Behavioural Descriptions of Indian Pangolins (Manis crassicaudata) in Captivity

Abstract

conservation breeding programmes as an necessity tool for conservation of endanger species require a good cognition on behavior of the species. At present time, cognition of behavior and biota of amerind pangolins is inadequate and discrepant. During the present study, an ethogram was developed based on the behavioral observations of seven indian pangolins ( Manis crassicaudata ) at Pangolin Conservation Breeding Centre, Nandankanan Zoological Park, Odisha, India, between February 2012 and January 2013. A sum of 27 behaviours of seven distinct behavioral categories ( stationary consistency positions, locomotory patterns, care behaviours, exploratory behavior, defensive demeanor, reproductive/social behavior, and others ) were described and illustrated. The results offer a consistent human body of reference for far studies on behavioral patterns of indian pangolins. Besides, these preliminary observations could be useful in management and breeding of the species in captivity .

1. Introduction

indian pangolin ( Manis crassicaudata ; family Manidae ; order Pholidota ) is one of the eight living species of pangolins of the populace. They are toothless mammals with 11–13 rows of boastfully overlapping corneous scales, retentive protrusile tongue, and prehensile tail with a terminal scale on its ventral side [ 1, 2 ]. They are lone, fossorial, nocturnal, and insectivorous. indian pangolin occurs throughout peninsular India [ 3, 4 ]. Its scope extends as far west as Pakistan, east to West Bengal ( India ) and Yunnan ( Southwest China ), south to Sri Lanka, and north to Nepal [ 5 ]. Their populations are increasingly under menace throughout their image due to domestic and international demand for know pangolins and their skin, scales, and kernel. The biota of indian pangolins particularly gloomy generative rate and a wide distribution make them vulnerable to overexploitation [ 6 ]. captive breed broadcast, which is essential for the conservation of the species requires detail cognition about the behavior of the species. The indian pangolin is a ill known species. little attempt has been devoted to understanding its biology, ecology, and behavior, possibly ascribable to nocturnal and close habit of the species. available published information on amerind pangolin is primarily from natural history observations, rescue reports, reports of illegal trade, and captive studies. many practical questions remain unanswered because of incomplete information on ecological and behavioral biology of the species. Comprehensive cognition of pangolin behavior will be central to assess wellbeing and management of pangolins for potential captive reproduction program [ 7 ]. The ethogram for amerind pangolin could not be found in the available literature. Keeping all the points in opinion, an attack was made to prepare a standard ethogram for indian pangolins in the present wallpaper based on the observation in enslavement at Pangolin Conservation Breeding Center ( PCBC ), Nandankanan Zoological Park, Odisha, India.

2. Methodology

Nandankanan Zoological Park has the experience of maintaining indian pangolins since 1962 [ 8 ]. A Pangolin Conservation Breeding Center ( PCBC ) was established in 2008 in the park with an objective of scientific management and education of amerind pangolins. Study was conducted on seven ( 4F:3M ) indian pangolins between February 2012 and January 2013. Details of housing and farming for these animals were described elsewhere [ 9, 10 ]. Briefly, pangolins were housed in naturalistic soil-substrate enclosures of 4.8 m × 4.2 molarity × 3.0 megabyte dimensions, with hollow wooden logs, dry tree branches, and dish shaped pool as enrichment materials. The daily farming everyday consisted of enclosure cleaning, body of water successor, run, and health monitoring. Since pangolins are nocturnal and intermittently active, their behaviours were recorded through digital video recording recording system assisted by infrared enabled CCTV cameras, following Mohapatra and Panda [ 9 ]. Most of the observations were based on the individually housed pornographic pangolins except one female pangolin ( beget ) with its youthful ( observation period = 91 nights ) and copulate house of inverse sexual activity adult individuals ( observation menstruation = 14 nights ). Besides CCTV monitor, pangolins were besides observed intermittently through aim observation using depleted volume sparkle followed by photodocumentation of different behaviours. While developing ethogram, behaviours were defined in terms of consequences, that is, effect of the behavior of the pangolin on its environment and on other individuals or frailty versa. Behaviours sharing alike function were clustered into allow behavioral categories. The behavioral repertoire presented in this newspaper is strictly qualitative and the descriptions cover most common behavioral country and events shown by indian pangolins .

