Journal of Threatened Taxa | www.threatenedtaxa.org | 26 October 2022 | 14(10): 21928–21935
ISSN 0974-7907 (Online) | ISSN 0974-7893 (Print)
#7793 | Received 17 December 2021 | Final received 24 August 2022 | Finally accepted 29 September 2022
Kleptoparasitic interaction between Snow Leopard Panthera uncia and Red Fox Vulpes vulpes suggested by circumstantial evidence in Pin Valley National Park, India
5 firstname.lastname@example.org (corresponding author)
Abstract: In the present study, we describe an interspecific kleptoparasitic interaction between two sympatric mammalian carnivores in the high altitudinal Trans-Himalaya region of Himachal Pradesh, India. The study was based on the inferences drawn from the circumstantial evidence (direct and indirect) noticed in the study area in Pin Valley National Park. The inferences from the analysis of the evidence suggested the interaction between a Snow Leopard Panthera uncia, a Red Fox Vulpes vulpes, and a donkey. The arrangement of evidence in a sequential manner suggested that a donkey was killed by a Snow Leopard and a Red Fox stole the food from the carrion of the Snow Leopard’s prey. The Red Fox was killed by the Snow Leopard, which was caught while stealing. The present study represents an example of kleptoparasitic interaction between the Snow Leopard and the Red Fox. This study also proves that such interactions may cost the life of a kleptoparasite and supports the retaliation behaviour of Snow Leopards.
Keywords: Animal interaction, carnivore, mammals, prey, Trans-Himalaya.
Species interaction is an important component of an ecological community, which also works as a balancing force in it (Purves et al. 1992). Species interactions are direct (predation and interference competition) and indirect (trophic cascades and exploitative competition) (Case & Gilpin 1974; Estes & Palmisano 1974; Menge & Sutherland 1987; Paine et al. 1990; Bengtsson et al. 1994; Wootton 1994; Menge 1995). Kleptoparasitism is a form of indirect exploitative competition that refers to the stealing of any kind of resources by intra-or inter-specific members of a community (Webster & Hart 2006; Iyengar 2008). The member that steals the resource is called a kleptoparasite, and the other is the host. Kleptoparasitic interactions can influence the evolution of behavior and morphological traits of host and kleptoparasite (Iyengar 2008). The interspecific kleptoparasitic interactions may affect the entire ecosystem if the host, which also happens to be the apex predator, has a depleted prey base. Despite many studies carried out on species interactions, very little information on their effects, direct or indirect, on food webs involving terrestrial mammalian carnivores, particularly on keystone species, is available (Terborgh & Winter 1980; Pianka 1988; Pimm 1991; Strauss 1991; Terborgh 1992; McLaren & Peterson 1994; Palomares & Caro 1999). Therefore, studies throwing light on such interactions, more particularly involving apex predators, need to be carried out. Kleptoparasitism is a type of competition that may occur (intra- or inter-specific) between unrelated individuals (Iyengar 2008). The present study documents one such example of inter-specific kleptoparasitic interaction between two sympatric mammalian carnivore species. The two species are Snow Leopard and the Red Fox. The former is a keystone species of the high mountain ecosystem in the western Himalaya of India as it has a disproportionately larger impact on its ecosystem relative to its abundance (Bhatnagar et al. 2001; The Snow Leopard Conservancy 2007). The study was part of a larger study carried out by us on the genetic diversity and conservation status of Snow Leopards Panthera uncia in India from 2011 to 2013. Based on inferences drawn from the observations, we tried to show how interspecific kleptoparasitic interactions may affect the lives and behaviour of participants.
