Diversity and distribution of birds in the Bharathapuzha River Basin, Kerala, India

: Bharathapuzha River is the second largest, west-flowing river in Kerala, Western Ghats. This river is exposed to high levels of anthropogenic and natural pressures. This study attempts to understand the diversity and distribution of birds in this river basin. The observations were made from October 2017 to July 2019 in 70*1 km 2 grids distributed in three strata (i


INTRODUCTION
Rivers are considered an important ecological entity that supports rich biodiversity.The water flow, geography, interaction between the terrestrial and aquatic ecosystems, and the dynamic nature make the rivers one of Earth's most complex biophysical systems (Naiman et al. 1993).Though the rivers harbour rich biodiversity, they are also prone to many natural and anthropogenic challenges.Therefore, understanding the biological communities of the river system is essential for its management and conservation prioritization.The diverse habitats on the river corridors support many birds (Stevens et al. 1977;Stauffer & Best 1980;Knopf 1985).Since birds are considered as ecological indicators, habitat quality can be assessed through long-term avifauna monitoring.Understanding the bird communities and habitat association of different species (including migratory species) in different seasons is important for planning conservation strategies (Rice et al. 1980;Naiman et al. 1993;Gergel et al. 2002).
Kerala is one of the important places for avian research.The high level of habitat heterogeneity and its mosaic nature supports a wide range of birds (Neelakantan 1969(Neelakantan , 1970(Neelakantan , 1981(Neelakantan , 1982;;Neelakantan & Sureshkumar 1980;Neelakantan et al. 1980;Ali & Ripley 1983;Pramod 1995).The wetlands in Kerala enhance avian diversity by hosting migratory birds, hence many of the larger wetlands in Kerala were announced as Ramsar sites (Jayson 2002;Nameer 2005) Bharathapuzha River (10.416-11.25 N and 75.833-76.916 E) in Kerala is known for its cultural and ecological significance.This river is considered as the cradle of civilization in Kerala.The major portion of the Bharathapuzha River flows through a human-dominated and agricultural landscape.The diverse habitat in the fluvial channel of the river supports great bird diversity.Many researchers have attempted to document the bird diversity in the river basin (Namassivayam & Venugopal 1989;Namassivayam et al. 1989;Kurup 1991;Uthaman & Namassivayam 1991;Neelakantan et al. 1993;Pramod 1995;Kurup 1996;Bijukumar 2006;Arif et al. 2010).However, the information available about the bird diversity of this river basin is sporadic.In this investigation, we considered the river basin as a single ecological entity.We employed a ridge-to-reef approach to document the bird diversity from headwaters, main tributaries, mainstream and estuary.This study aims to establish baseline information about the avifauna of the Bharathapuzha River Basin and as a potential survey design for other river basins.

Study area
The river Bharathapuzha originates from the southern part of the Palakkad Gap, in the Anamalai hills in the state of Tamil Nadu.It flows through the Palakkad gap covering Pollachi in Tamil Nadu; Palakkad, Thrissur, and Malappuram districts in Kerala and debouches into the Arabian Sea at Ponnani on the Malabar coast.The total length of the river is 250 km, of which 209 km flows through Kerala and 41 km through Tamil Nadu (Figure 1).The total extent of the river drainage basin is 6,186 km 2 between an elevation gradient of 2,461-0 m with an annual discharge of 3.94 km 3 water.The study divided the river drainage basin into three different ecological zones based on the stream orders as per Strahler (1957).Streams of order one to three were denoted as upper reaches (Image 1), order four to five as middle reaches (Image 2) and sixth-order streams were denoted as lower reaches (Image 3) (Abel et al. 2008).
The major tributaries of the river are Chiturpuzha, Gayathripuzha, Kunthipuzha, and Kalpathipuzha.All these tributaries originate from the northern and southern tips of the Palakkad Gap, which are the permanent and important water sources for the river.There are 11 dams constructed on this river for drinking water supply and irrigation to serve millions of people in the region.

