Influence of work on nutrient utilisation in semicaptive Asian elephants (Elephas maximus)

Abstract

Two feeding trials were conducted to evaluate the feed consumption, nutrient utilisation, blood biochemical and faecal microbial profile of working and nonworking semicaptive Asian elephant. During each trial, six captive elephants were placed in two groups of three each. Elephants in one group performed the scheduled work at the park, i.e., 4-h safari with tourists, while the other group performed no work. During nighttime, all the elephants were kept in respective individual enclosure so that feed consumption and faeces voided could be measured accurately. During day time, all the elephants were allowed to forage in nearby forest. Intake (kg/d) of sugarcane (Saccharum officinarum) and sugarcane leaves was more (P < 0.01) in nonworking elephants as compared to working elephants. Working elephants consumed more (P < 0.01) forages during foraging than nonworking elephants. Average daily dry matter intake (DMI) and DMI (% body weight, BW) were comparable between the groups. Apparent digestibility (%) of DM, OM, crude protein (CP), neutral detergent fibre (NDF), acid detergent fibre (ADF), hemicellulose, cellulose and gross energy (GE) were higher (P < 0.01) in working than nonworking elephants. Activity of ALT (IU/l) was higher in working as compared to non-working elephants. The relative population of Fibrobacter succinogenes and Ruminococcus flavefaciens and total fungi were numerically increased in working elephants as compared to nonworking elephants. It was concluded that 4 h of work has no adverse impact on food consumption and blood metabolite profile of semicaptive Asian elephants; rather it improved the digestibility of nutrients. Work showed positive effect in restricting the calorie supply closer to requirement.

Keywords:

• exercise/work
• Asian elephants
• nutrient utilisation
• microbial profile

View correction statement:

Erratum

This article was originally published with errors. This version has been corrected. Please see Erratum (http://dx.doi.org/10.1080/09712119.2013.889909)

1. Introduction

Elephants are generalist feeders. In wild, they forage on variety of plant materials. Their grazing behaviour is influenced by season and food availability (Sukumar 1989). Work conducted so far indicate that average daily dry matter intake (DMI) is 1–1.5% of body weight (BW) in adult elephants (Ullrey 1997) and young animals show little more DMI up to 2% BW (Loehlein et al. 2003). Elephants have capacious caecum and colon where fermentation of feedstuffs takes place. Various bacteria, protozoa, and fungi are present in hind gut which helps in degradation of fibre. Type and population of microflora are influenced by diet. Jenson (1986) reported that Asian elephants can derive 100% of their maintenance energy from volatile fatty acids (VFA) produced in the hind gut. Although their relative energy requirements are less, because of large size, elephants require large amount of food. Majority of these feedstuffs are poor quality roughages and characterised by low digestibility. Lesser mean retention time (MRT) and higher passage rate in elephants than other herbivores contributed to lower digestive efficiency (Loehlein et al. 2003). Consequently, Asian elephants have to graze for 12–16 h/d to fulfil their nutritional requirements (Sivaganeshan 1991).

Captive elephants in most of the national parks have to perform 4–6 h of touristic work. Effective grazing time may be reduced due to work as have been observed in horses (Fall et al. 1997). Thus, working elephants may not get sufficient foraging time to fulfil all their nutritional needs. However, reports indicate that captive elephants in zoos performing no work receive energy in excess of their requirement (Clauss et al. 2003). Giving exercise to such elephants could be beneficial as working animals could burn more energy as has been observed in horses (Frape 1994). Thus, there is need for a clear understanding of relation between work and nutrient utilisation in elephants. Specific objective of this experiment was to observe the effect of 4 h of touristic work on feed intake, diet digestibility, and blood metabolites in semicaptive Asian elephants (Elephas maximus). Secondary objective of the study was to generate baseline data on gut microbial profile of Asian elephants.

2. Materials and methods

2.1. Experimental site

This experiment was conducted at Jim Corbett National Park, Ramnagar, Uttarakhand, India, situated 385–1100 m above msl at longitude 78°5′E to 79°5′E and latitude 29°25′E to 29°40′N.

2.2. Animals and design of the experiment

Six semicaptive elephants at the Jim Corbett National Park were used for this experiment. Elephants were placed in two groups of three each. Elephants in one group performed the scheduled work at the park, i.e., 4-h safari with tourists, while those in other group performed no work. During nighttime, they were kept in respective individual enclosure (8 × 6 × 5.5 m) so that faeces of each individual could be collected separately and one animal had no access to the feed of the other. Concentrate offered consisted of wheat roti (wheat floor: 6 kg; water 2 l; common salt 150 g, and jaggery 500 g), 70% of which was offered to all the animals at 19:00 h and 30% at 05:00 h. All elephants were provided night shelter from 17:00 to 05:00 h. Rest of the time they were allowed to forage in the nearby grassland/forest. During nighttime, the animals were provided sugarcane (Saccharum officinarum).