3. Results

A total of 27 different behavior patterns were observed. All the demeanor patterns observed were grouped into one of the seven unlike behavioral categories. These categories were stationary body positions, locomotory patterns, alimony behaviours, exploratory behavior, defensive demeanor, reproductive/social behavior, and others. The observe behaviours with their respective behavioral categories were briefly described. In addition, some of these behaviours were illustrated in Figure 1 .(a)
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3.1. Stationary Body Positions

This behavioral class includes stationary position with either afford or conclude eyes while the pangolins were sleeping or resting .

3.1.1. Sleeping

During sleep, the pangolins remain in a elongated inactive state of matter with minimal or no limb or capitulum motion. They normally attain a handbuild model with close eyes ( calculate 1 ( a ) ). They move deep inside the burrow to rest/sleep during the day in soil-substrate enclosures. When such provisions were not available ( for example, enclosures with concrete substrate ), pangolins prefer corner area for sleeping. If hole wooden logs were provided, they move inside the log during the day .

3.1.2. Resting

During resting the pangolins were found immobile with eyes capable or partially closed. Three discrete resting postures were recorded : ( 1 ) being accumbent with short or no slant born on limbs and adaxial surface of the body resting on the grind and hook of forelimb crouch back ( Figure 1 ( b-complex vitamin ) ), ( 2 ) coiled soundbox military capability with lateral recumbence and drumhead between the limbs ( figure 1 ( a ) ), ( 3 ) lay on back exposing adaxial open of their body ( design 1 ( carbon ) ) .

3.2. Locomotion Pattern

Observed locomotion patterns of pangolins include quadrupedal bowel movement from one point to another, horizontally or vertically, towards or away from facing direction. There were two kinds of locomotory behaviours .

3.2.1. Climbing

While standing, both forelimbs and hind limbs were lifted consecutive from fourth dimension to time, moving up, down, or sideward ( Figure 1 ( d ) ). They climb up in the confront direction and climb down either in the confront or back focus. They are agile climbers and, in godforsaken conditions, they credibly climb trees in avocation of ants [ 11 ]. They use their claw of the limbs to grip the tree and their prehensile tail for support while positioning their forelimb further up the tree torso [ 4 ] .

3.2.2. Walking

Manis crassicaudata walks quadrupedally, with back arched and buttocks held off from the ground ( Figure 1 ( e ) ). During walk, the front toes were bent under soles. The whole sole of hind limb is however applied to the earth [ 4 ]. Pangolin can change its direction on the ground or while moving in the branches by making a twist, alternatively of backward drift. In some instances, for exercise, during grok, pangolin moves backward as it throws dug-out soil outside the burrow. Besides, backward motion was besides sometimes observed, when pangolin climbs down from the branches and chain-linked argue .

3.3. Maintenance Behaviours

Maintenance behavior is performed by an animal in the normal course of its daily activities and is critical to its survival [ 12 ]. Six types of maintenance behaviours exhibited by the pangolins were described below .

3.3.1. Drinking

Drinking takes home by lowering head below the level of back and consume water by lapping movement of the tongue ( Figure 1 ( f ) ). Although pangolins drink water as and when required, they may live without water for a longer period [ 4 ] .

3.3.2. Feeding

Feeding involves lowering of pass below the level of back and consumption of prey ( ants and termites ) by frequent in and out movement of its gluey tongue ( Figure 1 ( gram ) ). Feeding comprises excerpt and consumption of available food resources. In the baseless, the food of pangolins consists of egg, young and adult of termites and ants. They relished ants ’ eggs more than the ants themselves [ 4 ]. In captivity, they prefer to eat their ant/termite diet before the intake of supplementary fertilize, that is, minced hard-bitten eggs and milk powderize. When termite comb was provided, the pangolins break down the comb into humble pieces which makes the inhabitants, that is, termites, come out or assessable to feed. then the termites were quickly licked off by its gluey tongue and swallowed .

3.3.3. Bathing

Pangolin dives into water from one end of the pool and comes out from the early goal. The early carriage includes laying submerged inside the pool keeping the anterior part of the body out of the water ( Figure 1 ( hydrogen ) ). At times, pangolin plays by moving to and fro inside the pool .

