Journal of Global Biosciences ISSN 2320-1355 Volume 5, Number 1, 2016, pp. 3450-3460 Website: www.mutagens.co.in E-mail: [email protected] [email protected] Research Paper FEEDING RATE AND DIET OF THE NEAR THREATENED ORIENTAL melanogaster IN KUTTANAD WETLANDS OF KERALA, INDIA Narayanan, S. Prasanth and A.P. Thomas Advanced centre of Environmental Studies and Sustainable Development, Mahatma Gandhi University, Priyadarsini Hills, Kottayam, Kerala, India.

Abstract A study on the feeding rate, prey of the near threatened Oriental Darter Anhinga melanogaster was studied at the Kuttanad wetlands. It showed more or less steady feeding rate throughout the day with a slight reduction in the noon time. The feeding rate was found almost stable from June to September and a declining trend was noticed from October. Direct observation at the foraging areas in the Vembanad Lake and various adjacent paddy fields showed that it preyed on altogether 17 species of fishes and prawn/shrimp species. family species and Stolephorus species formed the dominant prey species. Mean length of fishes from the direct observations, samplings in the selected areas and regurgitation did not show any significant variation. Key words: Oriental Darter, prey, Kuttanad, Vembanad Lake .

INTRODUCTION Waterbirds use diverse food items including seeds, leaves, tubers and rhizomes, invertebrates and vertebrates such as fishes and amphibians [1]. Composition, distribution, amount and spatiotemporal dynamics of these food resources is the key factor which determines the distribution of waterbirds on the feeding grounds and can be important indicators of the habitat quality [2-4]. Food preference of waterbirds can vary greatly among species, even among those within the same group [1]. The diet of varies through the day, through the year, and between years, sites, sexes, or age groups and even between individuals [5]. Waterbirds also can change their diet composition with season and site [6]. Prey size also affects the prey selection of waterbirds [2,7]. However, the relationship between waterbirds and their food is still largely unexplored [1]. Oriental Darter normally inhabits shallow inland wetlands including lakes, rivers, swamps, village ponds, and reservoirs, as well as estuaries, tidal inlets, mangroves and coastal lagoons [8-10]. As per Rahmani [11] need unpolluted, medium and large sized, deeper water bodies. Being a diving waterbird they are mainly piscivorous and at certain times they used to eat some too large ones for the birds’ slender bill and gullet and shows local movements depending on the water conditions [8,9]. Workers such as Ali [12]), Neelakantan [13], Sivaperuman and Jayson [14], Narayanan and Vijayan [15] put light on the feeding habits and prey fishes of several wetland birds of Kerala. But details on the food and feeding rate, rhythm, prey species and abundance of the near threatened Oriental Darter in Kerala has not yet been Journal of Global Biosciences Vol. 5(1), 2016 pp. 3450-3460 ISSN 2320-1355 explored and hence the present study was carried out in selected feeding areas of the in Kuttanad wetlands.