Feeding cycle started at 05:00 h when each elephant was handfed wheat roti, after that working elephant went for work (tourist safari), while sugarcane was offered to non-working elephants when they were in their enclosure. However, working elephants had access to sugarcane only after 17:00 h. Working elephants returned from work at 09:00 h, and then all the elephants (working and nonworking) were allowed to forage in nearby forest. All elephants came back from foraging by 13:00 h. After foraging, they were allowed to take bathe from 13:00 to 15:00 h. After completion of bathe, all elephants were again allowed to forage up to 17:00 h. After this final foraging, all elephants were kept in their individual enclosure and were offered measured amount (∼40 kg) of tree branches (Ficus religiosa) and sugarcane leaves (∼40 kg). Sugarcane leaves are separated form stem and offered separately. At 19:00 h, all elephants were handfed remaining quota of concentrates. Prior to the experimental feeding, all the animals were dewormed with oxyclozanide (19 mg/kg BW). Proper managemental and sanitary guidelines as suggested by the Central Zoo Authority (CZA 2000) were followed during the course of experimentation.

2.3. Estimation of intake and digestibility

Two feeding trials were conducted. First trial was conducted after a preliminary period of 15 days followed by a collection period of 5 days. Similarly, the second trial was conducted during days 30–35. Faeces voided during 17:00 to 05:00 h when animals were in their individual enclosure was collected directly and measured. When animals were out (either for work, forage, or bathe), they were accompanied by one researcher and Mahout. Whenever elephant defecated, total amount of faeces was collected, weighed and sampled. Faecal samples for analysis were collected with care after removing outer layer of dung to avoid any soil contamination. On two occasions, elephants defecated in water stream, and it was not possible to collect that samples. To correct it, average weight of faeces per defecation for that particular elephant was added. Thus, total volume of faeces voided for 24 h was collected in full. Amount of sugarcane, sugarcane leaves, tree branches and concentrate offered to the elephants and their refusals was also measured correctly. Representative samples of forages consumed during foraging were also sampled. Feed consumption during foraging was measured indirectly using lignin as an internal marker. Body measurements were taken on day 0, 30 and 35 of the trial to calculate body weight. Heart girth was measured by encircling the measuring tape tightly around the chest just caudal to the elbows. BW was calculated using following formula (Hile et al. 1997):

Pedometers were used to monitor the distance travelled during each foraging day. Pedometers were calibrated regularly against a known distance.

2.4. Blood collection and analysis

Blood was collected at the end of feeding trial on d 35 at 07:00 h from all elephants by puncturing ear vein. Blood glucose and hemoglobin was determined on spot using glucose and haemoglobin metre (Medical Equipment India, Delhi). Serum was harvested and stored at −20°C in clean sterile vials and analysed for total protein, albumin, urea, cholesterol, creatinine, alanine transaminase (ALT), aspartate transaminase (AST) and alkaline phosphatase (ALP), using commercial diagnostics kits (Span Diagnostics Ltd., Surat, India).

2.5. Chemical analysis

Chemical composition of ground samples of feed/forages offered, refusals, and faeces was done as per the methods of Association of Official Analytical Chemists (AOAC 2005), and fibre and its fractions were analysed as described by Van Soest et al. (1991). Hemicellulose was calculated as the difference between neutral detergent fibre (NDF) and acid detergent fibre (ADF); similarly, cellulose was calculated as the difference between ADF and lignin. Gross energy (GE) content of feed, forages and faecal samples was analyzed using Ballistic Bomb Calorimeter (Gallenkamp, C.B.370, Expotech, USA. INC, Houston, Texas).

