Avifaunistic study in mangrove areas in a stretch of the São Caetano de Odivelas – Pará coast

— The knowledge of the coastal avifauna is essential to understand the dynamics of the coastal ecosystem along the northern coast of Brazil, which is considered an area of high priority for the conservation of regional biodiversity. The Equatorial Region includes the coast of the States of Rio Grande do Norte to Amapá, and the coast of the States of Maranhão, Pará and Amapá is made up of mangroves, an ecosystem of transition between the terrestrial and marine environments, subject to the tidal regime, this ecosystem on the Amazon coast is of paramount importance because the States of Pará and Maranhão represent 57% of the mangroves in Brazil. This research aimed to determine the occurrence of resident and migratory coastal species, as well as their ecological importance and use in the mangrove ecosystem, the study site was São Caetano de Odivelas, in the locality of São Miguel, the methods of data collection used were: visual observation with the method by estimation in larger populations and open ornithological networks linearly from 6:00 a.m. to 11:00 p.m. and from 3:00 p.m. to 6:00 p.m. for two consecutive days totaling the sample effort amounted to 1.080 net hours. The results showed that 72 species of birds were recorded distributed in 27 families and 11 orders, being these residents, seasonal visitors from the northern hemisphere and other endemic to Brazil. It is concluded that there are several species recorded on the coast in São Caetano de Odivelas - Pará, such as endemic species, residents, and other seasonal visitors.


I. INTRODUCTION
The mangrove forest is one of the ecosystems with the greatest socioeconomic and ecological importance and one of the most productive on the planet. It presents high soil fertility, permanent humidity and high temperatures that generate favorable feeding, reproduction, and protection conditions for many marine species of commercial interest. The environment reduces the vulnerability of the coastal zone to global climate changes, such as changes in rainfall and temperature regimes, an increase in extreme events such as storms and extreme high tides, an increase in the average sea level in the coastal zone and an increase in the concentration of carbon dioxide [17,07,31].
The mangrove forest is defined as "a coastal ecosystem, of transition between terrestrial and marine environments, characteristic of tropical and subtropical regions, subject to tidal regimes" [45]. The global distribution of the mangrove forest reaches 137,760 km², while in Brazil it is extremely significant for its extension and distribution along the coastline occupying an area of 11,144 km² [28]. Brazil has 120 conservation units with mangroves in the interior (55 federal, 46 State and 19 municipal, of which 83% are for sustainable use and 17% for full protection) covering an area of 1,211,444 hectares, which represents 87% of the entire ecosystem in Brazil [31]. The northern region has more than 80% of the national mangrove areas, concentrated in the States of Amapá, Pará and Maranhão.
representation of northern migrant species and colonies of Ciconiiformes [44] using the coastal strip during their life cycle, for reproduction and obtaining food, because it provides the necessary resources for the continuation of biological processes such as feather seedlings, to later return to their areas of origin, thus completing their biological cycle, reproduction and landing area, being indicators of environmental conditions [09, 16,11].
These environments present characteristic avifauna, with restricted species and reproductive strategies strongly influenced by the environmental conditions of the mangrove. This ecosystem is also used as nesting areas by colonies of several species of birds, with a strong hierarchical disposition in the occupation of the best places by the species considered stronger, such as the genus Ardea [33,47]. It is possible to observe all the phases of the reproductive process in the nest area, with a gradient that includes from couples in pre-nuptial ceremonies to pairs with already grown puppies. Adults can move at considerably long distances to capture food for the offspring.
In the neotropics the species of birds well represented in the mangrove area are among the stork families (Ciconiidae), herons and punches (Ardeidae) and spoonbills (Threskiornithidae), being represented by about 10 species almost all colonial. Several species of Neotropical Passeriformes demonstrated a trophic relationship with productivity in the mangrove swamp. The importance of mangrove food resources for this group, where data with different arthropod taxa show a temporal pattern like the pattern of abundance of Passeriformes during the annual cycle in mangrove areas in Venezuela. Studies highlight the importance of these environments for the conservation and maintenance of avifauna [02,42,54,04,23,26,05,06,18]. In this context the research aimed to determine the occurrence of resident and migratory coastal species, as well as their ecological importance and use in the mangrove ecosystem.