Study design
The hydrology layer for the river basin was extracted using ASTER GDEM V2 and stream orders were established using the Strahler (1957) method.Field surveys were conducted along 453 km stretches at these ecological zones (Figure 1).These stretches were divided into 70 grid cells of 1 X 1 km.These selected locations were sampled from October 2017 to July 2019 in three replications which include two migratory (November-March) and one non-migratory season (April-October).In each cell bird observations were made for a 15 min period using point count with the fixed-width method (Reynolds et al. 1980).A total of 840 point counts were conducted in the sampling area.Over-flying birds, bird detections >50 m, and uncertain bird identifications were truncated from the data to improve the robustness of the study.Direct and indirect signs of birds were observed at 0600-1100 h and 1530-1900 h in each location.Direct observations were made using binoculars and spotting scopes.Bird identification was done using field guides (Ali & Ripley 1983;Ali 1999;Grimmett et al. 1999;Kazmierczak 2000) and photographs.The bird checklist was prepared using Praveen et al. (2020).

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Opportunistic bird observations, i.e., the birds observed in the study areas after the predesigned observation period were recorded as ad libitum.The time of observation, date and number of individuals sighted, and habitat were noted.
Data analysis: Bird abundance data was arranged in the species vs sites contingency table.Absolute species richness for each region was tabulated.To check sampling adequacy, species richness was also estimated using Chao 1 ™index.To compare diversity, dominance and evenness Shannon-Weiner (H') and Simpson index were estimated  (Magurran 1988).Relative abundance for all species was calculated in each ecological zone (Sutherland et al. 2004) using the formula.
Where RA = relative abundance of species i, Ni = Abundance of species i in ecological zone, P = Population of all species in river basin.
Relative abundance was calculated with the whole population of birds in the river basin to make it comparable J TT between ecological zones.The relative frequency of occurrence (RF) of birds in grids was used to understand the commonality/rarity of birds in each ecological zone.Hence the birds with RF more than 50% are considered as common, 20% to 50% as less common and >20% as rare.
To understand the migratory species of birds, bird species observed were classified into three categories such as resident, local migrant or long-distance migrant (SoIB 2023).To assess species distribution patterns, rank abundance distribution patterns were examined.All statistical analyses were performed using R statistical language V4.3.0 with R Studio IDE for R V2023.03.01.Diversity indices and rank abundance distributions were estimated using 'vegan': Community Ecology Package 2.6-4 (Oksanen et al. 2013).

Diversity
The bird observations were conducted from 0ctober 2017 to July 2019.A total of 262 species of birds were recorded belonging to 20 orders and 71 families (Table 1).Out of 262 bird species recorded in the study area 235 species of birds were recorded while employing the bird survey method; 27 bird species were observed in the opportunistic observations.Ecological zonewise sampling efforts, bird species observed and the number of individual birds sighted are shown in Table 2.A total of 36,811 individuals were recorded from the river basin in migratory (n = 27,242) and non-migratory (n = 9,569) seasons during the survey.Passeriformes were the most dominant group in the river basin (42%) followed by Charadriiformes (13%), Falconiformes (8%), and Ciconiformes (6%).Passerine birds were the most dominant group (N = 146) followed by waders (N = 33), raptors (N = 20), and shorebirds (N = 19).Absolute species richness and estimated species richness using Chao-1 was similar (Table 3) indicating sampling was adequate.While the Shannon-Weiner index (H') shows higher species diversity in upper reaches (Table 3) than in middle and lower reaches.However, Simpsons' index for evenness and dominance was found to be similar across all ecological zones.

