Journal of Threatened
Taxa | www.threatenedtaxa.org | 26 February 2023 | 15(2): 22606–22610
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8172.15.2.22606-22610
#8172 | Received 02
September 2022 | Final received 31 January 2023 | Finally accepted 07 February
2023
Differential kleptoparasitic
interactions of Himalayan Vulture Gyps himalayensis
with conspecifics and heterospecifics during various
stages of breeding
Hameem Mushtaq Wani
Department of Zoology, Central
University of Kashmir, Ganderbal, Jammu and Kashmir
191201, India.
Abstract: Reports of kleptoparasitic
events involving Gyps himalayensis (Himalayan
Vulture) are limited. In this article we document intraspecific and
interspecific kleptoparasitic interactions at nesting
sites, and analyse factors influencing this behaviour. The study was carried out at Hirpora
Wildlife Sanctuary of Kashmir Himalaya, at an elevation of about 2,546 m. We
observed 61 instances of food theft involving conspecifics (n = 12) and heterospecifics (n = 49). The highest number of incidents
were observed during the chick rearing period (n=40), followed by incubation (n
= 10) and pre-laying periods (n = 5). We observed the highest number of attacks
at nesting sites (n = 30) and the lowest in flight (n = 9).
Keywords: Himalaya, Hirpora
Wildlife Sanctuary, Kashmir, Kleptoparasitism, nest,
vulture.
Editor: Bahar
S. Baviskar, Wild-CER, Nagpur, India. Date of publication: 26 February
2023 (online & print)
Citation: Wani,
H.M. (2023).
Differential kleptoparasitic interactions of
Himalayan Vulture Gyps himalayensis with
conspecifics and heterospecifics during various
stages of breeding. Journal of Threatened Taxa 15(2): 22606–22610. https://doi.org/10.11609/jott.8172.15.2.22606-22610
Copyright: © Wani 2023. 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: None.
Competing interests: The author
declares no competing interests.
Author details: Hameem Mushtaq
Wani did his PhD programme from University of Kashmir, Srinagar.
His doctoral thesis majorly
focussed on bioecology and conservation status of vultures in Hirpora Wildlife Sanctuary of Kashmir Himalaya. He is currently
working as a teaching faculty
in the Department of Animal Science (Zoology), Central University of Kashmir, India.
Acknowledgements: Author is grateful to the
Department of Wildlife Protection, Government of Jammu & Kashmir, for
providing necessary permission to work in Hirpora
Wildlife Sanctuary.
INTRODUCTION
Kleptoparasitism is the acquisition of resources
by theft (Brockmann & Barnard 1979; Hadjichrysanthou et al. 2018) such as prey or other
materials that require time and effort to obtain. The practice is not without
risk, since a kleptoparasite might be injured by its victim if it defends its
prey (Iyengar 2008; Hadjichrysanthou
et al. 2018). This behaviour is relatively widespread
among birds, particularly sea birds. Kleptoparasitic
interactions involving vultures, for example the Lammergeier Gypaetus barbatus and Black Vulture Aegypius monachus,
have been reported in the literature (Margalida &
Heredia 2002). Data on this behaviour at nesting
zones, however, is limited. This may be due to the fact that while vultures
congregate at carcasses (Mundy et al. 1992) they carry food in their crop to
the nest where chicks are fed via regurgitation (Mushtaq 2020), making theft by
other birds difficult.
Himalayan Vultures feed on carcasses
of dead animals (Image 2) (Wani et al. 2021) along
with other scavengers including large billed crows and raven (Navaneethan et
al. 2015). The availability of carrion can vary spatially and seasonally,
thereby playing an important part in movement and distribution of species
feeding on it (Wani et al. 2020). Himalayan vultures
show intensive parental care during chick rearing periods. In this article, we
documented intraspecific and interspecific kleptoparasitic
interactions of Himalayan vulture at nesting sites, and analysed
the factors influencing this behaviour.
