Journal of Threatened Taxa | www.threatenedtaxa.org | 26
December 2019 | 11(15): 14971–14978
A
comparative analysis of hair morphology of wild and domestic ungulate prey
species of Leopard Panthera pardus fusca (Mammalia:
Carnivora: Felidae) from Goa, India
Bipin S. Phal Desai 1, Avelyno
H. D’Costa 2 & S.K. Shyama 3
1 Goa Forest
Department, Government of Goa, Goa 403001, India.
2 Department of
Zoology, Dhempe College of Arts & Science,
Miramar, Goa 403001, India.
3 Department of
Zoology, Goa University, Goa 403206, India.
1 phaldesaibipin00@gmail.com,
2 avelynodc@gmail.com, 3 skshyama@gmail.com
(corresponding author)
Abstract: Guard hairs were collected from four live domesticated
ungulate species and shed guard hairs of six wild ungulate species from zoo
captive animals from five individuals each.
Photographic reference was prepared showing analytic features of hair
characteristics. Study results were
analysed and cuticle and medulla patterns were identified along with
pigmentation features from the literature available for wild and domestic
ungulates from India and abroad. Clear
and easily distinguishable morphological characters of hair medulla and cuticle
were used in the present study. Scat
analysis of big cats used in this study is easy, speedy and efficient which can
be used in routine investigations related to wildlife, crime forensics as well
as human animal conflicts by studying carnivore feeding habits. In a majority of the animal species, the
distal part of the hair showed maximum variation from the rest of the hair portions. The cuticle scales were imbricate in all
tested animals. Scale position in almost
all the tested animals was transversal except in goat (proximal part and medial
part) and mouse deer (Distal part).
Majority of the species showed smooth margins at proximal and medial
part. Whereas the distal part scale
margin was crenate and rippled in appearance the proximal part and medial part
of hair of the majority of sampled animals showed a regular wave -type scale
pattern whereas the distal part of hair showed irregular wave-type scale pattern
in dominance. The composition of the
medulla was multicellular in all the sampled deer species. Only the cow calf’s hair medulla was
unicellular and uniseriate in appearance. A comparison of the hair of the domestic pig
with that of the wild boar and gaur hair with that of cow calf and buffalo calf
hair was made for the first time in the present study. Similarly goat hair
morphology can also be differentiated from other cervids
in this study. Medulla and cuticle
characters in combination with each other can help differentiate wild ungulate
species from the domestic ones since these wild ungulate species are frequently
involved in hunting crime investigations.
Therefore, the photographic reference presented in this study can be
used in wildlife forensic science as well as predator diet analysis as an
appropriate reference for prey species identification.
Keywords:
Carnivore prey identification, hair pigmentation, medulla, ungulate.
doi: https://doi.org/10.11609/jott.4894.11.15.14971-14978
Editor: Nishith Dharaiya, HNG
University, Patan, India. Date
of publication: 26 December 2019 (online & print)
Manuscript details: #4894 | Received 14 February
2019 | Final received 12 October 2019 | Finally accepted 20 November 2019
Citation: Desai, B.S.P., A.H. D’Costa
& S.K. Shyama (2019). A comparative analysis of hair morphology of wild and
domestic ungulate prey species of Leopard Panthera
pardus fusca (Mammalia:
Carnivora: Felidae) from Goa, India. Journal of Threatened Taxa 11(15): 14971–14978. https://doi.org/10.11609/jott.4894.11.15.14971-14978
Copyright: © Desai et al. 2019. Creative Commons Attribution 4.0 International
License. JoTT
allows unrestricted use, reproduction, and distribution of this article in any
medium by adequate credit to the author(s) and the source of publication.
Funding: None.
Competing interests: The authors declare no competing
interests.