Bird species occurrence in different ecological zones
Rare birds were more compared to common and less common birds in all ecological zones.The upper reaches of the river basin reported 45 species of resident, two species of local migrants and four species of long-distance migrant birds as common, while 91 residents, 10 local migrants and eight long-distance migrants were rare.In the middle reaches, 43 residents, two species of local migrants and one species of long-distance migrant birds were common.58 residents, six local migrants and three long-distance migrants were rare.In lower reaches, 48 residents, two local migrants and five migrant species were common and 48 residents, two local migrants and 10 migrant species were rare (Table 4).
Zipf-Mandlebrot distribution was found to be the best-fit model for upper reaches (deviance = 401.60)and lower reaches (deviance = 465.40).However, bird species in the middle reaches followed a log-normal abundance distribution (deviance = 615.83)(Table 5).Lower reaches had a steeper distribution than upper reaches and middle reaches indicating a high species turnover rate.While upper and lower reaches show shallow slopes, Middle reaches have more even abundances with species ranked with log-normal distribution.The study identified 60 species that are specific to the upper reaches, four to middle reaches and 16 to the lower reaches.119 birds were common to all regions (Figure 2).Out of these, 17 birds were endemic to Western Ghats including one 'Endangered', seven 'Near Threatened', and four 'Vulnerable' birds as per the IUCN Red List of Threatened Species.This indicates that productive and heterogeneous habitats of the Bharathapuzha River Basin support birds from different niches and foraging guilds from forest to wetland-dependent birds as well as synanthropic species.

DISCUSSION
Upper reaches show higher species richness than middle and lower reaches because of the presence of primary forests, human habitations, and dams.Hence this region supports different foraging and feeding guilds (Ali & Ripley 1983;Wiens 1989).Also, the presence of dams in the upper reaches and the presence of estuary and check dams in the lower reaches enables to host a large number of migratory birds such as Little-ringed Plover Charadrius dubius, Marsh Sandpiper Tringa stagnatilis and Barn Swallows Hirundo rustica.However, due to the lesser availability of the wintering grounds in the middle reaches, fewer migratory birds were observed.
Ziph-Mandlebrot distribution of rank abundances in upper reaches and lower reaches has steep concave slope indicating that few species occur in high abundances (Figure 3).Species with high abundance ranks in these regions are migratory species like Black-headed Gull Chroicocephalus ridibundus and Pallas's Gull Ichthyaetus ichthyaetus with flock sizes of <5,000 individuals which dwarf the abundances of resident species.However, in the middle reaches, flock sizes of migratory birds are smaller which shows a more even distribution of rank abundances.

Status of migratory birds in the Bharathapuzha River
Purathur in the Bharathapuzha River basin was identified as one of the major stop-over sites for many migratory birds (Kurup 1991;Kumar 2001).Large flocks of Black-headed Gull, Pallas's Gull, & Brown-headed Gull (<5,000), Whiskered Tern (<100), and resident egrets such as Cattle Egret and Little Egret (<100) were recorded from the Purathur region during the study period.Smaller migratory bird flocks of Little-ringed Plover and Common Sandpipers were reported from the dams and several other parts of the main course.Solitary and passage migrant birds such as the Amur Falcon were reported from the headwater region.There were consecutive sightings of these passage migrants in the river basin from 2017 (Malampuzha Dam), 2018 (Thirunavaya), and 2019 (Malampuzha Dam).This indicates the importance of the river Bharathapuzha and associated habitats for the conservation of migratory and resident birds.

Major Threats
During the study period, natural vegetation near the sampling locations in upper reaches was cleared for expansion of agriculture especially for cash crops like rubber, teak, coffee and coconut.Such deforestation activities for the construction of dams, human settlements and infrastructure development were also reported in various studies (Nossiter 1982;Eapen 1999;Kumar 2005;John et al. 2019).

Passeriformes: Pellorneidae
Puff-throated Babbler Pellorneum ruficeps LC 0.04 (16) @ 0.00 (0) 0.00 (0)     illegal sand mining altered the river ecosystem, especially in the mainstream.The illegal sand mining and overexploitation of sand destroyed the river ecosystem (Sreedhar & Irfan 2016).There were several sighting reports and nesting records of 'Endangered' Black-bellied Tern in the river basin (Susanthkumar 2004;Aarif et al. 2010).However, in this study, we couldn't find nesting of these birds in the river basin.Sand mining is still prevalent in the lower reaches of the Bharathapuzha River Basin.
It can be detrimental to the benthic ecosystem on which many bird species are dependent.Hence sand mining may have cascading effects on the biodiversity of the entire river basin.
Due to the strong opposition by the local people, nature enthusiasts and NGOs, there have been various regulations and restrictions imposed on sand mining activities.Even though, illegal sand mining is prevalent in several locations in the river basin.Interestingly, legal sand mining in the estuary region, at Ponnani is also observed (Image 4).