2.6. Hind gut microbial profile

Gut microbes, namely, total bacteria, Fibrobactor succinogenes, Ruminococcus flavefaciens, methanogens, and total fungi, were quantified by real-time PCR (qPCR) using faecal genomic DNA as a template. The isolation procedures of faecal genomic DNA were performed using the ZR faecal DNA kit (Zymo Research, CA, USA) as per manufactures instructions. The quality as well as quantity of the genomic DNA was determined using a Nanodrop spectrophotometer (Thermo Scientific, Wilmington, Delaware, USA). The samples with values between 1.8 and 2.0 were further processed for quantification of faecal microbes using real-time PCR (Biorad, Applied Biosystems, Hercules, CA 94547, USA). The 16S rRNA genes were amplified according to Chen et al. (2008) using the universal primers f5′- CGGCAACGAGCGCAACCC-3′, r5′-CCATTGTAGCACGTGTGTAGCC-3′ for total rumen bacteria, f5′-CGAACGGAGATAATTTGAGTTTACTTAGG-3′, r5′-CGGTCTCTGTATGTTATGAGGTATTACC-3′ for R. flavefaciens, and f5′- GTTCGGAATTACTGGGCGTAAA-3′, r5′-CGCCTGCCCCTGAACTATC-3′ for F. succinogenes, f5′-TTCGGTGGATCDCARAGRGC-3′, r5′- GBARGTCGWAWCCGTAGAATCC-3′ for methanogens and f5′- GAGGAGTAAAAGTCGTAACAAGGTTTC-3′, r5′-CAAATTCACAAAGGGTAGGATGATT-3′ targeting a portion of internal transcribed spacer 1 (ITS1) region for fungi. The PCR reaction was carried out in a real-time PCR machine using 2 µl of the template DNA, 10 µ1 KAPA SYBR^® FAST qPCR Kit master mix (^®KAPA Biosystems, Boston, USA), 0.6 µl each forward and reverse primers and 6.8 µl nuclease free water. The real-time PCR machine was programmed for denaturation at 95 °C for 10 min, followed by 40 cycles of 30 sec each for denaturation at 95 °C, annealing at 60 °C and extension at 72 °C. The amplified product specificity was determined by dissociation curve obtained by the cycle of 2 min at 95 °C, 15 sec at 60 °C and 15 sec at 95 °C. The population density of microbes was expressed considering control as 1.0 (Livak & Schmittgen 2001).

2.7. Calculations and statistics

Data obtained were analysed using student's “t” test (Snedecor & Cochran 1989) and treatment means were tested by applying Tukey's test by using SPSS software package, version 13 (SPSS, Chicago, IL, USA). Various microbial populations in the samples were analysed considering total bacteria as “housekeeping gene.” The real time PCR data were analyzed using 2^−ΔΔCt method as per Livak and Schmittgen (2001), where, ΔΔCt = (Ct of target gene − Ct of endogenous control gene) treatment diets − (Ct of target gene – Ct of endogenous control gene) control diet. The means of different treatments were separated using Tukey's test.

3. Results and discussion

3.1. Chemical composition of feeds and forages

Sugarcane was characterised by low crude protein (CP) and GE content. Concentrate (wheat roti) offered in this study was higher in GE and moderate in CP content. Tree branches contained moderate amount of CP and GE (Table 1). This trial was conducted during winter season (December–January). During this period, there is scarcity of forages in and around the Park area. Sugarcane is abundantly available during this period, and it is a common practice to feed sugarcane to captive elephants (Arora 2001). Sugarcane possesses high concentration of sucrose and other soluble sugars. The CP and NDF content of sugarcane observed in this study was similar to that reported by Pate et al. (2002). However, NDF contents of sugarcane were higher than earlier studies (López et al. 2003). This discrepancy could be due to different stages of maturity. In this experiment, mature sugarcane was used, whereas in earlier studies, premature sugarcane was fed. The CP contents of concentrate (wheat roti) fed to elephants was lower than earlier reports (Herrera-Saldana et al. 1990). This difference in CP content of wheat might be due to agronomic conditions (Brandt et al. 2000). Singh et al. (2009) reported 13.48% and 3.65% CP in tree leaves of F. religiosa. Tree branches (bark and stem) used in the present experiment contained more fibre, and less protein than the previous study. Such differences could be due to part of the plant used for analysis. We used bark and stem, whereas Singh et al. (2009) analysed only leaves, which contain more protein.

Table 1. Nutritional characteristics of feeds and forages fed to non-working and working semi-captive Asian elephants (during both the trials).

