Journal of
Threatened Taxa | www.threatenedtaxa.org | 26 May 2024 | 16(5): 25129–25136
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8898.16.5.25129-25136
#8898 | Received 02 January 2024 | Final received 15 March 2024 | Finally
accepted 05 April 2024
Small Wild Cats Special Series
Shomita Mukherjee 1, Arati
Ramdas Gawari 2, Kartik Pillai 3,
Pankaj Koparde 4, P.V. Karunakaran
5 & Nayan Khanolkar
6
1,5 Sálim Ali Centre
for Ornithology and Natural History, Anaikatty,
Coimbatore, Tamil Nadu 641108, India.
2 Post Barav, Shivneri Fort Road, Junnar, Pune, Maharashtra 410502, India.
3 Nav Krushnai CHS-HSG, New Ayre Road, Dombivli (East), Maharashtra 421201, India.
4 Department
of Environmental Studies, Dr. Vishwanath Karad MIT World Peace University, Kothrud, Pune,
Maharashtra, 411038, India.
6 B11, Om co.op society, Devil chowk, Shastri Nagar, Dombivli west, Thane, Maharashtra 421202, India
1 shomita.sacon@wii.gov.in
(corresponding author), 2 aratiarg@gmail.com, 3
pillai.kartik439@gmail.com,
4 pankaj.koparde@mitwpu.edu.in,
5 karunakaran.pv@gmail.com,
6 nayankhanolkar@gmail.com
Editor: Angie Appel, Wild Cat Network, Germany.
Date of publication: 26 May 2024 (online & print)
Citation: Mukherjee,
S., A.R. Gawari, K. Pillai, P. Koparde,
P.V. Karunakaran & N. Khanolkar
(2024).
Diet of Rusty-spotted Cat Prionailurus rubiginosus (I. Geoffroy Saint-Hilaire, 1831)
(Mammalia: Carnivora: Felidae) in Sanjay Gandhi National Park, Mumbai, India. Journal of Threatened Taxa 16(5): 25129–25136. https://doi.org/10.11609/jott.8898.16.5.25129-25136
Copyright: © Dhyani et al. 2024. 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:
Maharashtra Forest Department, (Ref: O.N. Room-3/Project/2229/Year 2016-17; O.N. Room-8/V.P./Research/Ch 01-B/2596/Year 2017-18; O.N.
Room-8/V.P./Research/Ch 01-B/Year 2018-19).
Competing interests: The authors declare no competing interests.
Author details: Shomita Mukherjee is a senior principal scientist
at the Sálim Ali Centre for Ornithology and Natural
History at Coimbatore, Tamil Nadu in the Division of Conservation Biology. Her
current work focuses on the ecology of small cats. Arati Gawari completed her master’s
dissertation on this project from VP.M’s B.N. Bandodkar College of Science, Thane. Kartik Pillai is a B.Tech Biotechnology graduate and is currently
working as a Naturalist for Exotic Hospitality Pvt. Ltd, Nagpur in Tathastu Resorts at Pench
National Park, Madhya Pradesh. Pankaj
Koparde is currently an assistant professor
with the Department of Environmental Studies, MIT-WPU Pune. His core expertise
is in subjects such as aquatic ecology, urban ecology, biogeography,
biodiversity informatics, and science communication. He primarily works on owls
and dragonflies. P.V. Karunakaran is a landscape ecologist working as a
senior principal scientist at Sálim Ali Centre for
Ornithology and Natural History (SACON). His current areas of research include
conservation and management of natural resources, protected area management,
community participation in biodiversity conservation, plant taxonomy and GIS
and Remote Sensing. Nayan Khanolkar is
an educator, naturalist and wildlife photographer. His current assignments
include documenting urban leopards, participating in citizen science programs
and teaching photography at various colleges across Maharashtra.
Author contribution: SM, NK and PVK conceptualised the study. PK, ARG, KP, SM and PVK analysed and mapped the samples. SM wrote the manuscript. PVK, PK and NK reviewed and edited the manuscript.
