Breeding ecology and causes of nest failure in the Indian Skimmer Rynchops albicollis

ABSTRACT

Capsule: The breeding success of the Indian Skimmer Rynchops albicollis in eastern India is significantly reduced by human activities at the breeding sites.

Aim: To investigate the breeding ecology of Indian Skimmer and factors affecting breeding success along the Mahanadi River in eastern India.

Methods: A total of 230 Indian Skimmer nests were monitored in 2017 and 2018. Population, breeding phenology, clutch size, egg dimensions and factors affecting breeding success rates were determined.

Results: Indian Skimmers arrived at the breeding sites during January–February followed by breeding activities during March–May. On a small scale, nests were more likely to be closer to water and ground vegetation than expected by chance, probably as mitigation against hot afternoon temperatures. Hatching success rate was higher (72.27%) in 2017 and chick survival rate was higher (33.15%) in 2018. Factors that affected breeding success were flooding, nest desertion, egg collecting by humans, predation and trampling.

Conclusion: The breeding success rate of Indian Skimmer could be increased by protecting the breeding sites and minimizing disturbances through community awareness.

The Indian Skimmer Rynchops albicollis is one of the three species of skimmers occurring worldwide and is native to the Asian countries of Bangladesh, India, Myanmar, Nepal, Pakistan and Vietnam. In contrast to its historic range, the bird is now believed to occur only along some large rivers in Pakistan, Nepal, India and Bangladesh with an estimated global population of 4000–6700 mature individuals (BirdLife International 2017). Recent surveys estimate the population in Bangladesh and India at just 1667 individuals (Mundkur et al. 2017). It is thought that the population decline of the Indian Skimmer is directly related to a reduction in their reproductive and foraging success from exploitation and degradation of habitats out of increasing anthropogenic disturbances, irrigation projects and pollution from agricultural and industrial chemicals (BirdLife International 2017). Additionally, the species nests on the ground on sand and shingle banks in, or by, rivers and so fluctuation in water levels in rivers is directly linked with nesting success: an increase in water level washes away the nests and low water levels allow predators and livestock to access breeding sites (Sundar 2004, Siddiqui et al. 2007, Debata et al. 2018). Therefore, owing to a rapidly declining population and the perceived threats, the Indian Skimmer has been categorized as ‘vulnerable’ in the International Union for the Conservation of Nature (IUCN) Red List of Threatened Species (BirdLife International 2017).

In India, although the Indian Skimmer has been reported from different major rivers and lakes throughout the country, it is mostly confined to the north from Punjab through Uttar Pradesh, Madhya Pradesh to West Bengal, extending up to Odisha (Rahmani 2012, Figure 1). Its known Indian breeding sites are in the National Chambal Wildlife Sanctuary (Sundar 2004, Das 2015) and Narora Ramsar site (Siddiqui et al. 2007) in Uttar Pradesh, the Pong Dam Wildlife Sanctuary in Himachal Pradesh (Fernandes & Besten 2013), the Son Gharial Wildlife Sanctuary in Madhya Pradesh (Dilawar & Sharma 2016) and, additionally, it has recently been recorded breeding along the Mahanadi River in Odisha, eastern India (Rajguru 2017, Debata et al. 2018).

Figure 1. Map showing the global distribution (light grey) of Indian Skimmer (from BirdLife International 2017) and the breeding sites along the Mahanadi River in Odisha, eastern India. ID number of the nesting sites refers to Table 1.

Vital information on the population status, breeding phenology, and factors affecting breeding success rate of Indian Skimmers are sparse. In this study, we monitored the breeding ecology of the Indian Skimmer along the Mahanadi River in Odisha, eastern India for two consecutive years and describe aspects of its breeding phenology and factors affecting the breeding success rate. We also recommend a conservation plan for the Indian Skimmer in India and elsewhere.