MATERIALS AND METHODS Regular foraging observations of the Darter were made during the daylight hours using Bushnell 7x35mm binoculars in open Vembanad Lake (part of Vembanad-Kole Ramsar Site) from June to November of 2010 and 2011 following the ‘focal sampling’ [16]. Feeding of the Darter was studied five time schedules per day during 6.00 - 7.00, 9.00 - 10.00, 12.00 - 13.00, 15.00 - 16.00 and 17.00 - 18.00 hrs. The focal bird was observed continuously for regular intervals. Feeding rate was found out using the formula, Feeding rate = total number of feeding observation / total time of observation of bird in minutes. Stomach content analysis was not carried out as sacrificing birds to determine diet only is nowadays usually considered unacceptable [5]. Prey items on which Darters eat were found out by the direct observation method at the Vembanad Lake and through opportunistic observation at various adjacent paddy fields within the study area, from regurgitates at the nesting sites and sampling at foraging areas. Direct observation and regurgitates at the nesting sites can be a reasonable method of estimating prey size [5]. In the case of direct observation the relative measure of the prey item is converted into actual length by multiplying with mean bill length. As per Ali and Ripley [8] beak length of Oriental Darter is 7.4cm in male and 9cm in female. It is difficult to differentiate the male and female in the field; hence the average (8.2cm) of above measurements was used as the base bill length of Oriental Darter for direct observation to estimate the prey length [5]. Cast nests are suitable for majority of the wetlands, especially the shallow ones [17,18]. Hence available fish species in the foraging sites were collected with the help of cast net, which is made of fine mesh having a radius of 2m. During each sampling, three cast net deployments were made from country boat and the data was used to measure the abundance and diversity. Samplings were done at 10 selected sites within the Vembanad Lake, which span from normal feeding areas to central deep water zone. Samplings were carried out once in every three weeks from June to November. Certain species of birds such as herons, pelicans etc. used to regurgitate whole fish and other items eaten [5,19]. Hence diet of nestling Darter was studied from regurgitated food items or from the prey items slipped out from the young one during the feeding frenzy collected from below the nesting trees at South Police Station heronry - Alappuzha. Prey items severely handicapped and decayed were not collected. Regurgitated samples were collected and analysed at several times during the study period. The weight and length of each fish collected were noted with the help of a balance and metric scale and then stored in 10% formalin solution. They were identified with the help of published works [20-24] and with the help of experts. The samples collected were computed for relative frequency by numbers (RFN), relative frequency of occurrence (RFO), and relative frequency of weight (RFW) of each prey species as follows: No. of individuals of a species Relative frequency by numbers (RFN) = ------x 100 Total no. of individuals of all species Weight of a species Relative frequency by weight (RFW) = ------x 100 Total weight of all species No. of samples in which the species occurs Relative frequency of occurrence (RFO) = ------x 100 Total no. of samples Calculations of Index of Relative Importance (IRI) were based on Findholt and Anderson (1995), and each prey species was ranked. IRI = (RFN + RFW) x RFO/200). The value of the IRI ranges from 0 (when all three values are 0%), to 100 (when all three values are 100%). Diversity indices, abundance etc were calculated using the BPMSG Diversity Online Calculator. Z test was used to find out any significant variation among the mean length of most commonly preyed fish species by Darter in direct observation, sampling and from the regurgitated http://mutagens.co.in 3451 Journal of Global Biosciences Vol. 5(1), 2016 pp. 3450-3460 ISSN 2320-1355 samples. The same test was also used to find out the significant variation in mean weight of fishes in samplings and regurgitations.

RESULTS A total of 70.5 hours of feeding data were gathered during the study period. Oriental Darter showed a feeding rate of 0.1/min. It was found that from June to September the feeding rate was almost stable but from October onwards it showed a declining trend (Fig. 1). Highest feeding rate was noticed in the month of June, 2011 but following a reduction in July. Oriental Darter showed almost stable feeding rate throughout the day, even though a reduction was noticed in the noon time. In the case of feeding rhythm, there showed slight variation in both years of the study period. Compared to 2011 feeding rate in 2010 was higher in 15-16 hrs and 17-18 hrs of observations (Fig. 2). But in the 2011, morning 06-07 hrs and 09-10 hrs showed higher feeding rate (Fig. 3). Among the 1014 feeding attempts observed during the study period Darters succeeded to catch the prey only in 421 times which is 42% of the observed feeding attempts. Successful feeding attempts were almost similar in both years, with the exception of high success in 2011 June month. Just like the feeding rate, successful feeding observation also showed a declining trend after September in both years of the study period. In certain instances Darters were found to feed even 18.45 hrs or beyond. 21.7 seconds was the average time (with a range of 6 to 73 seconds) Darter used to spend underwater as part of the preying attempt.