MATERIALS AND METHODS
Study area
Hirpora Wildlife Sanctuary spreads over
an area of 341 km2 in Shopian District,
Kashmir. At an altitude of 2,546 m, the sanctuary is located between 33.3955 oN & 74.3940 oE.
It has forests, pastures, scrub land, waste land water bodies. To the north,
the sanctuary is bounded by Lake Gumsar, to the east
by Rupri, to the south by Saransar,
to the west by the Pir Panjal
pass and to northeast by Hirpora village (Wani et al. 2020) (Image 1). The area is renowned for its
rich floral and faunal diversity. The main faunal elements of the sanctuary
include- Pir Panjal Markhor Capra falconeri,
Himalayan Musk Deer Moschus leucogaster, Himalayan Black Bear Ursus
thibetanus, Himalayan Brown Bear Ursus arctos,
Leopard Panthera pardus,
Red Fox Vulpes vulpes, and Tibetan Wolf Canis lupus. The vegetation of the sanctuary
is divided into mixed coniferous forests, deciduous subalpine scrub forests and
subalpine pastures. The coniferous forests are dominated by Kail
pine, the sub alpine forests are dominated by fir while the deciduous subalpine
scrub forests are dominated by Himalayan Birch Betula utilis
and Juniper Juniperus communis
(Wani et al. 2021).
Methods
Field work was undertaken in Hirpora Wildlife Sanctuary from June 2019 to May 2020.
Observations on food stolen, species involved and situation in which they
occurred (in flight, at nest and on feeding site) were made during pre-laying,
incubation and chick rearing period with the help of 10X binocular.
Observations were made from vantage points (at a distance of about 300–400 m)
that allowed a good view of nesting and feeding sites. In all intraspecific
interactions observed, we recorded the individuals’ age which was determined by
Grimmett et al. (2016).
Data analysis
Basic statistics such as, mean
and standard deviation were calculated for all the variables and were given as
X±SD. Statistical analysis were performed by using Windows based statistical
packages- Micorsoft Excel and MINITAB (Ryan et al.
1992). A non-parametric test, Kruskal-Wallis one way ANOVA was used for testing
the null hypothesis at p <0.05.
RESULTS
We observed 61 Himalayan Vulture
interactions of food theft, 12 with conspecifics and 49 with heterospecifics. These interactions varied among different
sites and seasons (Table 4, Table 5). The various heterospecifics
involved in these interactions included Bearded Vulture Gypaetus
barbatus (n = 7), Common Raven Corvus corax (n = 22), Large-billed Crow Corvus
macrorhynchos (n = 15), and House Crow Corvus splendens (n
= 5).
Interactions with conspecifics
We observed a total of 12
interactions of Himalayan Vulture with conspecifics (Table 2). In eight
interactions adult Himalayan vultures acted as kleptoparasites, and in four
interactions sub-adult vultures acted as kleptoparasites. During the former
case, four sub-adults and two adults acted as hosts whereas in the latter case,
one adult and one sub-adult acted as hosts. All these interactions with conspecifics
were statistically significant (H = 7.89; DF = 01; P <0.05) (Table 2).
Interactions with heterospecifics
We observed a total of 49
interactions of Himalayan Vulture with heterospecifics.
All these interactions were statistically significant (H = 7.32; DF = 03; P
<0.05). In 07 of these interactions, Gypaetus
barbatus acted as kleptoparasite with 05 such interactions in which
sub-adult Himalayan vulture acted as host. In rest of the two interactions,
adult Himalayan vulture acted as host. Rest of the interactions involved
different corvid species including- Common Raven Corvus
corax (n = 22), Large-billed Crow Corvus macrorhynchos
(n = 15), and House Crow Corvus splendens (n = 05). In 15 interactions with Common
Raven, sub-adult Himalayan vulture individuals acted as hosts and in seven such
interactions, adult Himalayan Vulture individuals acted as hosts. Similarly, in
eight interactions with Corvus macrorhynchos, sub-adult Himalayan Vulture and in seven
such interactions, adult Himalayan vulture acted as hosts. Among interactions
with Corvus splendens,
three interactions involve sub-adult Himalayan Vulture, and two
interactions involve adult individuals as hosts (Table 1).
