Herpetology Notes, volume 13: 1073-1077 (2020) (published online on 28 December 2020)

You can’t always get what you want: attempted predation and prey handling of fish by the Checkered Keelback, Fowlea piscator (Schneider, 1799) in Nepal (Serpentes: Natricidae)

Kamal Devkota1,*, Ayush Maharjan2, and Hinrich Kaiser3

The Checkered Keelback, Fowlea piscator (Schneider, During photography walks, the second author (AM) 1799)4 has an extensive distribution in South Asia, made serendipitous observations of encountered including Nepal, and throughout Southeast Asia herpetofauna at Taudaha Lake (27.6481°N, 85.2816°E, (Schleich and Kästle, 2002; Shah and Tiwari, 2004; elevation 1287 m), a small (4.63 km2) lake on the Whitaker and Captain, 2004; Das, 2010, 2012). It is a outskirts of Nepal’s capital city, Kathmandu. The fairly common aquatic snake that inhabits areas around lake and the surrounding area have experienced some freshwater bodies, rice fields, and marshy areas of human impact, but they are less polluted than the more lowlands and hills, entering the water while foraging urban water bodies and there is a significant diversity for a variety of prey during both day and night (Ahsan, of resident and migratory birds (Shrestha and Adhikari, 1983; Hossain, 2016; Parmar, 2018). Young snakes feed 2016). Among the fish, the population of native on aquatic insects, frog eggs, and tadpoles, whereas barbs, catfishes, and snakeheads is being disrupted adults prey on fish, frogs, and occasionally on rodents by several introduced carps, including Bighead Carp and birds (Shah and Tiwari, 2004; Whitaker and Captain, (Hypophthalmichthys nobilis), Common Carp (Cyprinus 2004). Almost the entire literature on feeding in this carpio), Grass Carp (Ctenopharyngodon idella), and species consists of reports from India, but websites in Silver Carp (H. molitrix). Our observations detail two other countries (e.g., Taiwan: Breuer and Murphy, 2010; predation attempts by F. piscator on fish, one on a native Thailand: Thai National Parks, 2020) and reports about catfish and the other on an introduced carp. parasitic infections (e.g., Indonesia: Audini et al., 2017) indicate that prey organisms listed for India are likely Results and Discussion taken by F. piscator throughout its range. Even though Observation 1.—At 13:50 h on 29 May 2019, AM this snake is a prominent member of the herpetofauna of walked near Taudaha Lake and encountered an adult Nepal, there have not been many reports on its feeding F. piscator pursuing a catfish (likely Clarias magur5) ecology in that country. Here we report two predation swimming near the water surface. He spotted the attempts by Fowlea piscator on two types of fish, catfish and carp, at Taudaha, Kathmandu, Nepal, which ultimately failed but provide an example for differential prey handling by this snake. 4 �������������������������������������������������������������������� give its name as Xenochrophis piscator. However, the species piscator was recently reassigned to the genus Fowlea by Pur- kayastha et al. (2018) and we follow their recommendations. 1 Nepal Toxinology Association, Major Chowk, Kawasoti-8, 5 ����������������������������������������������������������������� Nawalpur, Nepal. the catfish, but our images do not reveal complete views of the 2 Himalayan College of Agricultural Sciences and Technology, fish, making this a difficult task. Based on the faintly visible Kathmandu, Nepal. lateral line system we believe the catfish is not a member of 3 Department of Vertebrate Zoology, Zoologisches the genus Glyptothorax but of the genus Clarias. Of the two Forschungsmuseum Alexander Koenig, Adenauerallee species to most likely be encountered in Taudaha Lake, the 160, 53113 Bonn, Germany; and Department of Biology, darker belly colouration would indicate that the fish can be Victor Valley College, 18422 Bear Valley Road, Victorville, identified as C. magur. Whereas accurate prey species identity California 92395, USA. is not significant to our report or in a generalist predator, we * Corresponding author. E-mail: [email protected] attempted identifying the prey to the best of our ability. 