MATERIAL AND METHODS
The Pin Valley National Park (31.11°–32.03°N & 77.70°–78.10°E), Himachal Pradesh, India was the study site (Image 1). The National Park is situated in the Spiti Subdivision of Lahaul and Spiti district, a Trans-Himalayan cold desert mostly occurring above 3,200 m and a stronghold of Snow Leopards and Himalayan Ibex (Anonymous 2008). The kill sites were carefully marked for incidents, measured, and ad libitum information on the carcasses and spoor was recorded. Along with that, the data in the form of opportunistic evidence (direct and indirect) of suspected animal interactions were also recorded with details of time, date, and location. All evidence was photographed with the help of a DSLR camera (Sony alpha 35) and georeferenced with GPS (eTrex 10, Garmin). The evidence found in the study is denoted here by the numbers in brackets. The area between the entry point of the National Park and Thango (7.6 km) was walked on foot for three days from 1 to 3 May 2012 (Image 1). The natural animal trails were walked on foot for a total length of 15.68 km in 15.59 days hours, the details of which are as follows: May 1: 2.38 km from Ka Dogri to Gechang Base Camp (2.45 hours), May 2: 09.25 km to the west and back (8.05 hours), May 3: 4.05 km to the east and back (5.09 hours). It is to be noted that while returning to the base camp, the track followed was always 30–100 m apart from the track covered in the reverse direction. The scrapes and pugmarks were identified as per the ‘Snow Leopard Survey and Conservation Handbook’ (Jackson & Hunter 1995). The scats were identified as per the ‘Scat Survey Methodology for Snow Leopards’ (Janecka et al. 2008). The flies were identified using morphological identification keys by Szpila (2009). The beetle identification was carried out using the Encyclopaedia of Life’ (https://eol.org/pages/3383922/media).
On May 2, 2012, after walking around 3.4 km from the base camp at Gechang, a strong smell of something rotting attracted us to the carrion of a donkey (1) (Image 2A, 3A). A scat, possibly of Red Fox Vulpes vulpes or a Snow Leopard (2), was lying nearby (approx. 6 m) (Image 2A, 3B). About 30m away from the donkey carrion, a Red Fox was lying dead on the bank of the Pin River (3) (Image 2A, 3C). We labelled the area between the dead donkey and the Red Fox as an "incident site" near (approx. 2 m) the dead Red Fox was a scapula bone from the same dead donkey (4) and a scat (5) suspected of a Snow Leopard (Image 2A, 3D). The pugmarks of Snow Leopards were found about 120 m before the incident site (6) (Image 2A, 3E). There were wounds on the left lateral side of the Red Fox, from the neck to the mid-body, and flies were also found sitting on and around its body (Image 3F). On close observation of the fox’s body, pale-yellow maggots and beetles were found on the left side of the mouth (Image 3G). Some relevant observations made about the presence of Snow Leopards in Pin Valley National Park are as follows: On May 1, many pugmarks of suspected Snow Leopards were found on the bank of the Pin River about 1 km east of the base camp (7) (Image 2B, 4A). On May 3, scrapes and urine (8) (Image 4B) of a suspected Snow Leopard were found on the slope near the base camp. Further investigation led us to an overhang resting site (9) where pugmarks of a suspected Snow Leopard (10) and exposed bone (11) were found inside it (Image 4C). Further tracing the pugmarks (12, 13, 14) (Image 4D), a freshly killed Blue Sheep (15) (Image 4E) (without any larvae and smell) was found over the den on a ridge (approx. 300 m above the Pin River). Nearby (approx. 6 m away), we found a scat, suspected to be of a Snow Leopard (16) (Image 4F). The inferences drawn from the above evidence, if connected in the correct order, may help draw a sequence of events that might have taken place between the animals involved. Flies of blue metallic color were found on and around the Red Fox's body. These were identified as blowflies. The blowflies feed on carrion and belong to the family Calliphoridae of class Insecta (ITIS 2008). A large number of larvae were present on the body of the Red Fox and no smell was coming out of it, indicating it was in the bloated stage of decomposition (Matuszewski et al. 2008). The blowflies lay eggs on carrion and, after that, the development of larval (pale yellow) stages, from the first instar to the third instar, generally takes place between 23 to 72 hours (Jordan et al. 2018). The