0.16 0.14 0.14

0.12 0.1 0.11 0.12 0.11 0.10 0.09 0.09 0.11 0.08 0.09 0.09 0.06 0.07 2010 0.05 2011 Feeding rate/Minute Feeding 0.04 0.02 0.00

Figure 1. Feeding rate of Oriental Darter during the study period

0.20 0.18 0.16 0.14 0.12 06-07 Hrs 0.10 09-10 Hrs 0.08 12-13 Hrs 0.06 15-16 Hrs 0.04 17-18 Hrs 0.02 0.00

Figure 2. Feeding rhythm showed by Oriental Darter various months of 2010

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0.18 0.16 0.14 0.12 0.10 06-07 Hrs 0.08 09-10 Hrs 0.06 0.04 12-13 Hrs 0.02 15-16 Hrs 0.00 17-18 Hrs

Figure 3. Feeding rhythm showed by Oriental Darter various months of 2011

Fishes were found to form the major diet of the Oriental Darter in the study area. From the direct observation and the analysis of regurgitates it was found that the various species belonged to Cyprinidae family and Stolephorus spp. formed the dominant prey species. Direct observation study revealed that it preyed altogether on 17 species of fishes and prawn/shrimp species (Table 1). Among the fishes Amblypharyngodon melettinus, Puntius spp . and Etroplus maculatus were consumed by Darters in both the Vembanad Lake and paddy fields, but species such as Channa striata, Channa marulius, Heteropneustes fossilis and Anabas testudineus were found to be preyed only in the paddy fields. The mean length of prey fishes eaten by Oriental Darter in Kuttanad wetlands was 7.53±2.89cm within a range of 2.4 to 25.4cm. The largest fish happened to be devoured by a Darter was a catfish Heteropneustes fossilis and smallest were of Puntius vittatus. Species such as Stolephorus spp. , Amblypharyngodon melettinus , filamentosa, Puntius spp ., Parambassis spp . and Etroplus suratensis are the most commonly preyed species. Samplings were done at ten selected sites using the cast net to find out the available prey species. This revealed the presence of 19 species of fishes belonging to 10 families and one invertebrate species (prawn/shrimp). Stolephorus spp. (58.6%) and Parambassis spp. (11.3%) were the most abundant fish species collected during the samplings. These two species were present in almost all samplings. Species such as Systomus sarana subnasutus, Labeo dussumieri , Stenogobius gymnopomus, Mystus spp., Horabagrus brachysoma and Mastacembelus armatus were least abundant (0.2%). Abundance of each prey species during the whole time period of the study is given in Table 2. Chithira Kayal (site VII) showed high species diversity (1.8) followed by Pennar River mouth area (site I) and least were at the last site north of the Thannermukkom saltwater barrage and no prey species was collected from site IX. But Pathiramanal Island (site VIII) showed high species richness (12 species) followed by Chithirakayal (site VII) and Kumarakom Jetty (site IV) with a richness of 9 and 8 species respectively. Richness was low at site north of the Thanneermukkom saltwater barrage (Table 3). Mean length and weight of the most commonly collected fish species during the samplings are given in Table 4. Collection of the regurgitated prey items from the South Police Station heronry - Alappuzha yielded valuable information on the food items which is fed to the nestlings. A total of 65 individuals of 10 fish species and one prawn/shrimp species were collected from below the nesting trees. These breeding birds fed mostly on fishes and occasionally on prawns/shrimps (Table 1). The species of fishes collected were Stolephorus spp ., Amblypharyngodon melettinus, Systomus sarana subnasutus, Dawkinsia filamentosa, Puntius amphibius, Puntius vittatus, Puntius spp., Parambassis spp. and Anabas testudineus . Relative frequency of occurrence (%), relative frequency of weight (%) and relative frequency of number of each species are given in Table 5. Stolephorus spp . occurred in the highest frequency

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(85.71%) and three species such as Puntius vittatus, Systomus sarana subnasutus and Prawn/Shrimp spp. came in the lowest frequency (14.29%). Mean length of selected fish species during the direct observations, samplings in the selected areas and sampling based on the regurgitation showed only a slight difference (Table 4). The same was in the case of weight of fishes collected in samplings and in regurgitations. Z test carried out illustrated that there is no significant difference in the mean length of fishes sampled by the three methods and the same is the case with weight.