3.3.4. Digging

Pangolins have specialized adaptation for fossorial animation and normally live in burrows made by themselves [ 4 ]. They dig burrows with the help of their potent curved claw of the forelimbs and their hind arm aid in throwing soils out of the burrows ( design 1 ( i ) ) [ 11 ]. Pangolins were found to exhibit less overground activities and spend more time inside the burrows during the winter months than those of summer and showery temper .

3.3.5. Defecating

It refers to elimination of faeces in a quadrupedal standing position with back limbs placed apart and head lowered or crouch towards the ventral surface of the torso .

3.3.6. Territorial Marking

Pangolins normally urinate in a quadrupedal standing position ; the position is merely the like as when defecating. The urine is normally eliminated on the substrate but sometimes pangolins spray urine while climbing or clinging. The late appears to be a marking behavior as the urine is measuredly spread along the tree torso or on substrate. They besides emit a potent musky anal secretion, which could be a territorial score [ 13 ] .

3.4. Explorative Behaviours

Observed exploratory behaviours of pangolins were directed towards their proximate environment, including enclosure furnishings and/or conspecifics. Three types of exploratory behaviours observed during the award study were described below .

3.4.1. Sniffing

During quadrupedal locomotion, pangolins exhibit short head movements directed towards its proximate environment in a upright ( below to above or frailty versa ) or horizontal plane ( left to right or frailty versa ) to the longitudinal axis of the body. such behaviours may contribute to detecting odours in air, locating feed, locating intruder or animal custodian, locating conspecific as a depart of social interaction between a mother and her young, and intimate olfactory property discrimination between the opposition sex individuals .

3.4.2. Bipedal Stand

Pangolins rise on their hind limbs and show sniffing demeanor ( Figure 1 ( j ) ). The forelimb remain folded and unblock. At times, pangolin exhibits supporting bipedal stand where pangolin rests its forelimb on concrete wall or on tree torso and explores the surroundings or interacts with other pangolins at neighbouring enclosures .

3.4.3. Secretive Look

At times, pangolin came out of burrow partially, that is, front tooth one-half of the body visible to the outdoor ( figure 1 ( kelvin ) ), and exhibits sniffing behavior .

3.5. Defensive Behaviours

When alarmed, pangolin rolls up into a ball as a defensive pose and may produce hissing sound. These behaviours are described here below.

3.5.1. Alert

It is the attainment of a brief fast state by the pangolin, interrupting any activity it was engaged in ; head points to the management of a noise source, if any ; it normally occurs in the presence of animal custodian. At times, such behavior may be followed by bipedal stand, sniffing, or movement of pangolin into a shelter, for exemplar, hollow wooden log or to the burrow, away from the source of randomness or animal custodian .

3.5.2. Defensive Postures

Upon hearing any threatening heavy, pangolin bends its head down, positioning it between the forelimbs ( figure 1 ( fifty ) ). In refutation, the pangolin curls itself into an armored ball, exhibiting an enormous muscular office which defies any ordinary undertake to uncoil it [ 4 ]. When captured from tail to make them uncoil, they rotate their body in both clockwise and counterclockwise along their longitudinal axis to escape from the grip. They use their back limbs to push out the defy. Upon sensing any intruder or threat, they move debauched into the burrow or climb over tree trunks or to the chain-linked argue .

3.5.3. Vocalisation

The alone good produced by the pangolin is a loud boo, normally under stress or agitation [ 4 ]. During the sketch menstruation, forte hissing sound was exhibited by the pangolins when disturb and during mating between opposite sexual activity individuals. At times, hissing strait was besides produced during exploration and mother-young interactions .

3.6. Reproductive and Social Behaviours

Behaviours which include interaction among two individuals except aggression were included in this behavioral class. such behaviours include a sequence of events that occur between opposite arouse adult individuals and interactions among beget pangolin and her young, where the action of one individual may evoke a behavioral response in the early. Seven such behaviours were described here below .