Methods

Study area

The study area was a 58 km stretch of the Mahanadi River in Odisha, eastern India, situated between 20°22'4.06''N 85°24'0.82''E and 20°25'56.62''N 85°56'2.50''E (Figure 1). The climate of the area is tropical, with three distinct seasons: summer (March–June), monsoon (July–October) and winter (November–February). The annual mean temperature is 26.8°C which varies between a minimum of 12°C during January to a maximum of 42°C during May. With the onset of summer, many temporary sandy islands emerge from the river as the water level drops, and these provide breeding habitat for sandbar nesting birds, such as the Indian Skimmer. The area is an important waterbird site throughout the year (Kar & Debata 2018) but faces several threats. There are three barrages (Mundali, Naraj and Mahanadi barrages) and three canals (Taladanda canal (83.2 km), Puri main canal (40.1 km) and Kendrapara canal (62.7 km)) which have been constructed to control the river water for human use. Around 10 places in the study area are also used for sand mining. Furthermore, 35 villages with a human population of around 150,000 are situated along both sides of the river bank (District Census Handbook 2011) where they largely rely on year-round fishing and agricultural activities for their livelihood.

Data collection

We extensively surveyed all the available islands along the entire length of the Mahanadi River in 2017 and 2018 for Indian Skimmer nesting colonies. Once located, individual nests were identified with a small, well-camouflaged, numbered ground marker at about 1.5 m distance from the nest, following Sathiyaselvam & Balachandran (2007). All the nesting colonies were visited daily during the breeding period, either in the early morning or late afternoon, to monitor marked nests and identify new ones. At each nest, we recorded laying dates of each egg, complete clutch size, failure date of the failed nests and hatching dates of the chicks. The incubation period of the eggs was calculated on the assumption that first laid eggs would also hatch first. All nest monitoring activities were carried out in an ethical way and kept disturbance of the birds to a minimum. Each day we also counted the total number of individual birds throughout the nesting sites.

We considered any nest successful if at least one egg hatched and estimated the apparent hatching success rate as the proportion of successful nests to total number of monitored nests. The daily nest survival probability (S) and cumulative nest survival probability (S^d ) was calculated following Mayfield (1961, 1975) as$S=1\text{–}r$ $S^d=(1\text{–}r{)}^d$where r is the proportion of the total number of nests failed to total number of exposure days of the nests and d is the average incubation period.

We tried to identify the factors responsible for the failure of any nest by examining the nest and its surroundings. Each day while visiting the nests, we erased all nearby footprints of humans or other animals, if present; new footprints could then be used to ascertain the possible cause of nest failure. When the bottom of any nest was wet and/or the eggs were totally or partially submerged, we considered the nest as flooded. When there were human or other footprints near the nest and the nest or eggs were damaged, it was considered to be trampled. When eggs in a nest disappeared prior to hatching, we considered them either collected by local people or predated. Egg collection by humans was identified if the nest was intact but there were human footprints in the vicinity. We also interviewed local people about the collection of eggs. Eggs were considered to be predated when the nest was damaged and there were fresh animal signs and fragments of eggshell in the vicinity. We estimated the apparent hatching success rate as the proportion of hatched nests to the total number of monitored nests. We could not monitor the survival of hatched chicks from a particular nest as they left the nest after two to three days after hatching. However, in each monitoring day, we intensively searched for all the chicks and accordingly estimated the apparent chick survival rate of each nesting site as a proportion of the number of chicks reaching fledging to the total number of chicks hatched. Chick mortality was identified as died if the carcase of the chick was intact or predated if chicks were not further recorded before the expected fledging date. Different age classes of the hatchlings were identified as: (1) hatchlings not capable of flight, (2) fledglings able to fly with indistinct lower and upper mandible length and (3) juveniles equal to adult size with pale fringes on back and wing feathers along with distinct lower and upper mandible length with dark tip.