Author details: Mr. Bipin S. Phal Desai is a Range Forest Officer of
the Goa Forest Department, Government of Goa. He is also pursuing his PhD in
the Department of Zoology, Goa University. His research interests include wild
cat biology and man-wildlife interaction studies. Dr. Avelyno H. D’Costa is an Assistant Professor in the
Department of Zoology, Dhempe College of Arts &
Science which is affiliated to Goa University. He is an ecotoxicologist
and is interested in research related to genetics, ecology and
conservation. Dr. S.K. Shyama is a Professor (Retd.)
and ex. head of the Department of Zoology, Goa University. His area of
expertise is genotoxicology and interests include
ecotoxicology and wildlife biology. He has guided several PhD students in
toxicology and wildlife and conservation.
Author contribution: BSPD collected the hair
specimens, analyzed them and wrote the manuscript. AHD’C assisted with the
analysis of the specimens by providing protocols and revision of the
manuscript. SKS supervised the study and helped in the revision of the
manuscript.
Acknowledgements:
The authors wish to acknowledge Bondla Wildlife Sanctuary for providing the hair specimens.
The authors wish to thank the Department of Zoology, Goa University for
providing the necessary facilities.
Introduction
The presence of hair on the body is one of the
important characteristics of class
Mammalia. Mammalian hair is
structurally unique in different mammal species which is a result of adaptation
and evolution in response to the environment.
This characteristic is widely used to identify animals at species level
(Menike et al. 2012).
Identification of mammals using hair morphology has also been used in
diet analysis of predator species using scat analysis. In southern India several studies have
documented feeding habits of Leopard Panthera
pardus fusca during the
last two decades (Ramakrishnan et al. 1999; Athreya
et al. 2014). All these studies suggest
that wild as well as domestic animals form major components of leopard diet
especially in areas of human dominated landscapes. Predation of livestock is one of the most
important human- leopard conflict scenarios in India and is the primary cause
for leopard persecution. This in turn can lead to major threats to leopard conservation
goals. Therefore, understanding the leopard diet can play an important role for
its conservation in human dominated landscapes of India.
Photographic references of the hair structures of wild
and domestic ungulate prey species of leopard has effective practical
applications in understanding leopard feeding habits. Hair morphology is an important tool that can
be used to identify animal species (ENFSI 2015); however, identification of
species from hair structure is not a straightforward process and practitioners
need to develop expertise to identify and to be able to distinguish hair
characteristics especially in closely related species. Thus, the understanding and comparison of
hair structures is important to help distinguish one species from another.
Mammals have four types of body hair, of which guard
hair are the most important in differentiation between various animal species (Tridico 2005; Knecht 2012).
A typical mammal hair consists of a hair root and hair shaft. The root is embedded in the epidermis and the
shaft is the part which extends above the epidermis as a cylindrical structure.
The hair shaft is made up of three distinct morphological layers, i.e., medulla
(central layer), cortex (intermediate layer) and cuticle (outer layer) (Deedrick & Koch 2004a; Debelica
& Thies 2009; Knecht 2012). The medulla, which is the innermost layer of
the hair shaft, is a honeycomb-like keratinous structure which can be
continuous, discontinuous or fragmented with vacuoles in between (Deedrick & Koch 2004a). The cortex contains keratin fibers and pigment granules which are responsible for the
coloration of the hair. The cuticle, the
outermost layer, consists of overlapping keratin scales (Deedrick
& Koch 2004a). Two main patterns of
cuticle scales are: (i) imbricate, and (ii)
coronal. The distance between every two
successive scale margins can be close, intermediate or wide, depending on the
animal species (Debelica & Thies 2009).
The pattern of the cuticle scales, the type and the diameter of the
medulla and/or the characteristics of pigmentation can be used for animal
species identification (Brunner & Coman 1974).
The presence of high content of cysteine-containing
keratin and dead keratinocytes delays postmortem
changes and chemical decomposition in mammal hair (Harkey
1993; Knecht 2012). This property of
mammalian hair has helped in carrying out forensics investigations.
Although several studies have reported hair structure
identification for wild and domesticated mammal hairs (Dharaiya
et al. 2012), very few of them deal with ungulates. Further, such studies are also required to
create database for different geographical areas. In the present study we provide a
comprehensive comparative database about wild and domestic ungulate prey
species of the leopard in Goa.