Table 1. Prey items observed to be eaten in the wild and collected from the nesting sites of Oriental Darter Sl. No. Species Vembanad Lake Paddy fields Nesting site Fishes : Clupeiformes Family: Engraulidae 1 Stolephorus spp. + + Order: Family: Cyprinidae 2 Amblypharyngodon melettinus + + + 3 Barbodes subnasutus + + 4 Dawkinsia filamentosa + + 5 Puntius amphibius + 6 Puntius vittatus + + 7 Puntius spp. + + + 8 Labeo dussumieri + Order: Perciformes Family: Ambassidae 9 Parambassis spp. + + Family: Anabantidae 10 Anabas testudineus + + Family: Channidae 11 Channa marulius + 12 Channa striata + Family: Cichlidae 13 Etroplus maculatus + + + 14 Etroplus suratensis + Family: Nandidae 15 Pristolepis spp. + Order: Siluriformes Family: Bagridae 16 Mystus spp. + 17 Horabagrus brachysoma + Family: Heteropneustidae 18 Heteropneustes fossilis + Invertebrates 19 Prawn/Shrimp spp. + +

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Table 2. Abundance of prey items (%) at different sampling sites Sl. Species I II III IV V VI VII VIII IX X No. Fishes Order: Beloniformes Family: Belonidae 1 Xenentodon cancila 3.3 3.4 9.4 1.1 3.2 16.2 10 4.5 Family: Hemiramphidae 2 Hyporhamphus xanthopterus 2.2 0.5 2 Order: Clupeiformes Family: Engraulidae 3 Stolephorus spp. 51.1 79.3 71.9 51.4 68.3 45.9 38 70.5 Order: Cypriniformes Family: Cyprinidae 4 Amblypharyngodon melettinus 22.2 14.2 15.9 5 Systomus sarana subnasutus 0.6 6 Labeo dussumieri 3.4 7 Dawkinsia filamentosa 4.4 6.9 8.2 27 16 1.8 8 Puntius amphibius 1.1 9 Puntius mahecola 0.5 1.7 Order: Perciformes Family: Ambassidae 10 Parambassis spp. 11.1 6.9 15.6 23.5 1.6 5.4 16 1.7 25 11 Parambassis ranga 3.2 Family: Cichlidae 12 Etroplus maculatus 4.4 3.1 .5 1.6 2.7 8 3.4 13 Etroplus suratensis 4 2.8 Family: Gobiidae 14 Glossogobius giurus 1.7 15 Stenogobius gymnopomus 0.6 Family: Scatophagidae 16 Scatophagus argus 75 Order: Siluriformes Family: Bagridae 17 Mystus spp. 1.1 18 Horabagrus brachysoma 0.6 Order: Synbranchiformes Family: Mastacembelidae 19 Mastacembelus armatus 2 Invertebrates 20 Prawns/shrimps 6.3 2.7 4

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Table 3. Fish diversity indices and species richness in different sampling sites Sampling sites Shannon-Wiener Index Simpson Index Species richness Site I - Pennar River Mouth 1.45 0.33 8 Site II – Kavanar River Mouth 0.78 0.64 5 Site III – Fish Sanctuary 0.86 0.55 4 Site IV – Kumarakom Jetty 1.3 0.35 8 Site V – Net area 1.08 0.5 7 Site VI – Methran Kayal 1.36 0.31 6 Site VII – Chithira Kayal 1.8 0.22 9 Site VIII – Pathiramanal Island 1.19 0.51 12 Site IX – Kannankara Church 0 0 0 Site X – After saltwater barrage 0.56 0.62 2

Table 4. Mean length and weight of the most commonly preyed fish species by Oriental Darter Direct observation Sampling Regurgitation

Species Length Length Weight Length Weight Stolephorus spp . 6.47±0.68 6.34±0.38 2.13±0.95 6.15±0.40 1.86±0.37 Amblypharyngodon 7.1±1.38 7.63±0.37 3.53±0.54 7.04±1.96 3.81±0.70 melettinus Dawkinsia filamentosa 7.31±1.99 6.62±1.37 5.05±2.37 7.61±2.07 8.63±3.98 Puntius spp . 7.43±1.55 ------7.06±12.91 3.7±1.18 Parambassis spp . 5.69±1.29 5.36±1.01 1.90±0.82 5.37±0.84 1.83±0.15 Etroplus suratensis 9.66±4.4 6.16±0.35 5.44±1.26 ------Etroplus maculatus 5.72±1.53 6±1.38 5.08±2.44 6.45±1.06 6.1±0.71