3.6.1. Courtship

At PCBC, pangolins were housed in such a means that a pangolin can find a probability to interact with the opposite sex individual housed in the adjacent enclosure. Though there was no target ocular contact between individual pangolins when they were on labor, occasionally they do climb up the pile, water pool, or chain-linked fence and interact with each other. such interaction includes a bipedal rack or resting position near the chain-linked argue and sniff or looking at the adjacent enclosure for presence of the opposite sexual activity individual. At times, while interacting in a climb military capability, urine may squirt out by either of the individuals. male pangolins were besides observed repetitively following the gait of a female pangolin housed in the adjacent enclosure. Considering the above behavior as courtship behavior, the antonym arouse individuals involved in such interactions were released in a concrete floored enclosure for mating determination under lament observation .

3.6.2. Approaching

It includes walking or climbing movement towards another individual followed by nosonasal or nosogenital sniff. The above demeanor may lead to exhibition of one of the three possible behaviours : ( i ) female pangolin may remain stationary, allowing male pangolin to mount ; ( two ) male may chase the female pangolin as she cursorily walks away ; ( three ) female pangolin may retreat, attaining a handbuild position, and the male walks away from her .

3.6.3. Chasing

It is quadrupedal motion exhibited by one pangolin to follow another pangolin of the opposite arouse. The speed of chasing gait is greater than the convention walk gait. A hanker period of sniffing between individuals occurs before chasing. occasionally while chasing, the male pangolin rose on its hind limb with forelimbs extended apart and walked bipedally few steps towards the female pangolin to mount her ( design 1 ( m ) ) .

3.6.4. Mounting

The male climbs up the female ’ s back from rear or side with his claw of forelimb grasping female ’ s body. The male fully extends his neck over the female ’ randomness head and remains analogue to her ( figure 1 ( normality ) ). The male adjusts his relative position with the female to attain an ideal sexual intercourse country. Mounting demeanor may contribute to testing the receptiveness of the female to copulate with. If the female was found receptive, mounting may lead to the future behavior, that is, sexual intercourse ; differently the female moves out of clasp and become hideaway .

3.6.5. Copulation

After obtaining an ideal pose with his neck amply extended to point at the female ’ sulfur head, the male grasps the female ’ s tail with his stern and inserts his genitalia to that of female ’ sulfur ( Figure 1 ( o ) ). sexual intercourse may occur in lateral mounting position. insertion may be conformed ( very difficult ) if semen was observed afterwards in the genitalia. Event terminated when individuals break bodily contact. Upon termination of sexual intercourse, the copulate move away individually and at times become retreat .

3.6.6. Retreat

withdraw may be observed in pangolins as a precopulatory or postcopulatory behavior in response to the antonym sexual activity individual. It includes coiling around itself into a musket ball on substrate ( like to resting postures ) or clinging on chain-linked fence or on dry tree proboscis ( Figure 1 ( p ) ). At times, male pangolin was observed mounting the female pangolin which was distillery in a withdraw position and tries to uncoil her by expelling/dragging the stern aside with the avail of his claw of forelimbs .

3.6.7. Mother-Young Interaction

indian pangolins normally give birth to individual young [ 3, 14 ], but occasionally two are born [ 4 ]. Births have been reported throughout the year except for May and June months [ 10 ]. A 10.6 kilogram female gave birth at Nandankanan Zoological Park, Odisha, to an offspring that weighed 235 gravitational constant and measured 30 curium in total duration including 12.5 centimeter long tail [ 14 ]. indian pangolins have a pair of mammary glands in their pectoral region. Young pangolin suckles from her beget while positioned amid mother ’ mho coiled consistency ( figure 1 ( q ) ). At times, pamper hides its headway underneath the ventral surface of her mother keeping its chase curling up mother ’ south body or tail. As the baby was growing, the mother pangolin used to relax its coil to accommodate the increasing size of the baby [ 8 ]. Young are carried on the dorsal base of the mother ’ mho tail [ 3, 15 ]. Young pangolin climbs on mother holding the tail basal of the mother pangolin with its limbs and its tail may remain latitude to that of the mother or go to a side ( digit 1 ( r ) ). When not riding, the young pangolin normally walks nearby her mother. The mother intermittently inspects the pamper pangolin. exploratory movement with intermittent sniffing behavior was observed in the beget pangolin, when the new pangolin moved to a distance. Repeated burrow inspection, that is, mother pangolin moves to the burrow and comes back after a short bust of staying inside the burrow, was observed when the young pangolin was present inside the burrow. When disturbed, the mother pangolin gets coiled into a sphere around the young pangolin [ 15 ] .