Acknowledgements: We thank the
Maharashtra Forest Department and the entire staff of Sanjay Gandhi National
Park for funding the project and for the support extended throughout the study
period. We are grateful to the former and current directors, as well as all
faculty and staff of SACON for their support during the project period. We are
obliged to Robin V.V. and members of IISER Tirupati for supporting the
molecular analysis in their laboratory facilities. We thank Nandini Rajamani for the discussions and support during the
analysis, and much appreciate the effort of all reviewers. Their comments
helped significantly to improve the manuscript.
Abstract: The 103.68
km2 Sanjay Gandhi National Park (SGNP), Mumbai, exists amidst human
densities that figure among the highest in the world. The rich biodiversity of
SGNP includes the Rusty-spotted Cat Prionailurus
rubiginosus, endemic to India, Sri Lanka, and
Nepal, and categorised as ‘Near Threatened’ on the IUCN Red List. Little is
known about its ecology and the dynamics of its coexistence with the other
small carnivores in SGNP. We conducted a study with citizen volunteers to
explore the diet of the Rusty-spotted Cat and other sympatric small carnivores
in SGNP and in the adjoining human-dominated areas of Yeur
village, Shivaji Nagar, Dahisar Quarry, and Aarey Milk Colony. After initial training, the volunteers
collected scat samples from all forest ranges in SGNP and the surrounding areas
outside, following defined protocols. Seventy-eight scat samples were analysed
for species assignments using standardised molecular techniques, felid-specific
primers, and DNA sequencing, and 24 were identified as of the Rusty-spotted
Cat. The contents of the samples were examined under a microscope to identify
prey remains. Results were presented as the mean number of scat samples containing
remains of specific taxa with 95% Confidence Intervals. Diet estimated from 22
Rusty-spotted Cat scat samples and 52 samples of other small carnivores
revealed rodents to be the major prey of the entire group. However, a higher
proportion of Rusty-spotted Cat scat samples had remains of rodents (95%) and
reptiles (6%) as compared to samples of other small carnivores, i.e., 79% with
rodent remains and none with remains of reptiles. On the other hand, a lower
proportion of Rusty-spotted Cat scat samples had remains of insects (14%),
plant matter (9%), and birds (5%) than samples of other small carnivores (40%
plant matter, 38% insects, 17% birds). Our results highlight the role of small
carnivores, especially Rusty-spotted Cat in regulatory services through pest
control.
Keywords: Ecosystem services, molecular tools, rodent
prey, scat analysis, small carnivores.
Small carnivores have demonstrated their value
in controlling pests, drawing attention to the larger effort required to
monitor their responses to changes in their environment, in order to
effectively plan their conservation (Marneweck et al.
2021; Bandyopadhyay et al. 2024). Further, Marneweck
et al. (2022) argue that small carnivores are an ideal group to study for
understanding the effects of global change due to their higher diversity,
intermediate trophic position, wider ecological niches, and higher reproductive
rates than of large carnivores.
Sanjay Gandhi National Park (SGNP), spread
over an area of 103.68 km2, is unique
in being located within one of the world’s most densely populated cities and is
popularly referred to as the lungs of Mumbai (Everard 2019). However, the
protected area faces severe threats from human encroachments and rapid
development along its boundary (Zérah & Landy
2013; Shinde 2017; Engineer 2018). Although several studies on various taxa
have been undertaken in SGNP, the Leopard Panthera
pardus has received most research attention,
largely due to severe conflict issues (Munde & Limaye 2013; Surve et al. 2022).