We also measured the length and width of 21 deserted eggs (11 in 2017 and 10 in 2018) using a digital calliper to the nearest 0.01 mm to calculate the egg volume (V_e) and egg shape index (SI) using the formulas following Coulson (1963) as$Ve=K\times L\times B^2$ $SI=\left(B/L\right)\times 100$where K is the volume coefficient with a constant value of 0.482 (Calvo 1994, Hanane et al. 2010), L is the egg length and B is the egg width.

Data analysis was carried out in PAST version 3.20 (Hammer et al. 2001).

Results

Description of the nesting sites

During two years of monitoring, nesting sites of Indian Skimmers were recorded from seven different islands (five in 2017 and four in 2018) along the Mahanadi River (Figure 1, Table 1). Nesting sites were mostly temporary, sandy islands spreading over an area of 1.50 –41.89 ha and situated at a distance of 0.07–1.61 km from the mainland and 0.18–1.94 km from the nearest human habitation (Table 1). These islands were mostly barren with sporadic patches of grasses and shrubby vegetation. The numbers of Indian Skimmer nests recorded from each island during the two years of monitoring are given in Table 1.

Table 1. Nesting sites, number of nests and breeding success rate of Indian Skimmers along the Mahanadi River in Odisha, India during 2017 and 2018. ID of the nesting sites refers to the locations in Figure 1.

					Number of nests		Hatching success (%)		Chick survival (%)
ID	Nesting sites	Area (ha)	Distance from mainland (km)	Distance from nearest human habitation (km)	2017	2018	2017	2018	2017	2018
1	Botalama	19.05	1.61	1.94	–	7	–	0	–	0
2	Bheda	17.68	0.64	1.91	–	34	–	38.23	–	22.9
3	Jatamundia	23.15	0.65	1.25	4	16	75	56.25	42.85	29.2
4	Kainmundi	41.89	0.31	0.79	6	–	0	–	0	–
5	Mundali upstream	4.80	0.65	0.83	65	–	30.76	–	19.04	–
6	Mundali downstream	1.50	0.44	0.51	16	72	100	62.50	36.37	36.7
7	Kakhadi	5.80	0.07	0.18	10	–	80	–	21.05	–
	Total				101	129	72.27	52.71	27.92	33.15

Population and breeding phenology

Within the study area, the population of breeding Indian Skimmers was estimated as 188 individuals in 2017 and 224 in 2018. Arrival of the birds to the breeding sites was first recorded on 22 February in 2017 and 6 January in 2018. Egg-laying started on 5 April in 2017 and continued for a period of 46 days whereas in 2018 it started on 1 March and continued for a period of 70 days. The peak egg-laying period in both years was during the first half of April (2017: 59%, n = 165 and 2018: 72.5%, n = 280) (Figure 2). In 2017, hatching was first reported on 25 April and continued for a period of 28 days, and in 2018 it was first recorded on 18 April and continued for a period of 26 days. In both years, the peak hatching activity was recorded during the second half of April (2017: 65.6%, n = 101 and 2018: 67.4%, n = 128) (Figure 2). The overall incubation period including both years of monitoring varied from 21 to 24 days with an overall mean (±se) of 22.3 ± 0.05 days; incubation periods were similar between years. Departure of the birds from the breeding sites started from the second half of May in both years and continued until first and second half of July in 2017 and 2018 respectively (Figure 2).

Figure 2. Phenology of nest initiation, egg laying and hatching of the Indian Skimmer along the Mahanadi River in Odisha, eastern India during 2017 and 2018.