Table 5. Relative frequency of number of species from the regurgitated samples

Species (N) RFN (%) RFW (%) RFO (%) IRI (%) Stolephorus spp . 27.69 11.59 85.71 16.83 Amblypharyngodon melettinus 15.38 13.02 71.43 10.14 Dawkinsia filamentosa 12.31 23.58 57.14 10.25 Puntius amphibius 9.23 10.42 57.14 5.62 Anabas testudineus 9.23 16.30 42.86 5.47 Puntius spp. 7.69 6.32 28.57 2.00 Etroplus maculatus 3.08 4.17 42.86 1.55 Parambassis spp. 4.62 1.88 28.57 0.93 Puntius vittatus 3.08 5.30 14.29 0.60 Prawn/Shrimp spp. 6.15 3.66 14.29 0.70 Systomus sarana subnasutus 1.54 3.76 14.29 0.38

DISCUSSION Kamsuk’s [25] study on the ecology of Oriental Darter at Phu Khieo Wildlife Sanctuary of Thailand found that the Darters used to feed before 07.00 and during 10.00 – 12.00 and 13.30 – 16.00 hrs. But the present study showed that it mainly preyed on the early morning and late evening hours. The reason would be the less disturbance level during these periods from the tourism activities in the foraging areas. The mean dive duration of 48.46 seconds was recorded at the Kalpally-Pallipoyil wetland of north Kerala by Chozhiyattel [26]. But here in Kuttanad it was 21.7 seconds. Chozhiyattel’s [26] finding was based on a total of 186 observations, but in the present study in Kuttanad it was 1014. The increase in the observation might be the reason

http://mutagens.co.in 3456 Journal of Global Biosciences Vol. 5(1), 2016 pp. 3450-3460 ISSN 2320-1355 for this reduced dive time in Kuttanad. The availability of the prey items might also be a factor behind the reduced diving time. The dive duration in Darter is more than that of the dive duration showed by the Little [26]. According to Hustler [27] Darters are able to exploit the whole water column and there is no relationship between the time spent underwater and the depth of water. During the extensive field visits of the present study none of the Darters were found to feed in the deeper water areas. Hence it is clear that these birds are mainly shallow water feeding species. Social feeding helps birds to exploit various prey items across their range [28,29]. But Darters are solitary feeding birds, even though used to forage in the same location but widely apart from each other. Being a solo feeding species, Darters may not be getting this benefit in its foraging zones. Solo feeding waders show cryptic plumage [28], which helps the birds in feeding. But the Darters are generally black birds with pale dorsal part; its plumage pattern may also help its underwater feeding mode. Occasionally darters used to feed in the same area with Little and Indian Shag. High number of foraging wetland bird species and their flocking patterns will also exert predator pressure on certain groups of prey [14]. Hence such occasional social foraging by Darters would be due to the concentration of prey species. During the study period at certain instances Darters were found to feed even at 18.45 hrs, but no nocturnal foraging has been recorded. Nocturnal feeding behaviour has been reported for the diurnal Double-crested Cormorants Phalacrocorax auritus at Mississipi, USA [30]. Hence chances for nocturnal foraging cannot be completely ruled out in this species. Johansen et al. [31] stated that, the daily foraging pattern is generally bimodal in many species with peaks in morning and evening; the same pattern was also noted in the present study. But it may be noted that a study carried out in Kuttanad wetlands on the feeding rate of diurnal Ardeidae family species did not show such bimodal pattern [15]. The dietery habits and related feeding ecology of the Darter have not been described in the wetlands of Kerala and the same is with other wetland birds of the state. A study on the food items of the Ardeidae family species at two selected areas of Vembanad Lake environs revealed that they feed on 8 species of fishes in the paddy fields [15]. 13 prey species was recorded from the Kole wetlands by Sivaperuman and Jayson [14]. In the present study Stolephorus spp . were the most abundant fish species collected from the sampling sites or during the direct observation or from the regurgitated samples collected at nesting the sites. But Narayanan and Vijayan [15] reported that the most abundant species was Puntius vittatus followed by the Amblypharyngodon melettinus . During the present work these species were collected but not as abundant compared to Stolephorus spp . But the Puntius genera species were one of the most commonly preyed fish forms by Darter in Kuttanad wetland. Species such as Aplocheilus blockii, Aplocheilus lineatus, Laubuca dadiburjori, Dayella sp ., Macropodus cupanus , Mystus gulio, Mystus vittatus reported by Narayanan and Vijayan [15] are found absent in this study. The reason for such a change would be due to sampling gear used and the habitat sampled. They have used cast and hand nets to sample fishes in the inundated paddy fields. But in the present study sampling was done in the Vembanad Lake by the cast nets. Kamsuk’s [25] study on the ecology of Oriental Darter at Phu Khieo Wildlife Sanctuary of Thailand also revealed that the fishes of Cyprinidae family formed the major part of the diet of Oriental Darter and the present study also agrees with the same. As per Dostine and Morton [32] Oriental Darter rather preyed relatively slow moving benthic types of fishes than the fast moving ones at Alligator Rivers region. But the present study noted that they mostly fed on the very fast moving species such as Stolephorus spp ., Amblypharyngodon melettinus , Puntius spp . etc. Vijayan [33] stated that the species of the genera such as Cirrhinus, Puntius, Oxygaster, Labeo, Mystus, Channa, Notopterus, Heteropneustes, Clarias, and Wallago were the most preferred diet items of Darter at the Keoladeo National Park of Rajasthan. Clarias and Wallago species are also found in Kuttanad wetlands [34], but none of these fish species were collected or found to be eaten in the present study. Hence it is clear that Darters are found to prey on species which are naturally available. Prey size is also an important factor in the prey selection of waterbirds [2,7]. Darters are mainly piscivorous species. In the present study prawns/shrimps were also found to be eaten by Darter and the same were also collected from the nesting sites. But studies on the diet of Australian Darter at Alligator River region of http://mutagens.co.in 3457 Journal of Global Biosciences Vol. 5(1), 2016 pp. 3450-3460 ISSN 2320-1355

