Observations on Indian Skimmer Rynchops albicollis Swainson, 1838 (Aves: Charadriiformes: Laridae) breeding colonies in Middle Ganges stretch, India

: Indian Skimmer Rynchops albicollis Swainson, 1838 is a riverine habitat specialist bird and a species of significant conservation concern. In 2020 it was up-listed to the ‘Endangered’ category of the IUCN Red List. Breeding grounds of the species are known from the major rivers of India like Ganga, Chambal, Son, and Mahanadi. We monitored breeding colonies of the species in two breeding seasons (2017 and 2018) in the middle Ganges stretch. We identified nine nesting islands and monitored a total of 111 active nests during the study period. A total of 302 eggs were counted with clutch sizes ranging 1–5 and the mean clutch size of 2.7 (±1.18 SD). We observed a 10% & 7% of hatching and fledgling success rate in 2017 and 10% & 17% in 2018, respectively. Low breeding success was probably due to the severe anthropogenic factors such as egg collection, cattle trampling, and stochastic weather events such as flooding and sand inundation by sand storms in nests. We also recorded instances of nest abandoning because of unknown reasons. This article recommends more surveys to identify new breeding colonies of Indian Skimmer in the middle Ganges and subsequently provide adequate protection to the colonies. We also recommend sensitization programs for different stakeholders to create more awareness for the conservation of this threatened species in the middle Ganges stretch.


INTRODUCTION
The Skimmers are a group of birds that belong to the genus Rynchops of the family Laridae (BirdLife International 2023).They are known for their uneven bill for foraging on the fishes, insects, and shrimps through skimming on the water surface (Zusi 1996;Martin et al. 2007).Globally, three members of Rynchops genus are known-the African Skimmer Rynchops flavirostris, the Black Skimmer Rynchops niger, and the Indian Skimmer Rynchops albicollis (Bhushan 2018).Among them, the Indian Skimmers are globally threatened riverine birds native to southern and southeastern Asia.They have been recently up-listed to the 'Endangered' category of the IUCN Red List because of the declining population trend (Birdlife international 2023).Indian Skimmers are medium, tern-size birds of 40-43 cm in length with a wingspan of around 108 cm (Grimmett et al. 2016;Shaikh et al. 2018).The adults have a drooping orangered bill with lower mandible projecting beyond the upper mandible (Ali & Ripley 1987).It has a black cap and mantle, and wings contrasting with white underparts (Grimmett et al. 2016).In 2001, the adult population was estimated to be 4,000-6,700 individuals.However, with the recent assessment in 2020, the population estimate of the Indian Skimmer is 2,450-2,900 mature individuals.It is estimated to be 41% decline of the population from 2001 to 2020 (Birdlife International 2023).
Historically, the population was distributed in the major river systems of Myanmar, Cambodia, Vietnam, and the Mekong delta (Sundar 2004).However, the current distribution of the species is believed to be from Pakistan and Nepal, with the stronghold of the population in India and Bangladesh (Rajguru 2017;Debata et al. 2019).In India, the breeding population of the species is known from the major rivers like Chambal, Mahanadi, Ganges, and Son (BirdLife International 2023).However, in recent years non-breeding population are also recorded from the peninsular India, east and west coast, and other wetlands (Gopi & Pandav 2007;Malla et al. 2015;Shaikh et al. 2021).There are also records of wintering and breeding grounds of the species from Bangladesh (Mohsanin 2014;Kabir et al. 2016;Chowdhury et al. 2020;Das et al. 2020).The known breeding grounds of the species reported from India are National Chambal Sanctuary on river Chambal in the state of Uttar Pradesh, Rajasthan and Madhya Pradesh (Sundar 2004;Das 2015;Shaikh et al. 2018;Singh & Sharma 2018), Narora Ramsar Site on river Ganges in Uttar Pradesh (Siddiqui et al. 2007), Son Gharial Wildlife Sanctuary on river Son in Madhya Pradesh (Dilawar & Sharma 2016), and Pong Dam Wildlife Sanctuary in Himachal Pradesh (Fernandes & Besten 2013).However, new breeding records have been reported in the last five years from the middle Ganges stretch (Ankit et al. 2018;Mital et al. 2019) and Mahanadi (Rajguru et al 2017;Debata et al. 2018).The breeding season starts after the winters ranging from February to May in different breeding sites.Indian Skimmers breed in colonies and sometimes with other species like River Tern Sterna aurantia, Little Tern Sternula albifrons, River Lapwing Vanellus duvaucelii, and Small Pratincoles Glareola lactea (Rahmani 2012;Rajguru 2017;Ankit et al. 2018;Debata et al. 2019).Generally, Indian Skimmers lay eggs in sandy spits of emerged river islands; the clutch size ranges between 1-5, and both the sexes are involved in incubation and parental care after the hatching of eggs (Shaikh et al. 2018;Debata et al. 2019).
Habitat degradation due to several anthropogenic disturbances resulting in low reproductive success is considered a major cause for the rapid population decline.Also, there are records of stochastic weather events causing nest failure of the species at different breeding sites (Shaikh et al. 2018;Debata 2019).However, the essential information pertaining to the breeding biology, threats to the breeding colonies, and long-term population monitoring are still very limited across its breeding ranges (Rajguru 2017;Debata et al. 2019;Shaikh et al. 2018).After the discovery of new breeding colonies in the middle Ganges stretch in the year 2017, we investigated different aspects of the breeding biology of Indian Skimmer.We also identified threats to the breeding colonies in the middle Ganges stretch by monitoring two breeding seasons, which is far apart from the earlier known breeding grounds of other riverine system.