Distribution and abundance of nests

During two years of monitoring, a total 230 Indian Skimmer nests (101 in 2017 and 129 in 2018) were recorded from the study area. The number of nests in each nesting colony is given in Table 1. Nests were characterized as shallow depressions on sand with the diameter ranging between 14 and 34 cm (mean ± se = 26.22 ± 0.24 cm). All the nests were located at a distance of 0.60–45 m (mean ± se = 10.42 ± 0.45 m) from water and 0.03–24 m (mean ± se = 4.40 ± 0.26 m) from ground vegetation. There were significantly more nests located closer (0–10 m) to water (χ² = 110.64, df = 2, P < 0.05) and vegetation (χ² = 391.46, df = 2, P < 0.05) than were located further away. Overall, more than 60% of the nests were located within 10 m of water and vegetation (Figure 3). The abundance of nests did not vary significantly between the years in relation to distance from water (F_1,3= 1.01, P > 0.05) and ground vegetation (F_1,3 = 0.02, P > 0.05). It was observed that Indian Skimmers shared their nesting colonies with Black-bellied Terns Sterna acuticauda, River Terns Sterna aurantia, Little Terns Sternula albifrons, River Lapwings Vanellus duvaucelii and Little Pratincoles Glareola lactea in our study area.

Figure 3. Frequency distribution of Indian Skimmer nests in relation to distance (m) from water and ground vegetation along the Mahanadi River in Odisha, eastern India during 2017 and 2018.

Clutch size and egg dimensions

Clutch size varied from one to five eggs in both study years and three-egg clutches occurred most frequently (44.5%; n = 45 of 101 nests in 2017 and 44.9%; n = 58 of 129 nests in 2018) (Figure 4). The mean (±se) clutch size was 2.73 ± 0.10 eggs in 2017 and 2.99 ± 0.08 eggs in 2018; with a significant difference between years (F_{1, 228}= 4.20, P < 0.05). Based on the measurement of 21 deserted eggs, the mean egg length, width, volume and shape index did not vary significantly between the two years (Table 2).

Figure 4. Frequency distribution of Indian Skimmer clutch sizes along the Mahanadi River in Odisha, eastern India during 2017 and 2018.

Table 2. Biometrics of a sample of 21 deserted Indian Skimmer eggs collected in the Mahanadi River in Odisha, India. F and P report the comparison between years.

Measurements	2017	2018	F	P
Sample size	11	10
Mean length (cm) ± se	4.06 ± 0.06	4 ± 0.04	0.56	0.45
Mean width (cm) ± se	3.01 ± 0.02	2.98 ± 0.02	0.74	0.40
Mean volume (cm³) ± se	17.70 ± 0.40	17.16 ± 0.21	1.31	0.26
Mean shape index ± se	74.22 ± 1.04	74.61 ± 1.01	0.06	0.79

Nest survival and breeding success

Among the 230 monitored nests (101 in 2017 and 129 in 2018), only 61.30% of nests (73 in 2017 and 68 in 2018) successfully produced chicks. Hatching success was higher in 2017 (72.27%) than 2018 (52.71%). The daily nest survival probability was estimated as 93.36% in 2017 and 89.48% in 2018. Similarly, the cumulative nest survival probability was 22.08% in 2017 and 8.48% in 2018. Overall, the daily and cumulative nest survival probability was estimated 91.11% and 12.56% respectively. The various causes of nest failure at the egg stage were flooding and desertion (26.97% each), egg collection by local people (21.35%), trampling by animals and predation (10.11% each) and trampling by people (4.49%). Between two years of monitoring, flooding, desertion and trampling were major factors of nest failure in 2017, while egg collection, desertion and flooding had a major impact in 2018 (Table 3).

Table 3. Causes of nest failure for the Indian Skimmer along the Mahanadi River in Odisha, India during 2017 and 2018.