beetle on the Red Fox's body identified, on morphological resemblance, as Thanatophilus minutus. Thanatophilus minutus is also a carrion beetle having distribution in Himachal Pradesh and is known to arrive on carrion after the blowflies (Ruzicka et al. 2011; Tariq 2020). Thanatophilus species larvae are darker in colour (Diaz-Aranda 2013) and did not match, in morphology, to the larvae found on the Red Fox. The donkey's carrion had a foul odor, no insect larvae were found on it, and the meat was dried. This indicated that it might either be in the active or the advanced stage of decomposition (Matuszewski et al. 2008). All this evidence proved that the donkey was killed earlier than the Red Fox. The incidents that happened, point towards the involvement of three species, i.e., a donkey, a Red Fox, and a Snow Leopard. There is no doubt about the donkey and Red Fox, as their carcasses were present. The pugmarks (6) (Image 2A; near the incident site), scat (5) of uniform diameter of 2.0 cm, segmented, with blunt ends, and having the presence of hairs in it point towards the involvement of a Snow Leopard. A Snow Leopard scat has an average diameter of 1.8 cm, which is uniform along its length, having constrictions and blunt ends (Janecka et al. 2008). The pugmarks (6) were identified as those of a Snow Leopard according to Jackson & Hunter (1995), which is the only large cat present in that habitat (Anonymous 2008). The shape and size of the scat (5) confirm the presence of Snow Leopard in and around the incident site. The Snow Leopard pugmarks were found frequently throughout the Pin Valley National Park on 1 & 3 May 2011. The pugmarks found near the bank of the Pin River on May 1 were found to be of Snow Leopard (Figur 4A). All the pugmarks and scrapes found on May 03 were from Snow Leopard. The scat ‘16’ was confirmed to be of a Snow Leopard through the genetic analysis done at our laboratory (study unpublished). The Grey Wolves and Brown Bears are known as kleptoparasites of the Snow Leopard (Hunter 2015). But no signs of Wolf or Brown Bear pugmarks were found on the tracks we covered between 1 & 3 May in the valley. A full-grown Snow Leopard hunts a large prey every 10–15 days and remains near it for about 3–7 days until it is finished (McCarthy & Chapron 2003; Hunter 2015). The presence of scat (5), which only could be of a Snow Leopard, as per its shape and measurements, in the vicinity of the dead donkey and the Red Fox, points out that, most probably, both were killed by the Snow Leopard at different times. The presence of donkey scapula (4) near the body of the dead Red Fox indicates that it was stealing the meat from the dead donkey during which it was killed by the Snow Leopard. On arranging all the above findings, the inferences can be drawn from the circumstantial evidence that a donkey was killed by a Snow Leopard. Since a Snow Leopard takes 3–7 days to consume its prey, the Red Fox was stealing the food from the Snow Leopard’s kill. At some time, the Red Fox was caught stealing food by the Snow Leopard and was killed. There are records of a Red Fox being accidentally killed by a Snow Leopard (Hunter 2015). The present findings point toward the first incident of kleptoparasitism by a Red Fox on a Snow Leopard in Pin Valley National Park, Himachal Pradesh. This incident of kleptoparasitic interactions between two sympatric mammalian carnivores also reveals the retaliatory behaviour of the Snow Leopard. The retaliatory behavior may be advocated as the Red Fox’s body remained uneaten even after 23–72 hours of being killed as suggested by the presence of blowflies larval stages.
Ackerman, B.B., F.G. Lindzey & T.P. Hemker (1984). Cougar food habits in southern Utah. Journal of Wildlife Management 48: 147–155.
Anonymous (2008). Fauna of Pin Valley National Park. Conservation Area Series 34: 1–147 Zoological Survey of India, Kolkata.
Bengtsson, J., M.T. Fagerstro & H. Rydin (1994). Competition and coexistence in plant communities. Trends in Ecology & Evolution 9: 246–250.
Bhatnagar, Y.V., V.B. Mathur & T. McCarthy (2002). “A regional perspective for Snow Leopard conservation in the Indian Trans-Himalaya”, pp. 25–47. In: Summit, T. McCarthy & J. Weltzin (eds.). Contributed Papers to the Snow Leopard Survival Strategy. International Snow Leopard Trust, Seattle, Wash, USA.
Case, T.J. & M.E. Gilpin (1974). Interference competition and niche theory. Proceedings of the National Academy of Sciences of the USA 71: 3073–3077.