II. MATERIAL AND METHODS
São Caetano de Odivelas is part of the Northeast region of the State of Pará and its main city is located at 00 °44 ' 33 'S and 48 ° 01' 03'W (SEPOF, 2011). It is limited to the north with the Atlantic Ocean; to the east with the municipality of Curuçá; to the west with the municipality of Vigia. It has an area of 724.10 km², including its urban center and 41 communities. It has a territorial area of 743.4 km2, with a population density of 22.72 inhab./km 2 and a population of 16,891 inhabitants according to IBGE estimates for 2010.
The vegetation found in the region are: restinga vegetation, mangrove vegetation, floodable natural field vegetation and secondary vegetation [39]. Mangrove vegetation is typically composed of tidal plains under the influence of brackish water, or fluvial marine plains, with ideal physiography for the formation of this vegetation, since they constitute marshy or muddy areas, covered by water during flood tides and discovered at ebb tides, also receiving water from river and underground drainage [40].
The data collection period was six months, being carried out from April 2015 to July 2016. For the census, it was considered the counting one by one when the population was small and, in the large one, the method by estimation was used, when a group of 10 is "mentally photographed" and the rest of the birds are counted by group of 10 [22]. The identification of coastal birds was performed at a specific level with the aid of Tasco binoculars (10X25) and specific identification guides [16].
Ten ornithological nets (2.5 x 12 m; mesh 36 mm) were used, which were positioned linearly in the mangrove. The nets were opened from 6:00 a.m. to 11:00 a.m. and from 2:00 p.m. to 6:00 p.m. inspected every 45 minutes) were simultaneously monitored [21,13]. The captured specimens, after identification, were released near the capture sites and the sample effort totaled 1,080 net hours. The classification and taxonomic order to compose the list of registered bird species followed the 12th edition of the Brazilian List of Birds, published by the Brazilian Committee of Ornithological Records [08].
The Frequency of Occurrence (FO) of the species registered per expedition was calculated. The FO was defined as the percentage of the number of individuals of a species in relation to the total individuals counted. The frequency was calculated with the number of visits in which the species was found over the number of visits made, multiplied by 100. The species were categorized as regular: present in more than 50% of the visits, sporadic: between 25 and 50% and occasional: in less than 25% of the species in the visits.

III. RESULTS AND DISCUSSION
The Neotropical region has a high diversity of birds and it is essential to expand the knowledge about the composition and richness of the bird population of a region to contribute to local ecological studies and migration groups. Birds represent about 38% of the vertebrate fauna associated with mangrove forests around the world, which makes this ecosystem essential for maintaining the diversity of this group. There are a variety of adaptations in birds that allow diverse feeding habits, such as frugivorous, granivorous, insectivorous, nectarivorous, carnivorous, piscivorous, detritivorous or necrophagous and omnivorous. Birds represent an important group for maintaining the ecological balance of an area, since they act as seed dispersers, pollinating agents, population regulators and are also bioindicators of conservation [10]. The Neotropical region has a high diversity of birds and it is essential to expand the knowledge about the composition and richness of the bird population of a region to contribute to local ecological studies and migration groups.
In the community of São Miguel, 72 bird species were recorded distributed in 27 families and 11 orders. Resident species, seasonal visitors from the northern hemisphere and endemic to Brazil (Table 01). The data corroborates the studies carried out in the Resex Mãe Grande Curuçá where 36 families and 70 bird species were recorded [12] and demonstrates its importance for the conservation of this group, since in Brazil 35 families and 86 bird species are recorded that use the mangrove forest in some way throughout its biological cycle [52]. At Rio de Janeiro, 31 bird species were recorded distributed in 18 families on the Pombeba island [51]. The Scolopacidae family had the highest richness with 15% of the species (n: 11), followed by Ardeidae with 13% (n:09), Columbidae 7% (n:05), Sternidae with 6% (n:04) Threskiornithidae , Cathartidae, Charadriidae, Alcedinidae, Accipitridae, Trochilidae, Tyrannidae and Thraupidae each one with 4% (n:03) Rallidae, Thamnophilidae, and Pipridae with 3% each (n:02) and Anatidae, Ciconiidae, Falconidae, Rynchopidae Pandionidae, Psittacidae, Eurypygidae, Picidae, Dendrocolaptidae, Formicariidae, and Turdidae with 1.5% each (n:01). The Scolopacidae family obtained the highest number of species (10) of seasonal visitor from the northern hemisphere. Migrations are seasonal movements at various geographical scales (local, regional, intercontinental, etc.), whose routes include a breeding area. Each year, thousands of birds that breed in the northern hemisphere move to various locations in the south, fleeing the boreal winter. The birds identified as migrants correspond to representatives of the Charadriidae and Scolopacidae families. The species of these families are basically related to the beach, but can be observed in flooded environments, such as swamps and mangroves (Graphic 1).