Eight other carnivore species have been reported in SGNP, including the
Rusty-spotted Cat Prionailurus rubiginosus and Jungle Cat Felis
chaus, Small Indian Civet Viverricula
indica, Asian Palm Civet Paradoxurus
hermaphroditus, Indian Grey Mongoose Herpestes edwardsii,
Ruddy Mongoose Herpestes smithii, Golden Jackal Canis
aureus and Striped Hyena Hyaena hyaena (Surve et al. 2015; Mukherjee et al. 2020). All these
species are placed in Schedule I of the Wildlife (Protection) Amendment Act,
2022. Among these, the Rusty-spotted Cat is a species of conservation priority
in India and SGNP, as the larger part of its relatively restricted global
distribution falls within the country (Munde & Limaye 2013; Mukherjee et al. 2016a).
The
Rusty-spotted Cat is categorised as ‘Near Threatened’
on the IUCN Red List, and is endemic to India, Sri Lanka, and Nepal (Mukherjee
et al. 2016a). It is the smallest member of the cat family, weighing 2 kg on
average (Pocock 1939; Nowell & Jackson 1996; Sunquist
& Sunquist 2002). Based on preliminary
information on habitat requirements, a population decline of up to 25% is
predicted in the next decade, largely due to habitat loss associated with
large-scale expansion of agriculture, development and urbanisation
(Mukherjee et al. 2016a; Sharma & Dhakad 2020).
Some observations on the cat suggest that it largely feeds on small mammals
(Patel 2006; Athreya 2010; Langle
2019). Although SGNP has a captive breeding facility for the Rusty-spotted Cat,
there is very little information available on its ecology within SGNP. The same
applies to all the other small carnivores with only sporadic reports from
by-catch data on camera traps placed for the Leopard.
Dietary
studies can provide useful insights into several aspects of small carnivore
ecology, e.g., community dynamics, competition, and niche spaces, and provide
information on ecosystem services and functioning (McNab 2002; Ćirović et al. 2016; Everard 2019; Müller et al. 2022).
A reason for this low volume of information on small carnivores is perhaps the
difficulty in studying their ecology, especially diet and behaviour
due to their largely cryptic habits. With molecular techniques, these aspects
can now be explored through non-invasive means (Piggott & Taylor 2003).
Available literature on the diet of some small cats suggests that rodents form
the major prey of the Jungle Cat (Mukherjee et al. 2004; Majumdar et al. 2011),
of the Leopard Cat Prionailurus bengalensis (Rabinowitz 1990; Grassman
et al. 2005; Rajaratnam et al. 2007; Shezad et al.
2012; Lorica & Heany
2013, Parchizadeh et al. 2023) and of the Caracal Caracal caracal
(Mukherjee et al. 2004; Braczkowski et al. 2012). In
contrast, viverrids and herpestids feed largely on
insects and plant matter (Su & Sale 2007; Kalle
et al. 2012; Akrim et al. 2023).
We involved
citizen volunteers in our research and exposed them to the scientific methods used
in studying the diets of small carnivores (Mukherjee et al. 2021). In this
paper, we present results from our study on the diets of Rusty-spotted Cat and
other co-occurring small carnivores in SGNP and the adjoining areas in Yeur village, Shivaji Nagar,
Dahisar Quarry, and Aarey Milk Colony.
SGNP is
credited with providing several ecosystem services, including provisioning of
water to the metropolis, recreation to tourists who visit daily and supporting
services for maintaining biodiversity (Everard 2019) (Figure 1). Tulshi and Vihar lakes are
located within SGNP and provision part of the city’s water requirements;
several streams and rivers flow through SGNP and into the Arabian Sea (Munde & Limaye 2013).
Due to its
proximity to the coastal region, SGNP experiences a mean humidity of 75% (Munde & Limaye 2013). The
southwest monsoon occurs from June to September with an average of 2,000 mm of
rain (Munde & Limaye
2013). The mean annual temperature is 27 oC,
occasionally soaring up to 40 oC, and
January is generally the coolest month with a mean minimum temperature of 19 oC (Munde & Limaye 2013).
The major
forest types in SGNP are Southern Moist Teak-bearing, Southern Moist Mixed
Deciduous, Mangrove Scrub, and Western Subtropical Hill forests (Champion &
Seth 1968). SGNP falls within the 5A-Malabar Plains Biogeographic Zone (Rogers
et al. 2002).
