Behavioural sampling techniques and activity pattern of Indian Pangolin Manis crassicaudata (Mammalia: Manidae) in captivity
Rajesh Kumar Mohapatra 1 & Sudarsan Panda 2
1 Pangolin
Conservation and Breeding Center,Nandankanan Zoological Park, Baranga,Khurda, Odisha 754005,
India
2 Nandankanan Zoological Park, Mayur Bhawan,Saheed Nagar, Bhubaneswar, Odisha751007, India
1 rajesh.wildlife@gmail.com (corresponding
author), 2 sudarsanpanda61@gmail.com
Abstract: The study presents data on six Indian
Pangolins Manis crassicaudataobserved in captivity at the Pangolin Conservation Breeding Centre, Nandankanan, Odisha, India over
1377 hours of video recordings for each pangolin between 1500hr and 0800hr on
81 consecutive observational days. Video recordings were made through digital systems assisted by infrared
enabled CCTV cameras. The data highlights
patterns relate to 12 different behaviour and enclosure utilization. Different interval periods for sampling
of instantaneous behaviour from video recordings have been evaluated to develop
optimal study methods for the future. The activity budgets of pangolins displayed natural patterns of
nocturnal activity with a peak between 20:00–21:00 hr. When out of their burrow, they spent
about 59% of the time walking in the enclosure, and 14% of the time
feeding. The repeatability of the
behaviours has a significant negative correlation with the mean time spent in
that behaviour. Focal behavioural
samples significantly correlated with instantaneous samples up to 15 minutes
interval. The correlation values
gradually decreased with the increase in sampling interval. The results
indicate that results obtained from focal sampling and instantaneous sampling with relatively shorter intervals (≤5 minutes) areabout equally reliable. The study
suggests use of focal sampling, instead of instantaneous sampling to record
behaviour relating to social interactions.
Keywords: Activity budget, behavioural sampling, focal sampling, Indian Pangolin,
instantaneous sampling, Nandankanan.
doi: http://dx.doi.org/10.11609/JoTT.o3423.5247-55 | ZooBank:urn:lsid:zoobank.org:pub:D5A984AF-8842-4C72-9C44-F315D8076C9E
Editor: L.A.K. Singh, Bhubaneswar, Odisha, India. Date of publication: 26 December
2013 (online & print)
Manuscript details: Ms #
o3423 | Received 03 December 2012 | Final received 05 July 2013 | Finally
accepted 11 November 2013
Citation: Mohapatra, R.K. & S. Panda(2013). Behavioural sampling techniques and
activity pattern of Indian Pangolin Manis crassicaudata (Mammalia: Manidae)
in captivity. Journal
of Threatened Taxa 5(17): 5247–5255; http://dx.doi.org/10.11609/JoTT.o3423.5247-55
Copyright: © Mohapatra & Panda 2013. Creative Commons Attribution 3.0 UnportedLicense. JoTT allows unrestricted use of this
article in any medium, reproduction and distribution by providing adequate
credit to the authors and the source of publication.
Funding: This study is a part of the research project funded by Central Zoo Authority, New Delhi.
Competing Interest:Authors declare no competing interests.
Author Details: R.K. Mohapatra is
working as Junior Research Fellow; has registered for his PhD in Utkal University, Odisha with an
objective to understand behavioural patterns, space
utilization, reproductive biology, haematology,
effect of environmental enrichment and identification of ecto-
and endo-parasites of captive Indian pangolins which will be ultimately helpful in captive managementand breeding of the species. Dr. S. Panda is currently working as
Director, Nandankanan Biological Park, Odisha. He is the project
investigator of the research project. He has co-authored 7 books and 30
research papers in the field of wildlife and biodiversity. His research
interest includes wildlife conservation, in-situ and ex-situ management of
wildlife and biodiversity studies.