Materials and Method
Sample collection and preparation
For preparing the photographic reference of cuticle
and medulla characters, shed hairs were collected from six wild ungulate
species from the night shelter enclosures of the Bondla
Zoo located at Bondla Wildlife Sanctuary, Ponda Goa and from four live domestic ungulate species from
five individuals each from Goa during January 2016 to December 2016. Guard hairs were separated from other hairs
based on their properties before analysis as given by De Marinis
& Asprea (2006).
Hairs were then immersed in 70% ethanol solution for 5–10 minutes to
remove any debris and non-hairy sticky materials. The hair strands were then dried and cleaned
on a blotting paper. Each hair length was divided into three parts: proximal
(base), medial (middle), distal (apical).
Longer hairs were cut into these three respective parts for comparative
analysis of each strand at different lengths whereas shorter hairs were used as
a whole.
Examination of hair cuticle scale pattern
Cuticle scales of individual hairs were analyzed using the methodology of Mukherjee et al.
(1994b). A 20% gelatin
solution was prepared by boiling the gelatin powder
in distilled water. The solution was
cooled and two drops of Leishman’s stain was added to the solution to obtain a
pale blue colour. One to two drops of
this solution was used to prepare a smooth film on a clean dry glass slide and
immediately cleaned hair shafts were superficially placed on the film. The glass slide was then covered with a glass
petri plate and left for 15–20 minutes at room temperature. The hair shafts
were then slowly separated from the gelatin film
using forceps such that an imprint of the scales was formed on the glass
slide. These imprints were observed and
photographed under (400X) magnification using a light microscope (Olympus
microscope BX 53).
Examination of hair medulla and pigmentation
For hair medullary pattern and pigment analysis, hairs
were immersed in xylene for 24 hours.
The hairs were then dried and then mounted on glass slides using a drop
of DPX and then covered with a coverslip (Mukherjee et al. 1994b). The slides were allowed to dry for an hour
and then observed and photographed under a light microscope at 400X
magnification.
Results
Hair structures from different species were identified
and compared for their cuticle and medulla patterns along with pigmentation
features from the literature available for wild and domestic ungulates from
India and abroad (Mukherjee et al. 1994; Dharaiya
& Soni 2012; Joshi et al. 2012; Ghallab et al. 2018).
Comparative analysis of cuticle
Cuticle scale position, scale margin, scale margin
distance and scale patterns were analyzed from guard
hairs collected from six wild and four domestic animal hairs at different hair
lengths (Table 1; Images 1–10). Analysis
of hair at three different levels revealed considerable variations in scale
margin, scale margin distance and scale patterns in all the sampled animals
whereas scale position showed no major variations at different hair
lengths. In a majority of the animal
species, the distal part of the hair showed maximum variation from the rest of
the hair portions. The cuticle scales
were imbricate in all the species studied.
Scale position in almost all the studied animals was transversal except
in Goat Capra aegagrus hircus
(proximal part and medial part) and Mouse Deer Moschiola
indica (distal part).
Based on scale margin type, pattern and distance, the
species of animals could be clearly differentiated. A majority of the species showed smooth
margins at proximal and medial part, whereas the distal scale margin was
crenate and rippled in appearance. The
proximal and medial parts of the hair of a majority of the sampled animals
showed regular wave type scale pattern whereas the distal part of hair showed
irregular wave type of scale pattern. A single chevron type of scale pattern
was seen in the medial part and distal part of gaur hair (Bos gaurus) and distal part of cow calf (Bos taurus) and goat (Capra aegagrus
hircus).
Buffalo calf (Bubalus bubalis) and domestic pig (Sus scrofa
domesticus) both showed double chevron type of
scale pattern in the medial part.
Therefore, the hair of Wild Boar Sus scrofa and domestic pig can be very well differentiated
from the analysis of cuticle characteristics.
Goat hair also can be differentiated from other sampled deer species
using cuticle pattern analysis. In case of the sampled deer species such as
Sambar Deer Rusa unicolor, Spotted Deer
Axis axis and Barking Deer Muntiacus
muntjac, including Mouse Deer Moschiola
indica—all exhibited very similar cuticular scale
patterns.