The faunal
diversity list of SGNP includes 172 species of butterflies, 50 species of
herpetofauna, 286 species of birds, and around 43 mammalian species (Kasambe 2012). Apart from the Leopard and smaller
carnivores, mammals occurring in SGNP include Sambar Rusa
unicolor, Chital Axis axis, Southern Red
Muntjac Muntiacus muntjac, Indian
Chevrotain Moschiola indica,
Wild Pig Sus scrofa,
Northern Plains Gray Langur Semnopithecus
entellus, Bonnet Macaque Macaca
radiata, Rhesus Macaque M. mullata, Black-naped Hare Lepus nigricolis,
Indian Crested Porcupine Hystrix indica, palm squirrels Funambulus
and several species of murid rodents (Edgaonkar
& Chellam 1998; Pradhan 2002; Surve
et al. 2015). Due to numerous human settlements within SGNP, several domestic
mammals are also present, including Domestic Dog Canis
familiaris, Domestic Cat Felis
catus, Goat Capra hircus,
Water Buffalo Bubalus bubalis
and Cattle Bos taurus (Surve
et al. 2015).
In March and
April 2017, volunteers from Mumbai were trained in field techniques which
included locating and collecting scats, using field instruments and software
such as hand-held GPS, mobile phone applications for marking coordinates and
uploading data, monitoring water bodies and streams, camera trapping, and the
basics of GIS applications (Mukherjee et al. 2021). Soon after the training,
from 16 April 2017 to 15 May 2018, volunteers formed three groups, one for each
of the three Forest Ranges closest to their residences and visited various
locations within SGNP to collect scat samples. Each group had a team leader who
prepared a schedule for sampling, which was restricted to weekends and
holidays. Each team comprised two to four volunteers who walked trails within
the Forest Range and collected scat samples following a specific protocol. Only
intact samples were collected. Once a scat was located, it was photographed
along with a labelled vial with the date, geographic coordinates and sample
number, a scale and GPS unit or android phone with the geo-coordinates visible,
placed next to it. This photograph, along with the names of members of the
sampling team, date, time, name of the Forest Range, and geographic coordinates
were uploaded onto the android application Epicollect
5 (Aanenson et al. 2009), which could be accessed by
the investigators.
The scat
samples were shipped to the Indian Institute of Science Education and Research
(IISER) Tirupati for further analysis. Due to the large number of scat samples
collected and the limited time to analyse them, they
were initially assigned to cats because of their compact shape that is
segmented and with tapering ends (Chame 2003) and
based on personal observations by the first author. A small portion of the
samples that was most intact and smooth, and visually assigned to cats, was
kept aside for molecular analysis and assignment to a predator species. These
samples were weighed and analysed for diet remains.
Prey remains such as teeth, bones, feathers and other undigested matter were
observed under a microscope. The percentage of samples containing specific prey
remains was determined (Klare et al. 2011). Data were
analysed using R version 3.2.3 (R Development Core
Team 2016), package “boot” version 1.3–24 (Canty & Ripley 2019).
Sub-samples equalling original sample sizes (n=22 for
Rusty-spotted Cat and n=52 for other unidentified small carnivores) were analysed using non-parametric bootstrap analysis with 6,000
simulations. Results were presented as the mean number of scat samples
containing remains of specific taxa with basic 95% Confidence Intervals.