CONCLUSION
The study covered 48% of the total bird species recorded from Kerala (Chandran et al. 2020).The last published checklist of birds of the region by Bijukumar (2006) has reported 143 bird species from the river basin.This study updates the checklist and increases the number of bird species on the list to 262.
The holistic approach of the river as a single ecological entity helps to understand the changes in the avian diversity in different regions of the river over time.The headwater region of the river basin supports the resident birds.The main course and estuary regions play a pivotal role in the conservation of migratory birds.Hence protection of the forests in the upper reaches and all-natural habitats in the lower reaches are equally important for the conservation of birds.Bringing back the natural ecosystem of the river is everyone's responsibility.Hence community-mediated policy interventions are very much required to reduce sand mining and rebuild the riverine ecosystem, which ultimately protects the biodiversity.
Diversity and distribution of birds in the Bharathapuzha River Basin, India Raj et al.

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Figure 1 .
Figure 1.Location map of Bharathapuzha River Basin showing streams and sampling locations.
Being a human-dominated landscape, some synanthropic birds such as the Common Myna Acridotheres tristis, House Crow Corvus splendens, and Black Drongo Dicrurus macrocercus, were dominant in the three ecological zones of the river basin region.However, Purple-rumped Sunbird Leptocoma zeylonica, Red-vented Bulbul Pycnonotus cafer, Common Tailorbird Orthotomus sutorius, Asian Palm Swift Cypsiurus balasiensis, Yellowbilled Babbler Turdoides affinis, and White-cheeked Barbet Psilopogon viridis were the other common resident birds in the river basin.The wetland associated birds such as Cattle Egret Bubulcus ibis, Little CormorantJ TT Microcarbo niger, Indian Pond Heron Ardeola grayii, and White-throated Kingfisher Halcyon smyrnensis were also found commonly in the river basin.Most of these birds are generalist feeders and adapt themselves to survive in any condition.Black-bellied Tern Sterna acuticauda, Darkfronted Babbler Rhopocichla atriceps, Asian Emerald Dove Chalcophaps indica, Indian Spotted Eagle Clanga hastata, Cinnamon Bittern Ixobrychus cinnamomeus, Striated Heron Butorides striata, Yellow Bittern Ixobrychus sinensis, Spot-billed Pelican Pelecanus philippensis, and Pheasanttailed Jacana Hydrophasianus chirurgus found as rare resident birds in the river basin in which a few of these birds were specific to ecological zones.Greenish Warbler Phylloscopus trochiloides, Grey Wagtail Motacilla cinerea, and Barn Swallow Hirundo rustica were found to be the common local migrant birds in the river basin.Chestnut-tailed Starling Sturnia malabarica, Bar-headed Goose Anser indicus, and Gullbilled Tern Gelochelidon nilotica were the rare local migrant birds.Blyth's Reed Warbler Acrocephalus dumetorum, Common Sandpiper Actitis hypoleucos, and Booted Eagle Hieraaetus pennatus were the common long-distance migrants.Booted Warbler Iduna caligata, Eurasian Curlew Numenius arquata, Whimbrel Numenius phaeopus, and Amur Falcon Falco amurensis were the rare long-distance migrants.Malayan Night-heron Gorsachius melanolophus, Chestnut-winged Cuckoo Clamator coromandus, Blackbellied Tern Sterna acuticauda, and Indian Spotted Eagle Clanga hastata were some of the important sightings during the study period.The maximum flock size is seen in Little Cormorants with <300 individuals in a single location at Walayar dam.Gull species such as Black-headed Gull Chroicocephalus ridibundus and Pallas's Gull Ichthyaetus ichthyaetus congregated highly in the estuarine region.Totally, 2,200 individual birds were encountered in a single grid at Ponnani.

Figure 2 .
Figure 2. Occurrence of various bird species in different ecological zones.

Figure 3 .
Figure 3. Best fit rank abundance model for birds observed in different regions of Bharathapuzha River Basin: 1-Upper reaches | 2-Lower reaches | 3-Middle reaches.