Author Contribution: Both
authors conceived the study, participated in its design and coordination. RKM
contributed in behavioural data collection, data analysis, review of literature and in drafting the
manuscript. Both authors contributed to revision of the manuscript and approved
the final manuscript.
Acknowledgements: The authors wish
to extend their sincere thanks to the Central Zoo Authority, New Delhi for
their financial support in undertaking the research work in Pangolin
Conservation Breeding Center at NandankananZoological Park, Odisha, India.
For figures, tables -- click here
INTRODUCTION
Pangolins are toothless small mammals with overlapping horny scales on
their body, protrusible long tongue and prehensile
tail, rolling up into a ball when threatened. They belong to the family Manidae of order Pholidota. Indian Pangolin Manis crassicaudata distributed throughout peninsular India, Sri
Lanka, Bangladesh and Pakistan (Heath 1995; Molur2008). The
Indian Pangolin is included under Appendix II of CITES, as ‘Near Threatened’
under the IUCN Red List (Molur 2008), and as a
Schedule I animal of the Indian Wildlife (Protection) Act, 1972. For better management, welfare and
breeding in captivity there is need for a better understanding of their
behaviour.
Behaviour is the exhibition of a phenotypic trait within the
environmental context for which primary selective forces have shaped it, the
outcome of which is inclusive fitness (Eisenberg 1981). Behavioural monitoring is a demonstrated
technique that can improve the welfare of animals in zoos (Kleiman1992), and meet conservation goals (Watters et al. 2009). Behavioural sampling method is crucial
to understanding and interpreting behaviour of an animal, because sampling bias
does not change the behaviour of the animal but can affect the efficiency and
reliability of data collection (Fragaszy et al. 1992).
There are different methods of behavioural sampling (Altmann1974; Martin & Bateson 1993; Lehner 1996). ‘Focal sampling’ is simple and easy to
use in a wide variety of environments (Tyler 1979; Lositoet al. 1989). ‘Focal sampling’ requires the use of a stopwatch for precise
recording of the transition times between activity states. As described by Altmann(1974), ‘instantaneous sampling’ records the state at fixed time points.
Choosing an appropriate interval between sample points is essential, particularly
for ‘bout lengths’ for meaningful and unambiguous ‘instantaneous sampling’
(Engel 1996).
The present study aimed at finding out the time-budget for various above-ground activities of captive Indian Pangolins. The study also determined the optimal sampling
interval for behavioural data collection with instantaneous sampling technique.
MATERIALS AND METHODS
I. Animals and housing conditions
The study was conducted between February 2012 and April 2012 on six
(three males and three females) Manis crassicaudata at the “Pangolin Conservation Breeding
Centre” of Nandankanan Zoological Park, Odisha, India (Table 1). Each pangolin was individually housed in
an enclosure 4.8x4.2x3.0 m in dimension, where 0.5m deep red laterite soil was provided as substrate over a reinforced concrete
base to prevent digging and escape of the animal. On all four sides above the concrete
base there was a reinforced concrete wall up to a height of 1.0m, above which
chain-link mesh was provided on all four sides upto the
concrete roof. An earthen mound,
2x2 m, and some hollow wooden logs and wooden poles provided enrichment
material in each enclosure. The
pangolins were microchipped with a passive integrated
transponder (PIT) for their individual identity. The microchip number and a short
reference name for each pangolin are given in Table 1. The daily husbandry routine consisted of
enclosure cleaning, water maintenance, feeding and health monitoring. Health monitoring comprised of (i) observation through video recordings to detect
inactivity or change in behaviour, (ii) intermittent direct observation for any
sickness, and (iii) faecal sample examination to detect the presence of
gastrointestinal parasites. Every
month physical examinations were carried out with each pangolin for measuring
the length and weight of the body, for detection of any injury or external
parasites and for secretion from their natural orifices like nose, mouth and
genitalia. During the study period all the pangolins were healthy and didn’t show
any adverse health parameters. The
average temperature during the study period was 28.40C, whereas the
maximum and minimum values recorded inside the enclosure were 22.10C
and 32.30C, respectively.