Study Area
This study was carried out in the Prayagraj District (25.4727 0 N, 81.8783 0 E) of Uttar Pradesh (formerly Allahabad) (Image 1).The district is known for the confluence of two major rivers of India-Ganges and Yamuna-and the invisible Saraswati.The river Ganges has been divided into three courses-Upper (stretch in mountainous regions of the Himalaya), Middle (stretch of floodplains), and Lower Ganges (stretch after the confluence of major river till it meets the Bay of Bengal) due to its characteristics such as flow, channel width, depth and sedimentation.settings.The Prayagraj J TT district is adjacent to middle Ganges stretch.Prayagraj experiences three prominent seasons, summer (March-June), monsoon (July-September), and winter (October-February).The average maximum temperature ranges 23°-41°C with 1,027 mm annual rainfall.The district is famous for 'Kumbh Mela' at the confluence point which is known for world's largest human congregation due to traditional beliefs.Additionally, the area also witnesses human gathering round the year due to religious practices, annual 'Magh Mela' during the winter is one of the examples.The Ganges in Prayagraj is also one of the polluted stretches because of several anthropogenic activities, including the effluent discharges from the leather industries of Kanpur city, which is located on the upstream of the river.However, the area supports good biodiversity of riverine species like the Gangetic Dolphin Platanista gangetica, Gharial Gavialis gangeticus, Marsh Crocodile Crocodylus palustris, different species of turtles, fishes, and wetland birds like the River Tern Sterna aurantia, Little Tern Sternula albifrons, River Lapwing Vanellus duvacellii, Small Pratincoles Glareola lactea, and Ruddy Shelduck Tadorna ferruginea.The dry and hot summer causing low water levels exposes sandbars and river islands, which facilitates breeding riverine birds like Little Tern, River Lapwing, and Indian Skimmer.As a part of an ongoing project on waterbirds, after a few sightings of Indian Skimmer in the confluence area in January 2017, we extensively surveyed a total of 75 km of riverine stretches in Prayagraj district (25 km stretch each upstream and downstream of the river Ganges and 25 km upstream of the Yamuna from the confluence) in January to June in both the year of 2017 and 2018.The banks of the rivers were mostly sandy with intermittent mudflats, cultivations and settlements.There were also exposed river islands mostly in the river upstream of Ganges (from the confluence) due to low water depth.