3.7. Other Behaviours

Some behaviours not included in the above behavioral categories, for exemplar, aggression, pace, cling, and signs of nausea, are described below .

3.7.1. Aggression

No direct observations were made of this particular behavior during the confront analyze. however, the evidence of death of a male pangolin on 25th July 2010 due to male-male aggression implied that pangolins ( at least male pangolins ) exhibit aggressive behavior. One of the male pangolin was seriously injured at its neck leading to his death. The wound appears to be caused by the claw of forelimb of the early male pangolin. The testify suggested that besides digging the hook are besides used for aggressive encounters .

3.7.2. Pacing

Pacing behavior was observed in two pangolins during study period. It includes repetitive quadrupedal walking movements in same path without any finish. Observed pace behaviours can be grouped into two types according to the condition of the path the pangolins normally follow while pace : ( one ) pacing in “ 8 ” shape ( Figure 1 ( s ) ) and ( two ) tempo in “ O ” shape ( Figure 1 ( triiodothyronine ) ). such behaviours are considered stereotypic and may associate with try due to suboptimal captive environment. Stereotypic behaviours are repetitive, unvaried, and apparently functionless behavior patterns which captive animals may develop as a response to physical restraint, miss of stimulation, or ineluctable fear or frustration. Independent evidence shows that they are associated with poor wellbeing [ 16 ] .

3.7.3. Clinging

Pangolins climb the chain-linked fence and remain in a cling military capability, preferably in high gear places with the avail of claws of their forelimbs and hind limbs and with support of their chase tiptoe. Head curled inward ventrally and intermittent urine spray were observed at times. Pangolins besides exhibit clinging behavior over the dry tree branches installed in the enclosure. They can remain clinging for solid day. Clinging may cause injury in limbs and make the animal stressed .

3.7.4. Signs of Sickness

The primary sign of good health status of pangolin is sound feed intake as they became off feed when vomit. even measurement weight unit of the individual pangolin can provide information about the overall growth and health condition as the pangolins were found to lose weight when ghastly. Body slant of an animal is associated with many features of physiology, ecology, and liveliness history and is besides an indicator of overall forcible condition [ 17 ]. regular observation for bearing of any injury and ectoparasites and for secretion from their natural orifices like scent, mouth, genitalia, and so forth can help to monitor their health condition. Pangolins with nasal consonant fire were observed producing a phone like “ umh ” repetitively as a signal of respiratory distress. At times, pangolin uses the presence limbs or hind limbs to scratch torso parts, credibly to get rid of ectoparasites ( ticks ) or other alien objects on the body. A vomit pangolin remains less active and spends more time in stationary model, for example, resting or sleeping. The chase of a healthy pangolin that normally is held off from grate while walking was found dragged when the animal is sick. sick individuals may develop an dip to spend more prison term laying inside water in pool. such behavior may lead to decline in normal body temperature, so it causes farther deteriorate of the health condition of the pangolin .