We used a
commercially available stool DNA extraction kit from HiMedia
Laboratories following the manufacturer’s protocols, with a control in each set
of extractions to detect any contamination. We targeted the 16s rRNA region of
the mitochondrial DNA for assigning the samples to predators, using primers
designed by Mukherjee et al. (2016b). The primers amplified a region of 200 bp and their sequences were as follows:
Felid16srRNA Forward: 5’ AATTGACCTTCCCGTGAAGA
3’
Felid16srRNA Reverse: 5’ TCCGACTGGTTAGTCTAGAT
3’
The Tm
of both primers was 58 °C, and we used an annealing temperature of 50 °C in the
Polymerase Chain Reaction (PCR) programme. PCR
reactions were set up in volumes of 20 μl with a PCR
Master Mix (MM) (Origin Diagnostics, Kerala). Bovine Serum Albumin (BSA)
(Sigma-Aldrich) was added to the reactions for better results. The volumes and
concentrations of the reagents used were as follows: 5 ml of MM, 2 μl of 2 mM primers, 2μl of 4 mg
BSA, 7 μl of Mili-Q water,
and 4 μl of DNA extract. Specifications of the PCR
program used were initiation at 94 °C for 10 minutes, denaturation at 94 °C for
30 seconds, amplification at 50 °C for 45 seconds, elongation at 72 °C for 50
seconds, and final elongation 72 °C for 10 seconds. The 2nd, 3rd
and 4th steps were repeated for 59 cycles.
We used
UV-treated hoods and had PCR negative controls to detect any contamination
during the PCR stage.
We viewed
the PCR products through gel electrophoresis on a 2% agarose gel (HiMedia laboratories) with Orange G loading dye from
Sigma-Aldrich and GelRedTM DNA stain (Life
Technologies, India). We loaded a 100 bp ladder (HiMedia laboratories) along with the PCR products as
reference. The PCR products that amplified with the felid primers were sent to Chromgene Biotech Private Limited for forward and reverse
reaction sequencing. We used Chromas version 2.6.5 (Technelysium
Pty Ltd.) to view and clean sequences, and then used the BLAST analysis (Basic
Local Alignment Search Tool) on NCBI (McGinnis & Madden 2004) for
identifying species. We aligned sequences using ClustalW
in MEGA 6.0 (Tamura et al. 2013) for alignments. For sequences that were
identified as Rusty-spotted Cat, we constructed a Neighbour
Joining phylogenetic tree in MEGA 6.0 (Tamura et al. 2013), rooted with members
of the genus Felis (Domestic Cat, Accession
Number: AF006453.1; Afro-Asiatic Wildcat F. lybica,
Accession Number: AF006395.1; Jungle Cat, Accession Number: AF006393.1). We
also included Leopard Cat P. bengalensis
(Accession Number: AF006437.1), Fishing Cat P. viverrinus
(Accession Number: AF006451.1) and an existing sequence of Rusty-spotted Cat (Accession
Number: NC_028304.1) to depict the accuracy of the assignments. All existing
sequences were obtained from NCBI (Clark et al. 2016). We mapped the locations
of Rusty-spotted Cat and other small carnivore scat samples used in the diet
analysis using QGIS Version 2.8.2-Wien (QGIS 2015).
Over
approximately five months, 126 scat samples were collected in Yeur, Tulshi and Borivali Forest
Ranges within SGNP and surrounding areas in Yeur
village, Shivaji Nagar, Dahisar Quarry and Aarey Milk Colony (Figure 1). From these, 78 were visually
assigned to small cats based on their shape. These 78 were subjected to DNA
analysis, of which 30 samples (38%) gave positive results with the felid
primers and were sent for sequencing. Results from BLAST revealed that 24 of
these were of Rusty-spotted Cat, comprising 20 from Yeur
Range, two from Shivaji Nagar, and one each from Tulshi Range and Dahisar Quarry area. Five were not of
felids but most similar to mongoose species. One scat did not generate a good
enough sequence for assignment. The average weight of Rusty-spotted Cat scat
was 4 g (range: 1.2–16.5 g). No Jungle Cat scat was reported through molecular
analysis.
Seventy-four
scat samples with discernible food remains were analysed
for diet and showed a predominance of rodent remains (Figure 2). Of the 24 scat
samples assigned to Rusty-spotted Cat, two from Yeur
Range had no identifiable remains and were not included in the diet analysis.