Observations on nesting birds
The survey method included trail walking along the banks and opportunistic surveys through mechanised boat from February to June.After observing the events of the courtship display and congregation of birds, we considered the river islands as the nesting island of the

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J TT birds.After 3-4 days, we visited the islands to record any breeding activity such as nest preparation.After getting ensured the sign of nest preparation, we considered it as nesting island.we started regular monitoring the nesting islands in the morning (0600-0800 h) or evening time (1600-1800 h) from the river bank using Bushnell 8 × 42 binocular.Only after observing signs of incubation, we visited the nesting islands using a non-motor boat, ensuring minimal disturbance to the breeding birds.Further, we started regularly visiting the nesting island in the morning (0600-0800 h) or evening (1600-1800 hs).Two observers visited the islands and separately recorded the number of individuals, nests, clutch sizes, hatchlings, nest failures, and anthropogenic disturbances.The observer's entry and exit times to the nesting island were fixed.One observer was followed by the second observer in the multiple straight lines with inter-distance of 1.8-2.4m (n = 8-18 depending on the size of the nesting island).The double observer method ensured the confirmed identification of the nests, and presence of new active nests.Since, most of the islands were having fewer active nests, the double observer method minimised the possibility of double counting or missing of active nests.
We ensured that the observation took minimum possible time while collecting the data, which were around 5-10 min depending on the number of nests and island size.We did not use any invasive techniques to mark the nest or the eggs, and during the observation, precautions were made to minimize the disturbance to the birds.We consciously walked on the islands to minimize the footprints on the island.Same survey and monitoring protocols were used in both the years of the breeding cycle.Successful nest was considered with the minimum one egg hatched in a particular nest and hatching success percentage was calculated as the proportion of number of successful nest and number of nests (Debata et al. 2019).Whereas, the fledgling success was calculated as the proportion of nest with fledglings and number of successful nests.We also analyzed the clutch size the percentage of the nest failure because of the different factors.

Sightings, abundance, and breeding phenology
Sightings of Indian Skimmers were continuous from January to March 2017 & 2018, mostly on flights or during foraging.We recorded the first congregation of the birds on a river island in late March 2017 and early April 2018.Subsequently, we recorded seven and two nesting islands in 2017 and 2018, respectively (Image 1).A total of 356 (n = 232 in 2017, n = 144 in 2018) individuals of Indian Skimmers were observed in the different nesting islands.The sporadic sightings of the birds during the surveys are excluded from the total count.Courtship display, mating, and nest preparation continued between late March and April in both years.However, mating events and nest preparedness were also observed in May and the first week of June 2017 in some nesting islands.In 2017 season, the first clutch was noticed during the first week of April.However, we located nesting in the second week of April in the year 2018.The first hatching of eggs in the nests was observed during mid-May in 2017 and late April 2018 (presuming the first clutch of the season in the last week of March).In 2017, the hatching of eggs was also observed till June in a couple of nesting islands.In May and early June, we observed the dispersal of fledglings from the nesting islands.Both the mating partners were involved in parental care and nest guarding during the breeding cycle.

Active nests and clutch size variation
All the nine nesting islands were approximately in the range of 15 km upstream of river Ganges from the confluence point.We recorded 111 active nests of Indian Skimmers (n = 73 in 2017 and n = 38 in 2018) and these active nests were the shallow depressions in sands, mostly away from the edges of the river islands (Table 1).A total of 302 eggs were laid by the species in the study area (n = 186 in 2017 and n = 116 in 2018) (Table 1).The clutch size varied between 1-4 and 1-5 in different nesting islands of 2017 and 2018 observations, respectively.The mean clutch size was 2.54 (SD ± 1.11) and 3.05 (SD ± 1.27) in the years 2017 and 2018, respectively.We also recorded the active nests and fledglings of River Lapwing, Little Tern, Small Pratincole, and Black-winged Stilt on the nesting islands of Indian Skimmer.

Breeding Success and possible causes of nest failure
Out of all the nine nesting islands in 2017 and 2018, nesting failure was observed in three islands due to anthropogenic and natural causes in the year 2017.The remaining six nesting islands recorded hatching (n = 4 in 2017 and n = 2 in 2018).Among all the monitored active nests, only 10% and 11% of the nest successfully produced chicks in 2017 and 2018 respectively whereas, 10% and 7% survived up to fledgling stage with respect to the number of nests in the year 2017 and 2018,

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respectively.The main causes of the nest failure were anthropogenic pressure such as cattle trampling, egg collection, and natural causes include predation, flooding, and sand inundation (Table 2).