Comparative analysis of hair medulla morphology and
pigmentation
In addition to cuticle scale characteristics, hair
medulla morphology, composition, structure, pattern and margins as well as the
pigmentation has been used to identify and compare the sampled wild and
domestic ungulate prey species of leopard.
The composition of medulla was multicellular in all the sampled deer
species. Only cow calf hair medulla was
unicellular and uniseriate in appearance. Medulla cell type could not be differentiated
in buffalo calf, domestic pig and goat.
Amorphous type medulla structure was observed in buffalo calf, domestic
pig, goat, Spotted Deer, Wild Boar and Gaur, whereas filled lattice type
medulla was observed in Sambar Deer, Mouse Deer and Barking Deer. Vacuolated and fragmented medulla was
observed only in case of spotted deer. A
majority of the sampled ungulate hairs showed irregular type margin type except
in case of Sambar Deer, Mouse Deer, Barking Deer and Gaur. Pigmentation was not observed in hair cortex
of cow calf, Spotted Deer and Mouse Deer (Table 2; Images 11–12
Morphometric analysis of ungulate hair
Total hair diameter as well as medullary thickness was
measured using binocular microscope with camera attachment using ProgRes software.
Total diameter of hair was maximum at the proximal part compared to the
rest of the portion of the hair in all the sampled ungulate species, whereas
thickness of medulla was maximum at the medial part in a majority of the
species with the exception of cow calf, buffalo calf and goat. Medulla did not extend to the distal end in case
of wild boar and to the proximal end in case of gaur whereas in case of cow
calf and spotted deer medulla was absent at both the distal far and proximal
end. Only domestic pig hair was devoid
of medulla completely in the distal part (Table 3).
Discussion
Our results showing hair morphological characters of
wild and domestic ungulates were similar to the available literature (Brunner
& Coman 1974; Knecht 2012), but with a few
exceptions. Our medulla analysis results
in the case of Spotted Deer showed fragmented amorphous medulla. During the study period since there was no
reports of leopard attacks on adult cow and buffalo in Goa, only the hairs of
the young one of these domestic ungulates were used in the study. Cuticle as well as medulla characters of
adult and young individuals of these species did not show any variation when
compared with the literature (Ghallab et al.
2018). Hair characteristics of domestic
pig have been compared with that of wild boar as well as gaur with that of cow
calf and buffalo calf for the first time in the present study. Similarly goat hair morphology can also help
differentiate it from other cervids in the present
study. This information can be put to
best use when identifying carnivore species in human-carnivore conflict
situations where they attack livestock and other domesticated animals. Unlike hair cuticle character, medulla of all
the studied species did not show variation along the hair length. Cuticle of hair at different lengths in all
the studied species showed variation in scale position, pattern, spacing and
margin. This is helpful in microscopic
analysis of hair fragments which are usually the case when studying the diet of
predators through scat analysis. Medulla
and cuticle characters in combination can help differentiate wild ungulate
species from the domestic ones since these wild ungulate species are mostly
involved in crime investigations such as illegal hunting.
Characters of hair when used in isolation may not be
of much value in species identification as they show high variation; however,
when these characters are analyzed in combination
these they may provide significant information for identification of species
(Brunner & Coman 1974; Teerink,
1991). Several studies are available on
the combined analysis of hair characters for species identification. Joshi et al. (2012) have done a comparative
hair study only on the basis of the hair colour and medulla structures in Mouse
Deer, Spotted Deer, Barking Deer and Sambar Deer. Dharaiya & Soni (2012) have documented characters of transverse
section of Spotted Deer, Sambar Deer, buffalo, cow, and goat, but have not
explored cuticle and medulla characters.
The remaining studies on ungulate hair are mainly based on the
predator’s scat-hair (diet) analysis.
Analysis and examination of animal hair plays a vital
role in wildlife forensics investigation.
Analysis of hair collected from the crime scene can provide essential
information about the species involved (Soni et al.