4. Discussion

In a captive situation, an understand of animal demeanor is all-important for the alimony of goodly and content animals. Any project that involves the captive care of animals groups should assign character of its resources for structuring its ethogram [ 18 ]. The present discipline addresses normally respect behaviours of indian pangolin and is wholly descriptive rather than quantitative. many of the behaviours performed by M. crassicaudata were like to that described for other pangolin species [ 19 – 22 ]. Although behavioral repertoire presented here was based on preliminary observations, it can be used as a ensnare of reference for details for behavioral studies of indian pangolin in the future. It is all-important for a good understand of physical, social, and psychological aspects of the animals that serves as an essential cock to meet farming and animal conservation goals [ 23 ]. feed was found to be the first behavior exhibited by indian pangolins once they emerge from their burrow. But, Thai et alabama. [ 22 ] reported defecation as an initial activity in prisoner Sunda pangolins ( M. javanica ). They have besides stated that most of the Sunda pangolins defecate in water and some individuals dig little holes in the reason and defecate inside these holes. During the present study, captive indian pangolins were normally found defecating on the substrate dirt, towards corner or peripheral areas of the enclosure. Defecation inside pool by two individuals was observed regularly during the summer season. Defecation inside small hole or near the opening of abandoned burrow was besides occasionally observed. Pangolins have very inadequate sense of imagination and hearing but an excellent sense of smell [ 3 ]. They frequently stand on their hind limb with head elevated to view the surroundings [ 3 ] and sniff intermittently for locating fertilize, intruder, and conspecifics. In the hazardous, pangolins dig both to reach at food resources ( for example, termites ) and to build live burrows [ 2, 4, 21 ]. Wet soils were found to be a choose locate for digging by pangolins at PCBC. Besides, when they were swapped into other enclosures, they dig out their own burrow rather of using the existing burrows of the previously housed pangolin. Observed sexual intercourse position of M. crassicaudata during the introduce study was like to that described for Cape pangolins ( M. temminckii ) [ 24 ]. social interaction between mother and young observed in indian pangolins appears to be similar to that described for chinese pangolins ( M. pentadactyla ) [ 21 ] and Cape pangolins ( M. temminckii ) [ 20 ]. Behaviours such as bathing inside pool, resting on back exposing the ventral airfoil of the body outward, and increased burrow utilization during winter months were believed to be associated with thermoregulation. Bathing behavior was observed regularly during the summer and showery season but rarely during the winter months. Bathing was besides observed as a postmating and postmounting demeanor in either of the individuals ( male/female ). Thai et alabama. [ 22 ] observed increase washup activity in M. javanica after feeding on live ants, which may help them to cool down, to reduce itch caused by ant pungency, or to remove ants from underneath scales. Jacobson et aluminum. [ 25 ] observed a female Cape pangolin laying in shade on her back exposing her belly during a hot day, permitting the animal to cool off. Pangolins were found exhibiting less overground activities during the winter months which might be associated with thermoregulation as the recorded temperature fluctuations inside burrow ( minimum to maximal temperature range = 17–24.5°C ) were apparently lower than that of the outside ( 15.5–34.5°C ) [ 26 ]. Increase in ambient temperature beyond 33°C may induce heat stress whereas abrupt decrease in temperature may cause pneumonia leading to death in taiwanese pangolins [ 27 ]. Thai et alabama. [ 22 ] stated that thermoregulation may play a character in the lower mortality rate of M. javanica residing in the “ pangolarium ” compared to the quarantine facility. Pacing was the only stereotyped behavior observed during the award report in two pangolins at the center. such demeanor has besides been observed in M. javanica and M. pentadactyla [ 19 ]. subsequent rearrangements of enclosure furnish or trade of pangolins among enclosures was found utilitarian to alleviate such behaviour. Thai et aluminum. [ 22 ] frequently observed some of the stress behavior in Sunda pangolins during quarantine period. These include quickly climbing on the enclosure telegram engagement and along the cable ceiling, running very promptly on the grate or branches, repeatedly putting their pass through the cable mesh while clawing at the engage, and scratching at the door of the enclosure. Pangolins displaying these behaviours lose weight, much hurt themselves, and normally die [ 22 ]. Though such behaviours are not observed in pangolins at PCBC, pangolins were found to lose weight unit when vomit and few days before death.

5. Conclusion

The present survey describing 27 different behavior patterns clustered in seven behavioral categories provides an initial framework for understanding the behavioral repertoires of indian pangolins. promote studies on behavioral biota of indian pangolins are urgently required for facilitation of both ex-situ and in-situ conservation of the species. Since a comprehensive examination cognition on behavioral biota of the indian pangolin is all-important for its management in enslavement, descriptions of this newspaper may besides useful in improving the farming and management of captive amerind pangolin and design future conservation efforts .

Conflict of Interests

The authors declare that none of them have a conflict of interests .

Acknowledgments

The authors are grateful to Central Zoo Authority ( CZA ), New Delhi for the fiscal back and the license to undertake the inquiry in the indian pangolins at Pangolin Conservation Breeding Center, Nandankanan Zoological Park, Odisha. We are grateful to Dr. L. N. Acharjyo, former veterinarian officer, NKZP, Odisha for going through the manuscript and for his valuable suggestions .

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