, where each pair incubates a single egg, soon after hatching, the young congregate in a flock “crèche” near the water’s edge, where they are fed by their parents until fledging .These two species unable to colonies areas with too high or too dense vegetation, but nest sites of the Bridled Tern differ according to vegetation cover, height of vegetation and other characters of micro-habitat [24,25]. The Bridled Tern prefers place with a certain degree of cover (Minimum 70%), or even totally covered. Nests of this species are very simple and make under the scrubs especially under the Suaeda sp and Atriplex sp (Figure 2). Nests of the White Cheeked Tern are well spaced out on the beach flat and are often neatly built of twigs. Two eggs are the usual complement, and the young remains near the nest during the fledging period. All four Tern species occur together on Ghabre Nakhoda and Dara islands, but each has distinctive nesting habitat. Khore Mosa complex (Channels, islands, beaches, mudflats and sand hills) is the most important habitat for water birds in Persian Gulf. For this reason, Khore Mosa complex was suggested for classification as sensitive habitat for breeding water birds, , but egg-collecting, chick and female harvesting, when the females site on eggs are serious treats to the breeding population of terns and Crab Plover (Figure 6). Density of bird’s population increased from7.07 to 10.44 and 8.01 to 10.66 on Ghabre Nakhoda and Dara respectively from August 2003 to 2016, but breeding population reduced 27.69% on Ghabre Nakhoda Island and increased more than two times in Dara from 2003 to 2016. Comparing these numbers shows, the breeding population move between to islands. When breeding population of terns on Ghabre Nakhoda island decrease, it leads to an increase on Dara Island. Little Egret had bred only on Gabre Nakhoda Island in 2009(2 pairs) and 2 individuals of Ruddy Turn stone Arenaria interpres had observed in 2009 on Dara Island. Ghabre Nakhoda and Dara islands are more sensitive habitats during summer, because 6 species of water birds (Crab Plover, Swift and Lesser Crested Tern, Bridled Tern and White-cheeked Tern Caspian Tern) breed regularly on these islands. Breeding population of Crab plover on Dara Island was 11500 pairs in 2013, but I could not count the nests of this species in 2016, thus breeding population can’t be compared between 2016 and 2003- 2012. The destruction of historical nesting and feeding grounds has forced water birds to compete for diminishing resources (Figure 6). Clearing and degradation of fringing and littoral island vegetation reduces water bird breeding success as a consequence of the loss of habitat and increased vulnerability to predation by a range of species. The following measures should be taken during Breeding time to protect nests and birds on the two islands. The islands are required to be stopped appropriately to check the fishermen boats anchor to prevent further Population loss of breeding birds. Strengthen enforcement of existing restrictions on the hunting of breeding birds .
a. The breeding success of the species is sensitive to food availability, predator presence, and human disturbance and oil pollutions in Khore Mosa, for these reasons Khore Mosa complex need to be protected during breeding season.
b. It is recommended to initiate study of bird diversity and population status immediately with periodic monitoring in all islands for their conservation and management.
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