II. Behavioural observation
The following terms are used to describe
present behavioural study: (i) ‘Ethogram’-
a complete inventory of the behaviour patterns of species (Tinbergen 1951);
(ii) ‘Focal Sampling’- continuous behavioural observation that records each
sample period for each focal individual (Altmann1974); (iii) ‘Instantaneous behavioural sampling’- the documentation of
individual’s current activity at preselected moments in time (Altmann 1974); (iv) ‘Activity pattern’- the time spent in
different above-ground behaviour when pangolins could be observed through CCTV
(close circuit television) cameras.
Data for this study was obtained from six
numbers of pangolins and comprised 1377 hours of video recordings for each
pangolin between 1500 and 0800 hr on 81 consecutive
observational nights. Since the
Indian pangolins are nocturnal, secretive, solitary and intermittently active,
behavioural observation was made through digital video recording system
assisted by infrared enabled CCTV cameras installed at each enclosure using
focal animal sampling. Though the
enclosures of each pangolin were regularly inspected during the remaining time,
i.e., from 0800 to 1500 hr, of the observational day,
no above-ground activity was observed and was not
subjected to analysis. An ethogram of commonly observed behaviour of pangolins was
prepared from the preliminary observations (Table 2). The observed behaviours with their
respective time intervals were documented in Excel worksheets.
The ‘focal samples’ comprised of the
durations of respective behavioural events extracted by continuous behavioural
scan from recorded video files. The
focal samples were used to create instantaneous sample data set. For example, behavioural scans at every
60th second were used to create the instantaneous sample for a
one-minute interval. Similar behavioural scans were carried out to prepare
instantaneous samples at 2, 3, 4, 5, 10, 15, 20 and 30 minute intervals. When behaviour was measured with
instantaneous sampling at intervals, the sampled behavioural data stands for
all the behavioural events that occurred during that particular interval. Therefore, ‘instantaneous behavioural
samples’ at different intervals, extracted from the ‘focal behavioural samples’
were multiplied with the sampling interval to represent ‘behavioural score’.
III. Data analysis
Estimates of sample size included mean, standard deviation and standard
error calculated for focal behavioural samples as well as instantaneous
behavioural samples. The mean ‘bout
duration’ of any behaviour was calculated by extracting at least 50 samples
from focal sampling data during initial observations. Similarly, the ‘mean
duration of repeatability’ of any behaviour was calculated from more than 30
samples extracted from the focal sampling data. Spearman rank-order correlations (rs) were calculated to correlate mean bout
duration, mean duration of repeatability and mean time spent in displaying the
behaviour. To find out optimal
sampling interval for Instantaneous behavioural sampling, the behavioural data
from focal samples and instantaneous samples at different intervals were
subjected to the following statistical tests. Pearson product correlations (r) were
used to correlate average time spent in different behaviour. Analysis of variance
(Zar 1984) was used to test the null hypothesis that
the expected means of all samples taken by different sampling methods are
equal. Rejection of null hypothesis
only implies that the group means were not the same. To find out the way in which
the group means were different, Fisher’s Least Significant Difference (LSD) was
conducted for pair-wise comparisons of sample means at same level of
significance (Chainy 2004; Meier 2006).
The focal behaviouralsampling data were used for generating patterns relating to the above-ground activities. The patterns included ‘total
activity time’ and the ‘duration of time spent’ for any behaviour(Tables 2 & 3). The average
activity pattern for each individual pangolin was calculated by converting the
minute-based time duration of behaviour to percentage
of time spent.
Behavioural diversity of individual
pangolins was calculated by Shannon-Weiner index (H) using PAST
(Paleontological Statistics ver. 2.12). All behaviouralstates were utilised for the calculation of
Shannon-Weiner index (Magurran 1988). To quantify the ‘space utilization’
during total activity time, the time spent by pangolins over different
substrates namely ground, water, mound, and enrichment material, were estimated
and analysed.