DISCUSSION
Long-term ecological monitoring is an essential tool for the conservation of any species.It provides basic ecological information of the targeted species and its associated community in lieu of different environmental conditions.It gradually helps in identifying key conservation priorities and monitoring the effect of change in policy and environment (Havstad & Herrick 2003;Giron-Nava et al. 2017).However, long-term ecological monitoring of the waterbirds and their associated habitats is limited in India (Prasad et al. 2002;Kar et al. 2018;Singh & Sharma 2018;Debata et al. 2019).The riverine systems of India facilitate the occurrence of river-dependent birds by providing shelter, forage, and breeding grounds (Islam & Rahmani 2008;Rajguru 2017;Sinha et al. 2019).Many species of birds are known to utilize the river and its associated habitats to complete partial or entire lifecycles (Page & Gill 1994;Vaughan et al. 2007;Froneman et al. 2011;Rahmani 2012).Additionally, the riverine system has an intricate relationship with humans, which sometimes causes overexploitation and habitat degradation, and can adversely impact the populations of species like the Indian Skimmer and the Black-bellied Tern Sterna acuticauda (Kar et al. 2018;Kar & Debata 2019).In our study area, we observed multiple pressures on the river system, which negatively impacts the breeding cycle of Indian Skimmer and may severely affect the species at the population level on a long run.

Population and breeding in the middle Ganges stretch
There were previous sighting and breeding records (Narora-Ramsar Site) of Indian Skimmers from the river Ganges (Siddiqui et al. 2007).The recent breeding records from the middle Ganges stretch is from Prayagraj (Ankit et al. 2018) (Image 2) and Varanasi (Mital et al. 2019).This study and previous records suggest the congregations of the birds in December and January in the middle Ganges stretch (Shukla 2016).Both the years 2017 and 2018, we observed the congregation of more than 100 Indian Skimmers in different Islands.However, the nesting islands were relatively less with respect to the total number of individuals sighted.There may be a possibility that most of the birds used these islands as a stopover site.There was a difference between the nesting islands in the years 2017 and 2018, we presume that after a couple of nest failures these individuals laid their second clutch in our study area hence, we located more breeding colonies in 2017.The records of only two breeding islands in 2018 led to the speculation that there would have been more nesting colonies in the upstream of the Ganges beyond our study area because of the observance of higher number of individuals in one of the nesting islands.These individuals might have shifted to the upstream for breeding as there are observations on breeding Skimmers in upstream of Allahabad recorded by Survey teams of Wildlife Institute of India in Bulandshahr and Farrukhabad districts in between the year 2017 and 2021.The breeding period  Poor breeding success and threats to the breeding colonies Prayagraj is one of the densely human-populated cities of the Northern-India; hence it poses severe anthropogenic pressure to riverine stretches adjacent to the city.All the nesting islands were in close proximity to the periphery of the city, which has caused the enabling of multiple threats to the breeding colonies.The main reason for the nest failure was due to the anthropogenic pressures followed by the stochastic events that caused low breeding success in the study area (Image 3).Similar threats have also been identified at different breeding sites (Siddiqui et al. 2007;Debata et al. 2018;Shaikh et al. 2018;Mital et al. 2019).The breeding success is very low when compared to the similar study of Debata et al. (2019) in the Mahanadi River in the same breeding season.It highlights the magnitude of anthropogenic pressure on the middle Ganges which may be negatively impacting other riverine species too.
Multiple anthropogenic threats were identified that had directly impacted the breeding colonies, such as cattle trampling.It was observed that because of low water depth, cattle use these islands as passage to go from one bank to other for foraging.Additionally, they venture in to the river islands to forage on vegetation growth.We also observed egg collection by the locals.However, no information on consumption or commercial use was available.There are indirect threats such as disturbances because of agricultural activities in the bank of the river and on river islands.The locals grow seasonal crop such as watermelon, pumpkin, and other cucurbitaceous crops of the gourd family on the sandy area of banks and river islands.We haven't recorded any agriculture on the nesting islands but we observed agriculture activity on the nearby banks.Additionally, free-ranging dogs, and boat activity, which may have led to the abandoning of the nests by the breeding pairs.
After the nesting failure in multiple nesting islands due to anthropogenic activities in 2017, we availed help from the forest department and Prayagraj administration for ensuring the protection of the nesting islands through awareness in adjoining villages for farmers working in the adjacent field.Forest officials were deployed in the daytime as nest guardians (near the bank) to minimize the anthropogenic disturbance.
No casualty was reported in the breeding island during the night and all the chicks fledged during this phase resulting in no nest failure at the chick stage in the year 2017.In the year 2018, the nest failure and egg J TT collection didn't happen probably due to the awareness created among the villagers in and around the nesting islands by the forest department team immediately after the locations were informed to the Forest department.Forest officials were deployed again in the daytime as nest guardians (near the bank) to minimize any sort of anthropogenic disturbance.However, after sunset, we recorded the event of cattle trampling in nesting islands which resulted some casualties on eggs and chick stages.The impact of pollution and prey availability due to fishing was not quantified in this study.This could have been the major cause of abandoning the nesting islands because of low food resources; hence, it needs investigation in the future.However, we observed disturbances to the breeding birds on the nesting islands due to fishing activity of human and boat in the proximity of the nesting islands.There were no instances of river bed material collection observed like in other breeding sites (Shaikh et al. 2018;Debata et al. 2019).However, erosion of non-nesting islands was observed because of increased water current and depth due to both natural and manmade factors, natural factors include unseasonal rainfall and manmade factors include water flow regulation from the upstream of Kanpur barrage for irrigation.However, we don't have data regarding the causes of water flow and water level fluctuation in the study area.