Australia, based on the gut content analyses revealed the occurrence of the fragments of freshwater sponges and aquatic macrophytes such as Hydrilla verticillata, Najas tenuifolia and various seeds of aquatic grasses [32]. The mean length of the fish species on which Darter preyed at Kuttanad wetlands were 7.53±2.89cm, but it ranged between 2.4 to 25.4cm. This also agrees with the report on the lenghth of prey items reported from the Keoladeo National Park by Vijayan [33], where Darter preferred mainly the prey species with a size range of 6 to 10cm. Dostine and Morton [32] reported that at Northern Territory of Australia, fish prey length ranged from 2.7 to 16.1cm. Earlier studies on prey size selection by wetland birds showed that there was pronounced tendency for larger birds to feed on larger prey [35]. Being a moderately sized bird, Darter feeds on relatively smaller sized prey items with a few exceptions. Commonly occurring fish species Xenentodon cancila , Hyporhamphus xanthopterus, Labeo dussumieri, Glossogobius giurus, Stenogobius gymnopomus , Scatophagus argus, Horabagrus brachysoma and Mastacembelus armatus were not found consumed during the direct observation, and were absent in the regurgitates also.

CONCLUSION The dietary habits and related feeding ecology of the Darter have not been described in the wetlands of the Kerala state. This study revealed certain aspects of the forgaing ecology of the Oriental Darter especially the feeding rate and species of fishes on which they feed in the Kuttanad wetlands. Prey species diversity recorded during the present study is much higher than that of the reported prey items of any pisciovrous wetland birds from the Kerala state.

ACKNOWLEDGEMENT The authors are grateful to Toms Augustine, Mr. Babu Padmakumar and Mr. Abdul Shukkur for their support during the fieldwork and timely assistance. Also would like to thank Dr. B. Sreekumar, President, Kottayam Nature Society for the encouragement and enthusiasm showed in the present study.

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