2003). Hair analysis has even proved
beneficial in tracing chemical poisoning cases in animals (Harkey
1993; Krumbiegel et al. 2014) and hence the same can
be utilized in wildlife forensic investigation where the carcass has decomposed
and tissues cannot be collected.
This photographic reference in the present study will
help to identify the ungulate prey species of leopard and other wild carnivores
from the scat analysis from such localities.
Therefore, the photographic reference presented in this study can be
used in wildlife forensic science as well as predator diet analysis, as an
appropriate reference for prey species identification.
In conclusion, the present study provides a first-step
towards preparation of local photo reference database of hair of wild and
domesticated ungulate species which can be used in forensic investigations as
well as to study human carnivore conflict scenarios arising out of livestock
depredation. Further studies using more
advanced techniques such as electron microscopy can be used to prepare a complete
local atlas for all wild and domestic animal species’ identification.
Table
1. Comparative analysis of the Cuticle characteristics of wild and domestic
ungulate species from Goa.
|
Species |
Proximal
part of hair |
Medial
part of hair |
Distal
part of hair |
|||||||||
|
|
Scale
position |
Scale
margin |
Scale
margin distance |
Scale
pattern |
Scale
position |
Scale
margin |
Scale
margin distance |
Scale
pattern |
Scale
position |
Scale
margin |
Scale
margin distance |
Scale
pattern |
|
Cow
calf |
Transversal |
Smooth |
Distant |
Regular
wave |
Transversal |
Smooth
|
Near |
Regular
and irregular wave |
Transversal |
crenate |
Near |
Single
chevron |
|
Buffalo
calf |
Transversal |
Smooth |
Near |
Regular
wave |
Transversal |
Rippled |
close |
Double
chevron |
Transversal |
Rippled,
crenate |
Near |
Irregular
wave |
|
Pig |
Transversal |
Crenate |
Near |
Irregular
wave |
Transversal |
Rippled,
crenate |
Close |
Double
Chevron |
Transversal |
Crenate |
Close |
Irregular
wave |
|
Goat |
Intermediate |
Crenate |
Distant |
Irregular
wave |
Intermediate |
Smooth |
Distant |
Irregular
mosaic |
Transversal |
Rippled |
Near |
Single
chevron |
|
Spotted
deer |
Transversal |
Smooth |
Near |
Regular
wave |
Transversal |
Smooth |
Near |
Regular
wave |
Transversal |
Smooth,
crenate |
Distant |
Regular,
irregular wave |
|
Wild
boar |
Transversal |
Rippled |
Close |
Irregular
wave |
Transversal |
Rippled |
Near |
Irregular
wave |
Transversal |
Rippled |
Near |
Irregular
wave |
|
Sambar
deer |
Transversal |
Smooth |
Distant |
Regular
wave |
Transversal |
Smooth,
Rippled |
close |
Regular
wave |
Transversal |
Rippled |
Near |
Irregular
wave |
|
Mouse
deer |
Transversal |
Smooth |
Distant |
Regular
wave |
Transversal |
Smooth |
Distant |
Regular
wave |
Intermediate |
smooth |
Distant |
Irregular
mosaic |
|
Barking
deer |
Transversal |
Smooth |
Near |
Regular
wave |
Transversal |
Smooth |
Near |
Regular
wave |
Transversal |
Smooth,
crenate |
Distant |
Regular
wave |
|
Gaur |
Transversal |
Rippled |
Near |
Irregular
wave |
Transversal |
Crenate |
Close |
Single
Chevron |
Transversal |
Crenate |
Near |
Single
Chevron |
Table
2. A comparative analysis of medulla and pigmentation features of wild and
domestic ungulate species from Goa.