Castle, G., D. Smith, L.R. Allen & B.L. Allen (2021). Terrestrial mesopredators did not increase after top-predator removal in a large-scale experimental test of mesopredator release theory. Scientific Reports 11: 18205. https://doi.org/10.1038/s41598-021-97634-4
Delibes, M. (1980). El lince ibe´rico: ecologı´a y comportamiento alimenticios en el Coto de Don˜ana, Huelva. Don˜ana Acta Vertebrata 7: 1–128.
Díaz-Aranda, L.M., D. Martín-Vega, B. Cifrián & A. Baz (2013). A preliminary larval identification key to European Coleoptera of forensic importance. Poster.
Estes, J.A. & J.F. Palmisano (1974). Sea otters: their role in structuring near shore communities. Science 185: 1058–1060.
Hunter, L. (2015). Wild Cats of the World. Bloomsbury Natural History. An imprint of Bloomsbury Publishing Plc., 240 pp.
ITIS (2008). Calliphoridae. Integrated Taxonomic Information System. Retrieved from Integrated Taxonomic Information System. Retrieved on 31 May 2008.
Iyengar, E.V. (2008). Kleptoparasitic interactions throughout the animal kingdom and a re-evaluation, based on participant mobility, of the conditions promoting the evolution of kleptoparasitism. Biological Journal of the Linnean Society 93: 745–762.
Jackson, R. & D.O. Hunter (1995). Snow Leopard Survey and Conservation Handbook (First edition). International Snow Leopard Trust Report, 120 pp.
Janecka, J., R. Jackson & B. Munkhtog (2008). Scat Survey Methodology for Snow Leopards. https://snowleopardconservancy.org/pdf/dna/methodology.pdf
Jordan A., N. Khiyani, S.R. Bowers, J.J. Lukaszczyk & S.P. Stawicki (2018). Maggot debridement therapy: a practical review. International Journal Academic Medicine 4(1): 21.
Krofel, M., T. Skrbinsec & M. Mohorovic (2019). Using video surveillance to monitor feeding behaviour and kleptoparasitism at Eurasian lynx kill sites. Folia Zoologica 68: 274–284.
Kruuk, H. (1972). The Spotted Hyena: A Study of Predation and Social Behavior. University of Chicago Press, Chicago, 388 pp.
Lindstrom, E.R. (1989). The role of medium-size carnivores in the Nordic boreal forest. Finnish Game Research 46: 53–63.
Macdonald, D.W. (1977). On food preferences in the red fox. Mammal Review 7: 7–23.
Major, J.T. & J.A. Sherburne (1987). Interspecific relationships of coyote, bobcats, and red foxes in western Maine. Journal of Wildlife of Management 51: 606–616.
Matuszewski, S., D. Bajerlein, S. Konwerski & K. Szpila (2008). An initial study of insect succession and carrion decomposition in various forest habitats of Central Europe. Forensic Science International 180(2–3): 61–69.
McCarthy, T.M. & G. Chapron (2003). Snow Leopard Survival Strategy. ISLT and SLN, Seattle, USA.
McLaren, B.E. & R.O. Peterson. (1994). Wolves, moose, and tree rings on Isle Royale. Science 266: 1555–1558.
Meinertzhagen R. (1959). Pirates and predators. Edinburgh: Oliver and Boyd, 230 pp.
Menge, B.A. (1995). Indirect effects in marine rocky intertidal interactions webs: patterns and importance. Ecological Monographs 65: 21–74.
Menge, B.A. & J.P. Sutherland (1987). Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. American Naturalist 130: 730–757.
Mills, M.G.L. & H.C. Biggs (1993). Prey apportionment and related ecological relationships between large carnivores in Kruger National Park. Symposium of Zoological Society of London 65: 253–268.
Okarma, H. (1995). The trophic ecology of wolves and their predatory role in ungulate communities of forest ecosystems in Europe. Acta Theriologica 40: 335– 386.
Okarma, H., W. Jedrzejewski, K. Schmidt, R. Komalczyk & B. Jedrzejewska (1997). Predation of Eurasian lynx on roe deer and red deer in Bialowieza Primeval Forest, Poland. Acta Theriologica 42: 203–224.
Paine, R.T., J.T. Wootton & P.D. Boersma (1990). Direct and indirect effects of peregrine falcon predation on seabird abundance. Auk 107: 1–9.