	2017		2018
Causes of failure	n	%	n	%
Egg stage failure
Desertion	7	25	17	27.87
Egg collection	0	0	19	31.15
Predation	4	14.29	5	8.20
Flooding	10	35.71	14	22.95
Trampling by people	2	7.14	2	3.28
Trampling by animals	5	17.86	4	6.56
Total	28	100	61	100
Chick stage failure
Died from unknown cause	67	60.36	89	70.08
Predation	44	39.64	38	29.92
Total	111	100	127	100

Similarly, among the 344 hatched chicks (154 in 2017 and 190 in 2018) only 106 reached the juvenile stage, corresponding to an apparent chick survival rate of 30.81%. It was higher in 2018 (33.15%; 63 out of 190 chicks) than 2017 (27.92%; 43 out of 154 chicks). Among the factors affected chick survival, predation accounted for 34.45% of chick mortality, and 65.55% of chicks died from unknown causes (Table 3). It was observed that the mortality rate was higher in chicks (44.12%; n = 105) than fledgelings (34.87%; n = 83) and juveniles (21.01%; n = 50).

Discussion

Waterbirds in general have not received adequate monitoring in India, except for one day during a mid-winter waterbird census once a year (Kumar et al. 2005, Rahmani & Nair 2012). The Indian Skimmer was believed to be a winter visitor to Odisha, until Rahmani & Nair (2012) first predicted, and then Rajguru (2017) and Debata et al. (2018) later confirmed, their breeding activities along the Mahanadi River. Our two years of monitoring, along with earlier observations by Rajguru (2017), suggest that Indian Skimmers congregate in our study area during January and breed between March and May. Our observations on breeding season phenology and selection of nesting sites by Indian Skimmers support similar reports from elsewhere in India (Sundar 2004, Das 2015, Siddiqui et al. 2007, Dilawar & Sharma 2016, Fernandes & Besten 2013).

In our study area, Indian Skimmers faced a wide range of threats during the breeding season (Figure 5). Flooding, desertion of nests and collection of eggs were found to be major factors causing nest failure for the birds. All the canals in our study area were constructed during the late eighteenth century primarily for irrigation and waterway transportation purposes and were further extended to meet the demand for water in industrial and urban areas. However, during the course of time, the channel capacity and flow of water in these canals has declined due to the erosion of soil from nearby areas, dumping of household waste and other anthropogenic activities (Prusty & Biswal 2017). Scarcity of water in these canals is severe during summer, when agricultural activities extensively depend on canal water. To overcome this situation, the water outlet gates downstream, near the Mahanadi and Naraj barrages are frequently closed to increase the water level of the river so that sufficient water can pass through the canals to meet demand. During these activities, the temporary islands frequently get submerged which floods the nests of Indian Skimmers and other species. During our two years of monitoring, flooding incidents affecting the nests of Indian Skimmers and other birds were recorded on 16 occasions.

Figure 5. Factors increasing the risk of nest failure for the Indian Skimmer along the Mahanadi River in Odisha, eastern India: (a) movement of cattle, (b) movement of stray dogs, (c) disturbance by local children, (d) sand extraction, (e) flooding of nests and (f) death of chicks.

All the recorded nesting sites were situated outside protected areas and within zones with high levels of human activity. A variety of grasses and shrubby vegetation grew on the islands as they emerged out of the water and local people took advantage of it to graze their buffalos, which trampled some of the nests and chicks. Moreover, as the water level in the river usually remained lower during summer, in many instances local children accessed the islands and played on them during afternoon hours. Collection of eggs was found to be another major factor affecting hatching success rate and it was only recorded along with the upstream areas near Botalama. Our discussion with the local people revealed that they collected the eggs of Indian Skimmers and other waterbirds for consumption. Intensive movement of fishing boats and heavy machinery used for sand extraction were additional threats during the breeding season. The combination of these human activities might have caused some incubating birds to desert their nests.

On several occasions, when the water level in the river was very low, stray dogs gained access to the islands and were seen to walk through nesting sites. Additionally, natural predators, such as Grey Herons Ardea cinerea, Brown-headed Gulls Chroicocephalus brunnicephalus, Black Kite Milvus migrans and Indian Monitor Lizards Varanus bengalensis were recorded on the nesting sites during the breeding season and they might have been responsible for the predation of some eggs and chicks.