|
Comparative
analysis of hair medulla morphology and pigmentation in different animal
species |
|||||
|
Animal
species |
Composition |
Structure |
Pattern |
Margin
type |
Pigmentation |
|
Cow
calf |
Unicellular |
Uniseriate |
Continuous |
Irregular |
No
pigments |
|
Buffalo
calf |
Cells
not visible |
Amorphous |
Continuous |
Irregular |
Granules
and streak like pigments |
|
Domestic
pig |
Cells
not visible |
Amorphous |
Continuous |
Irregular |
Streak
like pigments |
|
Goat |
Cells
not visible |
Amorphous |
Continuous |
Irregular |
Granules
and streak like pigments |
|
Spotted
Deer |
Multicellular |
Amorphous,
vacuolated |
Fragmented |
Irregular |
No
pigments |
|
Wild
Boar |
Cells
not visible |
Amorphous |
Continuous |
Irregular |
Granules
and streak like pigments |
|
Sambar |
Multicellular |
Filled
lattice |
Continuous |
scalloped |
Streak
pigments |
|
Mouse
Deer |
Multicellular |
Filled
lattice |
Continuous |
Scalloped |
No
pigments |
|
Barking
Deer |
Multicellular |
Filled
lattice |
Continuous |
Scalloped |
Streak
like pigments |
|
Gaur |
Multicellular |
Amorphous |
continuous |
Scalloped |
Streak
like pigments |
Table
3. Morphometric analysis of total hair and medulla of wild and domestic
ungulate species from Goa.
|
Morphometric
analysis of ungulate animal Hair |
|||||||||||||
|
|
Total
hair thickness (µm) |
Medulla
thickness (µm) |
|
||||||||||
|
|
Proximal
part |
SD |
Medial
part |
SD |
Distal
part |
SD |
Proximal
part |
SD |
Medial
part |
SD |
Distal
part |
SD |
Remarks |
|
Cow
calf |
70.17 |
±16.88 |
55.76 |
±2.78 |
31.06 |
±9.37 |
50.20 |
±7.49 |
30.42 |
±2.50 |
15.14 |
±2.57 |
Medulla
absent in distal end and proximal end |
|
Buffalo
calf |
266.88 |
±18.96 |
181.19 |
±2.57 |
37.21 |
±8.29 |
151.89 |
±2.10 |
149.68 |
±3.35 |
26.94 |
±8.29 |
- |
|
Domestic
pig |
120.08 |
±3.93 |
185.86 |
±16.90 |
38.26 |
±16.90 |
57.79 |
±13.05 |
163.85 |
±4.07 |
0.00 |
±0.00 |
Medulla
absent at distal part |
|
Goat |
153.75 |
±4.57 |
137.97 |
±2.35 |
34.03 |
±12.43 |
111.85 |
±6.82 |
106.70 |
±1.27 |
14.78 |
±4.94 |
- |
|
Spotted
Deer |
95.90 |
±19.73 |
134.30 |
±2.63 |
17.23 |
±4.99 |
53.77 |
±32.48 |
110.03 |
±4.03 |
12.39 |
±4.48 |
Medulla
absent at proximal and distal end |
|
Wild
Boar |
363.80 |
±4.43 |
372.30 |
±17.05 |
41.16 |
±5.33 |
278.08 |
±5.14 |
313.18 |
±10.33 |
29.99 |
±10.28 |
Medulla
absent at distal end |
|
Sambar |
240.57 |
±6.31 |
228.82 |
±1.55 |
20.33 |
±4.75 |
169.28 |
±37.04 |
193.50 |
±2.88 |
9.49 |
±1.56 |
- |
|
Mouse
Deer |
135.77 |
±5.19 |
159.04 |
±2.64 |
13.94 |
±5.79 |
97.03 |
±31.79 |
124.26 |
±3.22 |
9.19 |
±2.99 |
- |
|
Barking
Deer |
118.15 |
±61.11 |
180.22 |
±9.38 |
23.21 |
±5.09 |
129.02 |
±33.99 |
166.23 |
±2.39 |
25.12 |
±5.70 |
- |
|
Gaur |
120.68 |
±23.91 |
162.74 |
±2.00 |
46.15 |
±14.55 |
46.77 |
±21.22 |
104.22 |
±7.38 |
23.86 |
±7.77 |
Medulla
absent at proximal end |
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