RESULTS
The 12 behaviourscompared between six Indian Pangolins (Table 1) were presented in the ethogram (Table 2). Mean time spent (± standard deviation)
in different behaviours (in minutes) by individual
Indian Pangolins is given in Table 3. This study used analysis of focal behaviouralsampling data as the standard to compare instantaneous sampling data at
different interval. Means and
standard errors for all behaviours comparing
different sampling techniques are given in Table 4. Correlation values were determined
between focal sampling and instantaneous sampling. Behavioursmeasured at 1-minute intervals were highly significant with focal samples
(r>0.92, P<0.05). Focal behavioural samples significantly correlated (P<0.05)
with instantaneous samples up to 15 minuteintervals. The correlation values
gradually decreased with the increase in sampling intervals (Table 5). Taking individual behavioursinto consideration, walking (r=0.904, P<0.05), pacing (r=0.915, P<0.05)
and climbing (r=0.876, P<0.05) behaviours are
highly correlated in all the intervals of instantaneous sampling. We also found
that the repeatability of the behaviours have a
significant negative correlation with the mean time spent in that behaviour (rs=-0.721;
P=0.008). By comparing the
difference of means between focal samples and instantaneous samples with LSD
value, it was found that the mean values of the behaviours,
except social interaction samples, with interval ≤ 5 minutes were not
significantly different from focal samples (Table 6).
A peak in activity was
observed between 2000–2100 hr in the present
study on Indian Pangolins, except for the pangolin P395, which was found most
active between 2300–2400 hr, followed by
decreasing activity thereafter (Fig. 1). Pangolins were active, i.e., exhibited different behaviourover ground for 129.02±46.45 minutes (N=81days) on average in a day during the
study period. Out of the total active period, time spent on different behaviour were feeding (14±4.32%, N=6), drinking
(0.72±0.56%, N=6), bipedal stand (2.3±1.73%, N=6), coiling (0.61±0.43%, N=6),
digging (3.67±3.65%, N=6), exploration (6.59±3.91%, N=6), climbing (0.68±0.64%,
N=6), bathing (0.18±0.06%, N=6), walking (59.34±22.33%, N=6), and secretive
(1.84±0.83%, N=6). For two
pangolins social interaction scored 1.35±0.63%, and pacing was 19.18±15.15%. The beginning of activity was usually
directed towards feeding behaviour that started
3.5±1.8 minutes (N=81days) after emergence of pangolins from burrows, except
the pangolin P395 (30.8±24.6 minutes). Mean time allocated in individual pangolins is given in Fig. 2. The differences in equitability of behavioural diversity exhibited were tested for individual
pangolins. No significant
difference was observed in behavioural diversity
(F=0.577, N=6, P=0.719); with Shannon-Weiner diversity index (H) value,
0.791>H>1.586. It was found that pangolins spent most of the time on the
ground (73.25±58.23%) exhibiting, walking, pacing, digging and coiling behaviour (Fig. 3). The time spent near the feeding platform is the second highest
(9.66±4.28%) that spend for feeding and associated behaviours. Pangolins used the enrichment items
(2.99±2.35%) for climbing behaviour. They used given water pools (0.82±0.78%)
for drinking, bathing, water inspecting behaviour. Time
spent in mound utilisation (2.76±2.41%) includes
walking over mound and mound inspecting behaviours.
DISCUSSION
I. Behaviouralsampling
An observational study should
show that their sampling technique is reliable, i.e., they have small errors of
measurement and that the scores of individuals show stability, consistency, and
dependability for behaviour being studied. If the
measure is not reliable, it cannot be expected to show lawful relationships
with other variables being studied (Mitchell 1979). In most behaviouralstudies the standard is focal sampling (Mitlohner et
al. 2001) but instantaneous sampling is not uncommon. Instantaneous sampling
proved to be an accurate reflection of the amount of time spent by an animal in
various behaviours (Leger 1977). Several studies have used instantaneous
sampling technique with one minute (Bashaw et al.