On a small scale, we found that Indian Skimmers nested significantly closer to water and small patches of vegetation than expected, and we suggest that this behaviour is in response to the problem of thermoregulation for adults, eggs and chicks. Birds that nest on exposed ground face heavy heat loads during the hot hours of the day (Grant 1982). To mitigate this thermally stressful condition, they deploy certain behavioural and physiological strategies (Purdue 1976, Grant 1982, Downs & Ward 1997, Amat & Masero 2004, Mougeot et al. 2014). In our study, incubating Indian Skimmers were frequently observed to engage in soaking their bellies during the heat of the day, probably for thermoregulation to overcome heat stress (Amat & Masero 2007). When incubating birds leave their nests to belly-soak, the eggs are exposed to direct sunlight potentially resulting in a sudden increase in temperature which could be fatal for the eggs, leading to egg desertion (Amat & Masero 2004). Nesting closer to the water might reduce some of these costs for adult Indian Skimmers. Additionally, chicks were also recorded sheltering in moist areas near water and by ground vegetation during afternoon hours, probably to overcome high temperature.

During our two years of monitoring (2017 and 2018) and data from 2016 (Rajguru 2017), we observed between-year variation in nesting site selection and the egg-laying period in Indian Skimmers. Such nest site shifting and variation in egg-laying dates have also been observed in Black Skimmers (Furfey 2014) and this behaviour may reflect the challenges faced by skimmers in their temporary breeding habitats (Raynor et al. 2013, Owen & Pierce 2013, Furfey 2014). Availability of suitable nesting sites, flooding, interspecific competition and predation may all play important roles in nesting site selection.

Implications for conservation

Indian Skimmers face a wide range of anthropogenic as well as natural threats that affect their breeding success along the Mahanadi River in Odisha, eastern India. Protection of their nesting sites from human-induced threats could be increased with appropriate conservation activities supported by the Water Resource Department, Revenue Department and local people. Dredging and clearing the canals would allow sufficient movement of water for agricultural and other uses, so that there would be a reduced need to increase the water level in the river.

The use of artificial floating islands as nesting sites in habitats experiencing water level fluctuation can increase reproductive success for some species, for example, Red-throated Divers Gavia stellata, Black-throated Divers Gavia arctica (Merrie 1996, Hancock 2000), Great Northern Divers Gavia immer (Piper et al. 2002), Black Terns Chlidonias niger (Shealer et al. 2006) and Eurasian Pelicans (Catsadorakis 2017). It would be useful to try these for the Indian Skimmer and other co-nesting waterbirds.

Disturbance from sand extraction and fishing boats near nesting sites could be controlled during the breeding season. The possible effects of trampling of eggs and chicks from the movement of livestock, egg collection and disturbance by children in the nesting islands can be minimized by raising awareness among the local people and involving them in protection of the nesting sites (Claassen 2004, 2017). Accessibility of stray dogs and buffalos to the nesting sites could be controlled by fencing the connecting routes.

These recommendations will not only aid in the long-term conservation of the Indian Skimmer, by increasing their nest survival rate, but would also increase the protection for co-nesting threatened waterbirds such as the Black-bellied Tern, River Tern and River Lapwing which breed in similar habitats and experience similar threats (Rahmani 2012).

Acknowledgements

We thank the PCCF (WL) and CWLW for granting permission for the study. We thank the local Forest Range Officer for logistic and field-based support during the study. Special thanks to Sanjay Kumar Dalai for his assistance during fieldwork. Thanks to the reviewers for their valuable suggestions in improving the manuscript.

ORCID

Subrat Debata http://orcid.org/0000-0001-8296-1734

Tuhinansu Kar http://orcid.org/0000-0001-5264-7111

Himanshu Shekhar Palei http://orcid.org/0000-0001-7783-7587

Additional information

Funding

The study was carried out with financial support from Compensatory Afforestation Fund Management and Planning Authority, India allotted to Chandaka Wildlife Division.