The phylogeny of the sequences supported the BLAST results of assignments to
Rusty-spotted Cat (Figure 3). A comparison of diets revealed a higher presence
of rodents in the diet of the Rusty-spotted Cat (Table 1).
We presume
that the rodents consumed by the Rusty-spotted Cat belong to the Mus
genus, based on size and morphological characteristics of rodent molars found
in the sample (Image 1).
Our study is the first to involve citizen volunteers in sampling scat of
small carnivores in India and to systematically document Rusty-spotted Cat
diet. Our results of murid rodents forming the predominant diet of the
Rusty-spotted Cat corroborate earlier observations (Patel 2006; Athreya 2010; Langle 2019).
Systematic studies on the diets of other small cat species in varied habitats
reiterate the role of small cats as rodent control agents and highlight their
ecosystem services (Rabinowitz 1990; Mukherjee et al. 2004; Grassman
et al. 2005; Rajaratnam et al. 2007; Majumdar et al. 2011; Braczkowski
et al. 2012; Shezad et al. 2012; Lorica
& Heany 2013, Mukherjee et al. 2016b; Parchizadeh et al. 2023).
In contrast, the diets of the other small carnivores show a much higher
proportion of insects and plant matter than consumed by the Rusty-spotted Cat.
This is in line with existing information (Su & Sale 2007; Kalle et al. 2012; Akrim et al.
2023).
Future studies can focus on standardising
primers for other carnivore species, identifying the prey remains in scat with
greater precision through Next Generation Sequencing work, quantifying diets
and estimating prey abundance for more precise and meaningful results
(Mukherjee et al. 2004; Klare et al. 2011; Shezad et al. 2012).
Visual
assignment of scat had an error of more than 60%, where scat samples of other
carnivores were assigned to small cats. The primers designed for detecting
felids gave an error of 17%, where five mongoose scat samples were amplified,
an error that was noticed after sequencing. Based on these, we recommend using
PCR amplification followed by sequencing for assigning scat to species for
obtaining reliable results. Further, there is a possibility of false negatives
where the primers did not amplify small cat DNA, and some scat samples could
have erroneously been placed in the unidentified carnivore group, biasing the
diet results. In the future, this can be addressed by using additional primer
sets designed on other regions of the DNA (Liu et al. 2023).
Studies
conducted in other parts of the country had a larger proportion of 47–67% of
scat assigned to felids using molecular tools (Mukherjee et al. 2010, 2016b),
whereas only 38% in the current study in SGNP were detected as being felid
scat. This can either be attributed to the poorer condition of the scat samples
during collection or smaller populations of small cats in SGNP. A drawback of
this study was that most scat samples were collected in the Yeur
Range, which could reflect the possible unequal effort put in by volunteer
teams, since each team was assigned to a specific forest range and adjoining
areas outside.
A report by
Everard (2019) listing the potential ecosystem services of SGNP includes possible
regulatory services by predators that can be hampered by habitat destruction.
The results of our project highlight the importance of generating information
on such services, especially around the fringes and outside the perimeter of
SGNP. We also found scat near human habitation outside the boundary in Yeur and Dahisar Quarry, though most of the sampling was
restricted within SGNP. Unlike the Leopard, small carnivores do not pose a
threat to human lives, so the conflict with humans is unidirectional where
developmental activities are directly responsible for habitat loss.
Table 1. Mean percentage
frequency of prey items in scat of Rusty-spotted Cat and other unidentified
small carnivores from Sanjay Gandhi National Park and surrounding areas in
Mumbai, India, with bootstrap 95% confidence intervals (CI)
|
Prey |
Rusty-spotted Cat (n = 22) Mean (%), (95% CI) |
Other small carnivores (n = 52) Mean (%), (95% CI) |
|
Rodents |
95, (91–100) |
79, (69–90) |
|
Birds |
5, (0–27) |
17, (6–27) |
|
Reptiles |
6, (4–18) |
0 |
|
Insects |
14, (0–27) |
38, (25–52) |
|
Plant matter |
9, (0–18) |
40, (27–54) |
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