Palomares, F. (1993). Opportunistic feeding of the Egyptian mongoose, Herpestes ichneumon (L.), in southwestern Spain. Revue Ecologie (Terre Vie) 48:295–304.
Palomares, F. & T.M. Caro (1999). Interspecific Killing among Mammalian Carnivores. American Naturalist 153: 492–508.
Paquet, P.C. (1992). Prey use strategies of sympatric wolves and coyotes in Riding Mountain National Park, Manitoba. Journal of Mammalogy 73: 337–343.
Pianka, E.R. (1988). Evolutionary Ecology. 4th ed. Harper & Row, New York, 468 pp.
Pimm, S.L. (1991). The Balance of Nature? University of Chicago Press, Chicago, 448 pp.
Polis, G.A. (1981). The evolution and dynamics of intraspecific predation. Annual Review of Ecology and Systematics 12: 225–251.
Purves, W.K., G.H. Orians & H.C. Heller (1992). Life: The Science of Biology. Sinauer, Sunderland, MA.
Rochette, R., S. Morissette & J.H. Himmelman (1995). A flexible response to a major predator provides the whelk Buccinum undatum L. with nutritional gains. Journal of Experimental Marine Biology and Ecology 185: 167–180.
Ruzicka, J., H. Sipkova & J. Schneider (2011). Notes on carrion beetles (Coleoptera: Silphidae) from India. Klapalekiana 47: 239–245.
Smits, C.M.M., B.G. Slough & C.A. Yasui (1989). Summer food habits of sympatric arctic foxes, Alopex lagopus, and red foxes, Vulpes vulpes, in the northern Yukon Territory. Canadian Field-Naturalist 103: 363–367.
Stephenson, R.O., D.V. Grangaard & J. Burch (1991). Lynx (Felis lynx) predation on red foxes (Vulpes vulpes) caribou (Rangifer tarandus) and dall sheep (Ovis dalli). Canadian Field-Naturalist 105: 255–262.
Strauss, S.Y. (1991). Indirect effects in community ecology: their definition, study and importance. Trends in Ecology & Evolution 6: 206–210.
Szpila, K. (2009). Key for identification of European and Mediterranean blowflies (Diptera, Calliphoridae) of forensic importance, Nicolaus Copernicus University, 18 pp.
Tariq, A.M. (2020). The role of blue bottle fly in the science of crime analysis: a review. International Journal of Botany Studies 5(2): 25–28.
Terborgh, J. (1992). Maintenance of diversity in tropical forests. Biotropica 24: 283– 292.
Terborgh, J. & B. Winter (1980). Some causes of extinction, pp. 119–134. In: Conservation biology: an evolutionary-ecological perspective, eds Soulé ME, Wilcox BA. Sunderland, MA: Sinauer.
The Snow Leopard Conservancy (2007). Mountain Cultures, Keystone Species: Exploring the Role of Cultural Keystone Species in Central Asia. Final Report (Grant 2005–2019) submitted to The Christensen Fund by SLC/ Cat Action Treasury, Sonoma, California. 47 pages.
Theberge, J.B. & C.H.R. Wedeles (1989). Prey selection and habitat partitioning in sympatric coyote and red fox populations, southwest Yukon. Canadian Journal of Zoology 67: 1285–1290.
Theile, S. (2003). Fading Footsteps: the Killing and Trade of Snow Leopards. TRAFFIC International.
Webster, M.M. & P.J.B. Hart (2006). Kleptoparasitic prey competition in shoaling fish: effects of familiarity and prey distribution. Behavioral Ecology 17: 959–964.
Whitehouse, M.E.A. (1997). The benefits of stealing from a predator: foraging rates, predation risk, and intraspecific aggression in the kleptoparasitic spider Argyrodes antipodiana. Behavioral Ecology 8: 663–667.
Wootton, J.T. (1994). Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75: 151–165.
Zhang, Y., Y. Wang, J. Sun, G. Hu, M. Wang, J. Amendt & J. Wang (2019). Temperature dependent development of the blow fly Chrysomya pinguis and its significance in estimating postmortem interval. Royal Society Open Science 6: 190003. https://doi.org/10.1098/rsos.190003