Journal of Threatened Taxa |
www.threatenedtaxa.org | 26 October 2022 | 14(10): 21928–21935
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
https://doi.org/10.11609/jott.7793.14.10.21928-21935
#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 agaur@ccmb.res.in
(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.
Editor: B.R. Latha,
Tamilnadu Veterinary Animal Sciences University,
Chennai, India. Date of publication: 26 October 2022
(online & print)
Citation: Vipin., T.R. Golla, V. Sharma, B.K. Kumar & A. Gaur (2022). Kleptoparasitic interaction between
Snow Leopard Panthera uncia
and Red Fox Vulpes vulpes suggested by
circumstantial evidence in Pin Valley National Park, India. Journal of Threatened
Taxa 14(10): 21928–21935. https://doi.org/10.11609/jott.7793.14.10.21928-21935
Copyright:
© Vipin et al. 2022.
Creative Commons Attribution 4.0 International License. JoTT allows
unrestricted use, reproduction, and distribution of this article in any medium
by providing adequate credit to the author(s) and the source of publication.
Funding: The
present study was part of the project on genetic diversity and conservation
status of Snow Leopards Panthera uncia in
India funded by the Department of Biotechnology, Government of India, New Delhi
vide Financial Grant Sanction Letter No.
BT/PR-14672/BCE/08/832/2010.
Competing interests: The authors declare no competing interests.
Author
details: Vipin
was working as a research associate II in the Snow Leopard project at LaCONES, Centre for Cellular and Molecular Biology,
Hyderabad, Telangana. Tirupathi Rao Golla was
a senior research fellow in the Snow Leopard project at LaCONES.
Vinita Sharma is an assistant
professor in the Department of Zoology, Central University of Jammu, Jammu and
Kashmir. Her area of research is related to animal taxonomy, systematics and
behavior, wildlife and conservation biology, human-wildlife conflict, wildlife
forensics, comparative anatomy and geometric morphometrics. Bheemavarapu Kesav Kumar
was working as a Junior Research Fellow in the Snow Leopard project at LaCONES. Ajay Gaur
is a senior principal scientist and was the principle investigator of the Snow
Leopard project at LaCONES, CSIR-CCMB, Hyderabad. The
main area of his research is conservation genetics of Indian endangered
species. His research focuses on the development and application of DNA markers
in population genetics, evolutionary genetics, conservation breeding and
wildlife forensics.
Author
contributions: V, VS, AG designed the study; V, VS,
TRG collected the data; V, VS, AG analysed the data
and wrote the paper; TRG, BKK did the proofreading; and AG supervised the
study.
Ethics
statement: All data and samples were collected
with due permissions of the state forest department. All ethical conditions
implemented by the project running institute have been followed.
Acknowledgements: We gratefully acknowledge the support of the director,
CCMB, and in-charge, LaCONES. We express our sincere
gratitude to Dr. Yash Veer Bhatnagar, senior
scientist, Nature Conservation Foundation, Mysore for critically reviewing and
giving his valuable suggestion about this work. We are thankful to Dr. Satish Kumar for his continued support throughout the
project. We would also like to thank the Forest Department, Himachal Pradesh
for providing the necessary permissions for carrying out the fieldwork for this
study.
INTRODUCTION
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).
RESULTS
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.
DISCUSSION
The evolution of the morphology and behaviour of participants may be influenced by
kleptoparasitism (Iyengar
2008). Among the varied types of responses of a host towards
a kleptoparasite, the host may retaliate if
the kleptoparasite is large
and can consume
a substantial part of its kill (Iyengar 2008). In such conditions, a host can injure or kill
the kleptoparasite (Iyengar 2008). There are many examples of it. The food of predatory birds is stolen by smaller birds (Meinertzhagen 1959), stealing of sea star’s food by whelks (Rochette
et al. 1995), and many
spiders are killed by larger hosts while
stealing their food (Whitehouse 1997). The present case suggests
an example of retaliatory behaviour in Snow Leopards in Pin Valley
National Park. A survey on interspecific killings among mammalian carnivores revealed that the
Red Fox was the most affected
victim as a kleptoparasite than other species of canids, mustelids, and felids to
the killer species belonging
to the families of felids and canids
(Palomares & Caro 1999). There
is one report of kleptoparasitism
by Snow Leopards from Hemis National Park, India
(Hunter 2015). The accessibility of alternative prey may be a decisive
factor for interspecific mammalian carnivore killing and consumption
(Macdonald 1977; Polis 1981; Ackerman et al. 1984; Stephenson et al. 1991; Palomares & Caro 1999) because
the diets of sympatric carnivores often overlap (Kruuk 1972; Delibes 1980; Major
& Sherburne 1987; Lindstrom
1989; Smits et al. 1989; Theberge & Wedeles 1989;
Paquet 1992; Mills & Biggs
1993; Palomares 1993; Okarma
1995; Okarma et al. 1997; Palomares
& Caro 1999). It has been reported that a killer species eats its prey completely,
partially, does not eat, or never eats (Palomares & Caro 1999). However,
the victim’s characteristics have been found to
make no difference in the consumption by a killer species (Palomares & Caro 1999). The other
records of a Red Fox as a kleptoparasite are from central and
southeastern Europe (Krofel
et al. 2019). Therefore, the
partially eaten-up blue sheep’s body by the Snow Leopard and the presence
of its alternative prey (the donkey carrion), other than the natural
prey (Thiele 2003), in a sympatric
habitat might also have
been the reasons for the uneaten
Red Fox’s body which is further indicative of retaliatory behaviour in Snow Leopards. The differentiation
between different larval
stages of blowflies was not
done here, so we gave the general time range (23–72 hours) for development from the first instar to the third
instar larvae. If we compare the
blowfly’s larval
development between the average temperature range
16°–22°C, then the time
taken for the appearance of the first instar to the
third instar comes in the range of 52–96 hours (Zhang et al. 2019). Therefore,
the larvae found on the body of the red fox might be 2–4 days
old. The insect’s
development varies at different temperatures
and so at different habitats. Hence, it is very difficult
to estimate the precise death
time of an animal through forensic entomology until specific studies on blowfly
development are available from
that area. Comprehensive knowledge
of kleptoparasitic interaction
between Snow Leopard and Red Fox as well as among other sympatric carnivores is very important in
Pin Valley National Park and
similar habitats across the country. Because any future
decline of an apex predator
may jeopardize the animals at lower trophic levels through the release of mesopredators (Castle et al.
2021).
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