1074 Kamal Devkota et al. approximately 1-m-long snake swimming actively (2017) and Kalki (2020), who documented F. piscator towards its desired prey, and it was able to strike at it feeding on the eggs of Rhacophorus malabaricus inside in the water and hold onto it with its teeth (Fig. 1A). the foam nest of these treefrogs, and Moktadir and Hasan The fish was relatively large in comparison with the (2016), who reported that F. piscator consumed boiled snake’s head, and it struggled violently to free itself rice and cooked chicken from a student dormitory’s from the snake. The fish struggled for ca. 15 min and cafeteria outlet drain at night on two consecutive days finally succumbed to its injuries. After the fish ceased on the campus of Jahangirnagar University in Dhaka, struggling, the snake tried to swallow it while remaining Bangladesh. It would certainly appear that either fish in the water. However, perhaps due to size of the fish and the difficulty with manoeuvring slippery prey into an ideal position for ingestion, the snake was unable to consume the fish. After a few minutes of trying to eat the fish, the snake pulled the fish into a nook in the rock wall near the bank of the lake (Fig. 1B). It struggled there once again to swallow the fish (Fig. 1C) but was ultimately unable to do so. After several attempts and struggles, the snake departed and left the dead fish behind. The various scrapes and cuts on the body of the catfish and the changing position of the snake’s head during our observations (Fig. 1B, C) attest to the struggles of trying to subdue the fish and then to swallow it. The observation lasted ca. 35 min. Observation 2.—During another walk at Taudaha Lake, AM again encountered an adult F. piscator, at 12:45 h on 29 November 2019, this time chasing a Common Carp (Cyprinus carpio). He witnessed the capture and followed the snake swimming in the water with the fish in its mouth (Fig. 2A). This fish was also large in size and struggling to free itself from the snake’s grasp, but it eventually ceased struggling and died (Fig. 2B). Unlike in the observation with the catfish, this snake did not attempt to swallow the carp while remaining in the water. Instead, it kept a firm bite in the same position for the entire time of the observation and moved the fish to the lakeside rocks (Fig. 2C). It remained among the rocks for a few minutes with the carp held up out of the water (Fig. 2D). It subsequently attempted to swallow the fish but was unable to do so. Eventually, the keelback disengaged and left the fish among the rocks. The total time taken for these activities was about 20 min. Figure 1. Feeding attempt on 29 May 2019 by an adult Studies on the diet of F. piscator from across its range Fowlea piscator to capture and consume a catfish (likely include Norval et al. (2010), who reported predation Clarias magur) in Taudaha Lake near Kathmandu, Nepal. (A) on a microhylid frog (Microhyla heymonsi) and a fish Having bitten, subdued, and killed the fish, the snake engaged in several futile attempts to ingest it while remaining in the (the snakehead Channa asiatica) in Taiwan, Whitaker open water. (B) Having failed to swallow the catfish in the and Captain (2004), who reported its diet from Indian open water, the snake landed it and tried again at the water’s populations, and Hossain (2016), who recorded that edge. (C) Finally, after dragging its desired prey into the the major food items of F. piscator in Bangladesh were rocks bordering the lake, the snake again tried in vain several insects (56.5%), fish (26.1%), and amphibians (17.4%). times to consume the dead fish. Multiple injuries to the fish Among the more unusual observations on predation in sustained while handled by the snake are visible. Photos by F. piscator are observations by Phansalkar and Gowande