Fig.1: Number of species present in the families of birds registered on the island of São Miguel in the municipality of São Caetano de Odivelas -Pará, held between April 2015 and July 2016.
The Charadriidae family is distributed along the coast of Brazil, in the intertidal zone of beaches and mangroves, with displacement between these landscapes by the continuous movement in search of food both migratory . The birds feed on the invertebrates of the entomofauna of these habitats, the abundance of the organisms that constitute the food of these birds obeys seasonal cycles, and the peaks of this abundance occur in fixed periods, which makes it possible to synchronize the timing of the arrival of the birds in their "conditioning areas" adjusted to coincide with these peaks of food.
The exchanges between different areas within the landscape have the same ecological function as the more restricted movements between the spots that concentrate food in the same area [27,34]. Another factor can be the variation in scale and time of the density of invertebrates [29,22], and foraging by cohesiveness can quickly decrease the number of local invertebrates. When the abundance of local prey decreases, beach birds move to areas where the food density is higher, such as mangroves.
The protection of migratory birds is linked to the preservation of their breeding, feeding and resting sites. The loss or alteration of wintering and resting sites of these birds may result in the reduction and even the local extinction of some species or the decrease of the population. In this context, the conservation of the mangrove swamp on the island of São , it is necessary to highlight the importance of the quality of the habitats used as resting and feeding points for migratory birds, especially those that cross great geographical barriers during their movements [32].
The family Threskiornithidae (Ciconiiformes Order) includes 13 genera and 32 species of birds widely distributed around the globe, except in Antarctica, highlighting the ibis and spoonbills. They have long and curved beaks, long legs and neck, characteristics that contributed to the occupation of flooded environments and a diet based on aquatic species such as small crustaceans, larvae, mollusks, fishes, and crabs [48]. The Ciconiiformes of the northern coast of Brazil occupy both the continental wetlands, such as the Baixada Maranhense, and the mangroves where about 10 species occur, almost all of which are colonial, which can be monospecific or mixed. Coloniality has provided the development of scientific studies on development, reproductive strategy, and puppy diet due to high detectability.
Several species of Ciconiiformes have their reproductive strategy strongly influenced by the specific conditions of the mangrove swamp, either by their spatial configuration in the form of micro-habitat along a saline gradient or by seasonal variations in the abundance of resources [12].
The Ardeidae family consists of herons and punches and has as remarkable characteristics the long neck and legs; the straight and long beak, higher than wide, almost always pointed and in most cases with the presence of serrations for the capture of fish. The species Ardea alba (white-great-egret) presents greater daytime activity, of solitary habit, as in groups or flocks. It presents a diet composed of fish, invertebrates, reptiles, and amphibians, being predominant the consumption of fish. In foraging for food capture, it moves slowly walking in the water, near the margin to the location of the prey [30]. Ardea alba can form numerous nests, lay two to three blue-grey colored eggs and the incubation period is 25 to 26 days [19,25]. Eudocimus ruber, the guará is a representative of the Threskiornithidae family and is closely related to mangrove environments on the Brazilian coast [47,50]. In Brazil it is distributed in two disjoined populations, one in the North, in the State of Pará and the State of Maranhão [47.15] and another in the South, particularly in the State of São Paulo [48]. The carcinophagous species, such as Eudocimus ruber, are more dependent on marine resources and present a smaller laying size, about two eggs, which indicates an optimizing strategy for resources and the production of offspring [12].
On the island of São Miguel about 1500 reproductively active individuals of Eudocimus ruber were registered in the period from April to June 2015. The first study on the guará colonies was carried out between the mouth of the Orinoco and the Amazon, on the Amapá coast [50]. Later research in Viseu-PA [43] and on Cajual-Maranhão island [41] recorded the presence of nests of this species. In the State of Santa Catarina, after decades of absence, there were reports of the presence of reproductive activity in late 2012 [14].
The guarás were mostly observed sharing foraging and dormitory sites with other species. The sharing of feeding areas is known for several species of estuarine birds, and there is a general pattern of distribution for each one at the