Conservation actions required
The basic ecological knowledge of breeding biology, diet, and movement during the non-breeding period of Indian skimmers is inadequate from all the breeding locations.However, it is notable that emphasis has been given by the scientific community on breeding and non-breeding sites of the species through continuous monitoring on different ecological aspects (Kabir et al. 2016;Rajguru 2017;Shaikh et al. 2018;Debata et al. 2019;Chowdhury et al. 2020).Recently observation has been also made in other rivers like Gomti in Ganga Basin (Chauhan 2023).The continuous monitoring and exploration in the potential breeding areas will unearth more information pertaining to the species for conservation.
The middle Ganges stretch is in lieu of several disturbances around the year.Hence, it becomes crucial to identify the breeding colonies in this particular stretch through continuous surveys and expeditions.Subsequently, nest protection should be provided to the breeding colonies through nest guarding and minimizing the anthropogenic pressure especially fishing during the nesting season.The 'nest guardian' program for protecting Indian skimmer nesting colonies is already in practice in National Chambal Sanctuary (Mishra & Tandon 2021), which can be replicated in the middle Ganges stretch.Sensitization of different stakeholders J TT through awareness drives, workshops, and community participation can also help in the protection of the nest and nesting islands during the season.Convincing locals and farmers not to do agriculture on river islands can also provide more availability of nesting islands for the Indian Skimmer and other riverine birds during peak breeding periods.
The glimmer of hope is that surveys have been conducted at regular intervals under the objective of biodiversity conservation of National Mission for Clean Ganga program in the past few years.It has helped in the identification of breeding locations of Indian Skimmers along the Ganges.Additionally, community participation programs such as 'Ganga Prahari' under the same project to involve the locals in biodiversity conservation of the river Ganges.However, with all these efforts it is necessary to protect breeding colonies of endangered Indian skimmer in the future which may subsequently help in increasing the population of the species and its survival.The record of the breeding colony from Prayagraj and Varanasi are promising findings that warrant further exploration surveys for more breeding colonies in the future.
and May, similar to the observation made at different breeding sites(Dilawar & Sharma 2016;Rajguru 2017;Shaikh et al. 2018;Debata et al. 2019).Across the two monitoring years, no nesting islands were observed in the Yamuna stretch, possibly because of the unavailability of river islands as the river Yamuna which had high water levels during both the surveyed years.However, there are recent nesting records have been observed in Yamuna in Prayagraj District(Mani 2023)

Image 2 .
Series of events recorded for Indian Skimmers in Prayagraj: a-occasional sightings | b-congregation in river islands | c-courtship display | d-mating events | e-laying and incubation of eggs | f-hatching of eggs.© Kumar Ankit.

Image 3 .
Direct and indirect threats observed on the breeding colonies of Indian Skimmer a-Disturbance because of cattle and human | b-Island erosion | c-Disturbance because of free-ranging dogs | d-predation on the eggs by house-crow | e-chick mortality because of cattle trampling | f-inundation of sand in the nest because of rain and wind.© Kumar Ankit.