Ayush Maharjan. Attempted predation and prey handling of fish by the Checkered Keelback 1075 species in our observations would fall well within the (Nilssonia hurum) in Jagadishpur Reservoir, Kapilvastu, expected food spectrum of F. piscator. Nepal, an attempt that was likely also unsuccessful Clearly, each of the snakes we observed made an based on the width of the turtle’s carapace relative to the error in determining how to optimally exert its energy size of the snake’s head (the observation was fleeting to capture food, given that neither was successful in and when the snake disappeared from view it had not its attempt to eat the large fish. According to Greene yet swallowed the turtle; Kritagaya Gyawali, in litt.). (1997), colubrids commonly prey on animals weighing Another instance of poor judgment by a checkered about 20% of their own mass, with gape width generally keelback was reported by Patel et al. (2017), who found a determining factor. Prior to our observations, Gyawali a dead keelback that appeared to have been killed by the (2019) reported an episode of F. piscator attempting spines of its intended fish prey. to feed on a juvenile Indian Peacock softshell turtle Explanations for such odd occurrences may lie with

Figure 2. Feeding attempt on 29 November 2019 by an adult Fowlea piscator to capture and consume a carp (Cyprinus carpio) in Taudaha Lake near Kathmandu, Nepal. (A) After getting a firm grip on the fish, the snake swam while holding on to the fish until it died. (B) The snake elevated its head above the water level to move the fish, retaining a firm bite at an area dorsal to the anal fin. (C) Still firmly attached at the bite site, the snake landed the carp. (D) The snake moved the carp well into the rocks above the water level. After multiple vain attempts to swallow the dead fish, the snake disengaged and left the fish behind in the rocks. Photos by Ayush Maharjan. 1076 Kamal Devkota et al. the reduction of a natural food supply and opportunism. References The prey-predator weight ratios for the catfish and carp Ahsan, M.F. (1983): Study of food items. Stomach analysis of the described herein were significantly greater than the 20% checkered keelback snake, X. piscator in Bangladesh. Fisheries postulated by Greene (1997). With prey size beyond the Information Bulletin 1: 52–65. limit for the observed F. piscator individuals, these were Audini, I.S., Suwanti, L.T., Koesdarto, S., Poetranto, E.D. (2017): unable to feed on their intended prey. However, there Acanthocephalan in Xenochrophis piscator snake in Sidoarjo, might be other factors affecting feeding behaviour in F. Indonesia. KnE Life Sciences 3(6): 21–27. piscator, particularly in high-elevation lakes surrounded Breuer, H., Murphy, W.C. (2010): Snakes of Taiwan. Xenochrophis by disturbed areas and in the presence of a variety of piscator, Checkered Keelback. Available at https://www. snakesoftaiwan.com/Xenochrophis%20piscator/species_ exotic fish species. Although fish would appear to be xenochrophis_piscator.htm. Accessed on 24 April 2020. common food for F. piscator throughout its range, there Das, I. (2010): A Field Guide to the Reptiles of South-East Asia. are no published studies from Nepal to document the London, United Kingdom, New Holland Publishers. 376 pp. specifics. Das, I. (2012): A Naturalist’s Guide to the Snakes of South-East One aspect of the encounters that may shed some light Asia including Malaysia, Singapore, Thailand, Myanmar, on prey choice in F. piscator is the differential handling of Borneo, Sumatra, Java and Bali. Oxford, United Kingdom, John the catfish and the carp. Whereas the encounter with the Beaufoy Publishing. 160 pp. catfish (Fig. 1) involved attempts by the snake to ingest Greene, H.W. (1997): Snakes, the Evolution of Mystery in Nature. Oakland, California, USA, University of California Press. 