Fig.3: Eudocimus ruber (guará).
The genus Cathartes covers the necrophagous birds of the New World Vulture family (Cathartidae). There are three species classified in this genus. All species have featherless heads with bright colored skin (yellow or orange on the yellow-headed vulture, and bright red on the red-headed vulture). Cathartes aura has been frequently recorded in mangrove swamps, this species also occurs in forests, open lands, farms and on roadsides, captures small vertebrates on shallow flights and steals eggs from herons in nests. It sleeps in large flocks on dry trees and feeds on carcasses and, thanks to its keen sense of smell, is usually the first of vultures to find them. It also feeds on locusts and small fish; it appreciates fruits such as avocado and palm coconuts and stirs up fresh cattle manure for food.
The Alcedinidae family has a wide geographic distribution, occurring in tropical and subtropical zones, near aquatic environments [47]. Kingfishers are characterized as birds with colorful and bright plumage, robust body, relatively large head, short neck, short tongue, long beak, robust and pointed. The species Megaceryle torquata, also known as martim-pescador-grande or ariramba is the largest representative of this family, measures approximately 42 centimeters and weighs from 305 to 341 grams. This species was recorded more frequently in the rainy season, in this period there is an increase in soil humidity, which facilitates the construction of the nests, in addition to the increase in food supply. Another species recorded was Chloroceryle inda, , martimpescador-da-mata, this species feeds on fish, batrachios and crabs that it catches by diving from low perches in the mangrove vegetation near the water. Passeriforme birds are often cited in lists of bird species associated with mangroves [35,36,24,46,03]. In a study carried out in mangroves in the eastern State of Pará, the authors registered nine species of Passeriforme birds, which represented 50% of the inventoried species [35], while in another study 12 species were registered in mangrove areas in the island of Canela, Bragança, Pará [46]. In the island of São Miguel in the Municipality of São Caetano de Odivelas, the number of species belonging to the order of Passeriforme birds, was represented by 21 % of the species (n:15), demonstrating that this taxonomic group has an effective association with the mangrove ecosystem and, consequently, should exert some direct influence on the available resources and the dynamics of this ecosystem.
The arapaçus belong to the family Dendrocolaptidae formed by 14 genera, where 43 known species are classified in Brazil. The group is typical of the Neotropical regions of the New World, with distribution from southern Mexico to central Argentina. They are insectivorous birds that feed on insects preferentially crickets, cockroaches, ants, termites and beetles. Occasionally they also consume small amphibians or reptiles and only in conditions of extreme scarcity do they feed on fruits or seeds. The Xiphorhynchus spixii was registered in the study area and its distribution covers the Brazilian Amazon to the south of the Amazon River, extending south to Mato Grosso and east to Maranhão. It is also found in Colombia, Ecuador, Peru and Bolivia. It lives alone or in pairs, often accompanying mixed flocks of birds, and only eventually run ants.
Tyrannidae constitute the largest family of birds in the western hemisphere, where they occur exclusively, distributed from north to south of the American continent, with greater concentration in the Tropical region. This group gathers a wide diversity, totaling 413 species and constituting about 18% of the Passeriforme species in South America. In Brazil they occupy all types of landscape, most of which are arboreal and woodland, feeding essentially on insects and arthropods, but some species are frugivorous, granivorous and carnivorous [48]. The pyprids are fruit-eating species of understorey, present in general wide geographic distributions and high population densities, being found in the Amazon region the greatest richness of species per biome or ecoregion of the neotropics [01]. This family stands out for presenting a mating system in fans, in which males are grouped in places or traditional fans to execute cooperative exhibitions. The female of Manacus manacus (lace maker) was registered, a relatively small bird (15 -18 g) with a diet composed predominantly of fruits. They play an important role in seed dispersal, removing them from areas of high population density, near the mother-plant and places of intense predation by insects and mammals receiving in return nutritional content, play an important role as vectors in seed dispersal in the Neotropical region [48]. Representatives of the Thamnophilidae family are distributed in the Neotropical region and reach their greatest diversity in the Amazon basin. Thamnophilus aethiops (flat brook) is also known as xorró, measuring about 16 cm long and weighing 23 g. The male has a general dark grey coloration with the top of the head black and the female is brown with the lower part lighter. His diet is composed of insects and arthropods, including Aranea, Scorpiones, Chilopoda and Isopoda.
For a long time, scientists focused mainly on the conservation of terrestrial ecosystems, because among other reasons their impacts were directly observed. In a silent and less perceptible way, coastal zones, seas and oceans around the world also gradually suffered the effects of the expansion of occupation and anthropic uses. Among the main causes for the loss of coastal biodiversity were loss of habitat, contamination of continental waters by agrochemicals and fertilizers used in agriculture, toxic industrial waste [20] and human waste without treatment or partially treated, capture of fishing resources (fish, mollusks, crustaceans and algae) in quantities greater than their capacity for reproduction and climate change.
The coastal and marine ecosystem is home to a significant variety of living beings, and provides essential services for human survival, such as food, climate maintenance, water purification, flood control and coastal protection. The mangroves, in turn, present high structural and functional diversity, acting, together with the estuaries, as exporters of biomass to the adjacent systems, this system works as a place of refuge, rest, feeding and reproduction of several taxa of marine and terrestrial life, including birds.

IV. CONCLUSION
The Neotropical region of mangrove on the island of São Miguel, found along the coast of São Caetano de Odivelas -Pará, presents a high diversity of endemic, resident, migratory birds, and other seasonal visitors. Thus, it is necessary to expand the knowledge about the composition and richness of the bird species, in order to contribute to local ecological studies and migratory groups. According to the methodology used, it could be concluded that there were several bird species registered in the region, being those belonging to the Brazilian or migratory bird species, such as those of the Scolopacidae family. Thus, the maintenance of the mangrove swamp on the island of São Miguel is fundamental as a way to conserve these species, since it serves as habitat, resting point, and feeding point for birds, especially those that cross great geographical barriers during their displacement.