Interactions during different
periods
Highest number of attacks from
both conspecifics and heterospecifics were observed
during chick rearing period (n = 40) followed by incubation period (n = 10) and
pre-laying period (n = 5). In chick rearing period, 90% attacks were defended
successfully whereas in incubation period, only 62.5% of the attacks were
defended successfully. However, during pre-laying period, all attacks from
conspecifics and heterospecifics were defended
successfully. The percentage of defended and non-defended attacks were
statistically significant (H = 8.16; DF = 02; P <0.05) (Table 3).
Interactions at different sites
The number of interactions of
Himalayan Vulture with its conspecifics and heterospecifics
at different sites were statistically significant (H = 8.14; DF = 02; P
<0.05). We observed highest number of attacks at nesting site (n = 30) and
lowest number of attacks in flight (n = 09). A total of 22 attacks were
observed at feeding sites. Among 30 attacks, at nest site, 29 were defended
successfully. On the other hand, among 22 attacks at feeding sites, only 15
were defended and rest (31.81%) were not defended (Image 2). Out of nine
attacks in flight, seven were defended and in two attacks, kleptoparasite
remained successful in taking away the food from Himalayan Vulture (Table 4).
DISCUSSION
Kleptoparasitism occurs when there is an
association between species. However, it is equally obvious, that kleptoparasitism does not always occur when two species are
found together. Rather, there are various ecological and behavioural
conditions that make kleptoparasitism particularly
likely. These include- large concentration of host (John & Lee 2019), large
quantities of food (Mullers & Amar 2015) large and high quality food items
(Iyengar 2008), predictable food supply (Dekker et
al. 2012), visibility to food items (John & Lee 2019), food shortage behaviour of parasite (Mullers & Amar 2015), behaviour and habitat of host (Hamilton 2002).
Our results suggested that the Corvus corax, C. macrorhynchos and C. splendens
due to their little chance for foraging at carcass as compared to vultures, are
making use of the spatial and temporal predictability of food resources by
becoming kleptoparasites (Fisher 1985). Most of the thefts suffered at the nest
by kleptoparasites took place during chick rearing, a period when food items
often accumulate at the nest sites. Thefts in flight occurred during pre-laying
and incubation period, a time when food availability is reduced and when
weather may greatly limit the activities of foraging and locating food. For
those age groups (principally <3 years, i.e., sub-adults) that are more dependent
on predictable food sources such as feeding stations (Heredia 1991), this might
be a foraging strategy used much more regularly. These results are in agreement
with the idea that immature or inexperienced birds may compensate for their
less effective foraging abilities by kleptoparasitism
(Margalida & Bertran
2003). To the contrary, kleptoparasitism by adults
could be an opportunistic foraging behaviour. Our
observations were done in flight, in addition to nests and feeding sites. This
accounts for the fact that breeding adults were the host bird in 79% of all
observed events.
As a result of the cost/benefit
rate, two factors would determine that the species that attempted stealing
would resort to this indirect strategy: the territorial behaviour
of the host species (Margalida & Bertran 2000) and the accumulation of food resources in
nesting area.
Dominance of adults over immature
is a well-documented phenomenon in raptors (Moreno-Opo
et al. 2020), but a reverse dominance pattern also has been observed (Rodríguez-Estrella
& Rivera-Rodriguez 1992). In the case of conspecifics, plumage colouration of Himalayan vulture adults could act as a
status signal (Negro et al. 1999). This signal could be used by territorial
adults to displace other immature Himalayan Vultures not by attacking them, but
simply by signalling their status while approaching
them (Bautista et al. 1998).