351 the fish while floating in the water and subsequently pp. among the rocks, the second snake pulled the carp onto Gyawali, K. (2019): Cheloniophagy by Checkered Keelback, the rocks (Fig. 2C) without any attempt to disengage its Xenochrophis piscator (Schneider, 1799) on Indian Peacock bite or swallow it while afloat. Based on the position Softshell Turtle, Nilsonnia [sic] hurum (Gray, 1830). Bionotes and angle of the bite on the carp, from behind the dorsal 21(3): 67–70. fins near the tail section and just beyond the internal Hossain, M.L. (2016): Food habits of Checkered Keelback, organs, it appears almost incongruous that the fish would Xenochrophis piscator (Schneider, 1799), in Bangladesh. succumb to such an apparently minor injury. Fowlea Bangladesh Journal of Zoology 44(1): 153–161. Kalki, Y. (2020): Natural history notes. Fowlea piscator (Checkered piscator is non-venomous to humans, but irritation and Keelback). Diet. Herpetological Review 51: 143. itchiness has been supported at bite sites. It therefore Moktadir, N.A., Hasan, M.K. (2016): Unusual feeding behavior appears likely that some ingredient in the snake’s saliva, of the Checkered Keelback, Xenochrophis piscator in along with the stress of a predatory encounter, hastened Jahangirnagar University Campus, Savar, Dhaka, Bangladesh. the carp’s demise. Reptile Rap, South Asian Reptile Network 18: 32–33. In contrast, the attack on the catfish was at midbody Norval, G., Mao, J.J., Huang, S.C., Hou, C., Lee, J. (2010): and resulted in a multitude of perimortem, tooth- Xenochrophis piscator (Checkered Keelback). Predation. inflicted injuries to the fish (Fig. 1B, C). These were Herpetological Bulletin 112: 39–41. Parmar, D.S. (2018): Notes on the Checkered keelback, likely sustained during the attack and the attempts Xenochrophis piscator (Schneider 1799) in Gujarat, India. IRCF at swallowing, but no such injuries are visible on the Reptiles & Amphibians 25(2): 115–119. carp (Fig. 2C, D). In fact, the scaly covering of the Patel, K., Patel, K., Patel, H. (2017): Natural history notes. carp’s body may prevent serious external injuries from Xenochrophis piscator (Checkered Keelback). Diet and snakebite, although the carp also succumbed in the attack mortality. Herpetological Review 48: 869. by the snake. If this observed behavioural plasticity in Phansalkar, P.U., Gowande, G.G. (2017): Climbing behavior in prey handling is due to an ability of keelbacks to sense the Checkered Keelback or Asiatic Water Snake Xenochrophis differences in body covering on fish, then even though piscator (Schneider, 1799) (Colubridae: Natricinae) in the these two snakes did not get what they wanted, they Western Ghats, India. Russian Journal of Herpetology 24: 73–74. may be smarter than their failures suggest. Purkayastha, J., Kalita, J., Brahma, R.K., Doley, R., Das, M. (2018): A review of the relationships of Xenochrophis cerasogaster Acknowledgements. We thank Archana Prasad (Tribhuvan Cantor, 1839 (Serpentes: Colubridae) to its congeners. Zootaxa University, Kirtipur, Nepal) and Rahul Ranjan (Agriculture and 4514(1): 126–136. Forestry University, Bharatpur, Nepal) for helping us with the Schleich, S.H., Kästle, W. (Eds.) (2002): Amphibians and identification of the carp and the catfish, and Indraneil Das for his Reptiles of Nepal: Biology, Systematics, Field Guide. Ruggell, review of the manuscript. Liechtenstein, A.R.G. Gantner Verlag. 1201 pp. Shah, K.B., Tiwari, S. (2004) Herpetofauna of Nepal: a Conservation Companion. Kathmandu, Nepal, IUCN Nepal. 237 pp. Attempted predation and prey handling of fish by the Checkered Keelback 1077

Shrestha, S., Adhikari, P.L. (2016): Investigating temporal variation of water quality and benthic macroinvertebrates inTaudaha Lake, Kathmandu, Nepal. Journal of Water Resource and Protection 8: 1283–1296. Thai National Parks (2020): Checkered Keelback. Available at https://www.thainationalparks.com/species/fowlea-piscator. Accessed on 24 April 2020. Whitaker, R., Captain, A. (2004) Snakes of India: the Field Guide Book. Chennai, India, Draco Books. 495 pp.

Accepted by Anamarija Zagar