2003, 2007; Skibiel et al. 2007; Macri& Patterson-Kane 2011), two minutes (Anderson et al. 2010), 15 minutes
(Lyons et al. 1997) and 9–19 minutes (Vickery & Mason 2004) intervals
to study behaviour and their temporal changes in
different animals in captivity. Challender et al.
(2011) used scan (instantaneous) sampling with 15 minutes to study feeding,
locomotion, social behaviour and the activity pattern
of Sunda Pangolins Manis javanica. Mishra & Panda (2010) used instantaneous sampling with 10 minutes
interval to study the walking, digging, feeding, drinking,
climbing behaviour of Indian Pangolins. The results of the present study
indicate that instantaneous sampling techniques with relatively short interval
lengths (1, 2, 3, 4, 5 minutes) can be used reliably for measuring behaviours and significantly support focal samples, except
social interaction behaviour (Table 5). This may be due to less repeatability of
the behaviour (Table 3) than other behaviours. Therefore the study suggests use of focal sampling to record social
interaction behaviour. Besides, repeatability of behavioural measures also depends on the bout duration of
the behaviour. Studies have shown that the shorter the interval the more accurate
duration is obtained from time sampling (Powell et al. 1975; Sanson-Fisher et al. 1980). If short-duration behavioursare of interest and percentage observation time is the response dimension of
interest it is wise to choose shorter intervals as far as possible.
Instantaneous sampling is
often useful to avoid arbitrary definitions of behaviour’sstart and end time, which may be difficult to specify. It needs less time and number of efforts
than focal sampling, and it can easily be carried out in conjunction with
sampling other behavioural and ecological data (Doran
1992). One can study the behaviour of animals by circular scan in particular
interval of time and that interval can be used for recording data from another
animal. Instantaneous sampling can improve efficiency by avoiding observer
fatigue and inability to process desired volume of information. If the initial observation
yield a high correlation between focal behaviouralsampling and instantaneous sampling, the investigator may use the later for
further recording to save time and efforts. These outcomes lead many to
recommend instantaneous sampling as a mode of choice (Dunbar 1976; Leger 1977;
Powell et al. 1977; Shahon-Fisher et al. 1980;Ary & Suen 1983; Tagha et al. 1985).
II. Activity pattern
The result obtained in this
study is similar to that of Mishra & Panda (2010) that report captive
Indian Pangolins spend most of their time walking inside the enclosure under
simulated conditions of surroundings. The time of sunset plays a role in initiating the activities of the
pangolins and the activity pattern recorded for each individual is very
specific to each (Mishra & Panda 2010). Results from the present study suggest
that the pangolins were active intermittently between 1700 and 0500 hr. This is similar to the activity pattern
reported for Sunda Pangolins by Challenderet al. (2011). The peak period of
activity was during 2000–2100 hr with one
individual variation. Pangolin P395
was most active during 2300–2400 hr. It is clear from the present study that variations in behavioural diversity were observed between individual pangolins. Stereotypic pacing behaviourwas observed in some of the individuals, predominantly in P5FE (55.04±30.91%,
N=81 days) and P473 (2.29±2.13%, N=81 days). The forms and frequencies of pacing
observed in this study were comparable to those reported from Sunda Pangolins (Challender et
al. 2011). Maintaining Indian
Pangolins in natural enclosures, in which they can perform a full range of
natural behaviour and exert control over their
environment, is likely to offer some protection against behaviouraldeficits. Furthermore,
environmental enrichment has had some success in reducing the development of
stereotypes (Bashaw et al. 2003, 2007; Skibiel et al. 2007). Development of environmental enrichment for Indian Pangolin is a matter
for further study.
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