On the other hand, the Himalayan
Vulture having low wing loading and its large wingspan give this species great
dominance in flight (Donázar et al. 1993) and make it
difficult for an opponent to steal food successfully. In the case of
conspecifics, the fact that younger birds are less skilful
in flight would mean that they would be less successful in actions of direct
piracy, so that the energetic cost of those attempts might be greater than the
likely benefits obtained from those actions (Fisher 1985; Moreno-Opo et al. 2020).
The Himalayan Vulture’s attacks
of intruders in the vicinity of the nest throughout the breeding season (Margalida & Bertran 2000)
would act as deterrent and would make food at nest the least convenient for
stealing. The success in aggressive encounters appears determined by the body
size and condition, and the previous possession of the disputed resource
(Bautista et al. 1998). In contrast, those species with higher aerial
maneuverability but with smaller size, such as ravens, would have to focus
their actions at the nest, where prey remains also accumulate. Obtaining prey
remains there may be less costly for those birds: (1) adults are gradually less
often present at the nest as the breeding season progress (Margalida
& Bertran 2000) and (2) prey items present in the
nest have a higher meat content as consequence of differential requirements in
nutrients for the chick (Margalida & Bertran 2001).
Table 1. Kleptoparasitic
interactions of Gyps himalayensis with heterospecifics in Hirpora
Wildlife Sanctuary.
|
Kleptoparasite |
Host |
|
|
Gyps himalayensis (Subadult) |
Gyps himalayensis (Adult) |
|
|
Gypaetus barbatus |
05 |
02 |
|
Corvus corax |
15 |
07 |
|
Corvus macrorhynchos |
08 |
07 |
|
Corvus splendens |
03 |
02 |
|
Kruskal-Wallis one way ANOVA |
H = 7.32; DF = 03; P <0.05 |
|
Table2. Kleptoparasitic
interactions of Gyps himalayensis with
conspecifics in Hirpora Wildlife Sanctuary.
|
|
Host |
Kleptoparasite |
|
|
|
Gyps himalayensis |
Subadult |
Adult |
|
|
|
Kleptoparasite |
Sub-adult (04) |
02 |
02 |
|
|
Adult (08) |
06 |
02 |
|
|
|
Kruskal-Wallis ANOVA |
H = 7.89; DF = 01; P <0.05 |
|||
Table 3. Percentage of Kleptoparasitic attacks defended and not defended by Gyps
himalayensis during Pre-laying, Incubation and
Chick rearing period in Hirpora Wildlife Sanctuary.
|
Period |
No. of attacks |
Percentage of attacks |
|
|
Defended (%) |
Non-defended (%) |
||
|
Pre-laying |
05 |
5(100) |
0(0.0) |
|
Incubation |
16 |
10(62.5) |
6(37.5) |
|
Chick rearing |
40 |
36(90) |
4(10.0) |
|
Kruskal-Wallis one way ANOVA |
H = 8.16; DF = 02; P <0.05 |
||
Table 4. Kleptoparasitic
interactions of Gyps himalayensis with
conspecifics and heterospecifics in flight, at nest
and at feeding site.
|
Place/Site |
Thefts |
Defended |
Non-defended |
|
Flight |
09 |
07 |
02 |
|
Nest |
30 |
29 |
01 |
|
Feeding site |
22 |
15 |
07 |
|
Kruskal-Wallis one way ANOVA |
H = 8.14; DF = 02; P <0.05 |
||
Table 5. Kleptoparasitic
interactions of Gyps himalayensis with
conspecifics and heterospecifics during different
seasons.
|
Season |
Attacks |
Attacks defended (%) |
Attacks not defended (%) |
|
Winter |
28 |
92.85 |
7.15 |
|
Spring |
12 |
83.33 |
16.67 |
|
Summer |
14 |
57.14 |
42.86 |
|
Autumn |
07 |
71.42 |
28.58 |
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