Parameters	Sugarcane	Sugarcane leaves	Roti	Tree branches^a	Forages^b
Trial I
DM (%)	41.25	34	52.74	48.1	40.14
Nutrient content (%DM)
OM	91	92.2	98	92.34	90.23
CP	4.3	7.4	9.84	7.61	9.89
NDF	62.85	58.88	34.69	73.8	71.5
ADF	47.74	45.12	18.1	51.42	42.58
Hemicellulose	15.11	13.76	16.59	22.38	28.92
Cellulose	43.83	35.7	16.76	28.72	25.25
GE (kcal/kg DM)	3554	3374.57	4215.47	3564.58	3623.42
Trial II
DM (%)	38.75	35.0	51.86	46.7	38.5
Nutrient content (%DM)
OM	90.26	92.78	97.12	90.86	91.45
CP	5.0	7.7	10.62	7.06	9.38
NDF	64.91	59.98	36.10	74.17	70.14
ADF	48.87	45.78	17.46	52.37	43.11
Hemicellulose	16.04	14.20	18.64	21.80	27.04
Cellulose	43.24	35.50	16.32	27.98	26.55
GE (kcal/kg DM)	3612.20	3612.20	4295.73	3645.71	3718.58

Note: DM, dry matter; OM, organic matter; CP, crude protein; NDF, neutral detergent fibre; ADF, acid detergent fibre; GE, gross energy.

^a Tree branches of F. religiosa.

^b Twenty-one species of forages were consumed during foraging (chemical composition given separately in Table 2).

During foraging, elephants consumed 21 species of grasses/trees/plants (Table 2). Based on the requirement of horses (NRC 1989), Ullrey (1997) recommended that Captive Asian elephants’ diet should contain a minimum of 8%. Out of 21 forage species consumed by elephants during trial period, 13 contained more CP than requirement, whereas 5 were moderately deficient. The results of the present investigation indicate that deficiency of protein is unlikely to occur to Asian elephants ranging in Jim Corbett National Park. Contents of NDF ranged from 61.3% to 84.6% and DM ranged from 28.2% to 60.6% in various foraged species during trial period.

Table 2. Chemical composition of forages consumed by Asian elephants during trial period.

				(%DM)
Botanical name	Local name	Part analyzed	DM (%)	OM	CP	NDF
Ageritum conizoides	Eelame	E	28.20	90.73	7.57	74.57
Dendrocalamus strictus	Bamboo	L	44.39	87.67	10.07	72.81
Butea monosperma	Dhok	L	47.06	92.88	16.49	67.38
Cynodon dactylon	Dub grass	R	47.00	90.16	11.31	84.62
Wrighlia tinctoria	Duddhi	E	36.65	92.22	15.94	61.58
Pennisetum purpureum	Elephant grass	R	38.23	94.14	10.79	64.64
Ficus glomerata	Gulhar	S	42.64	89.52	6.30	64.13
Scirpus kysoor	Kasela	E	30.21	92.17	9.25	69.97
Vetiveria zizanioides	Khash	R	31.00	94.08	5.03	71.74
Solanum dulcamara	Malpindi	E	30.11	89.40	9.21	73.38
Arundo donax	Narkul	E	29.46	90.86	6.15	68.11
Glynus lotides	Pillu	E	31.46	93.23	12.65	62.60
Holarrhana antidysentrica	Safeda	L	37.35	92.15	11.01	61.32
Shorea robusta	Sal bark	B	46.18	94.06	10.43	67.25
Bombax ceiba	Shemal	B	30.25	92.34	7.47	69.87
Thameda arundinacae	Ullaha grass	E	38.81	88.95	8.95	68.62
Thysanolaena maxima	Zadu grass	R	38.73	92.34	10.44	72.96
Ficus infectoria	Khabad	B	60.65	91.14	5.82	82.53
Ficus religiosa	Peepal	B	41.71	90.49	6.90	71.63
Ficus rumphii,	Pilkhan	B	48.20	91.57	8.49	68.07
Ficus bengalensis	Barh	B	30.20	90.24	6.72	75.42

Note: Br, branch; L, leaves; B, bark; E, entire plant; DM, dry matter; OM, organic matter; CP, crude protein; NDF, neutral detergent fibre.

3.2. Feed consumption, nutrient intake and apparent digestibility of nutrients

Intake (kg/d) of sugarcane and sugarcane leaves was more (P < 0.01) in nonworking elephants as compared to working elephants because sugarcane was available to them for longer period of the time. Working elephants, however, continued their foraging activities during work. Thus, they consumed more (P < 0.01) forages than nonworking animals. Both the groups consumed similar amount of tree branches. Consequently, DMI was comparable between the groups (Table 3). In free range, elephants graze for 16–18 h (Sivaganeshan 1991). In most of the national parks, semicaptive elephants have to perform work, e.g., tourist safari. Thus, working elephants may not get sufficient time to fulfil their nutritional requirement. Contrary to this belief, we observed that during working time, elephants continued their foraging. Consequently, DM intake of all animals was comparable in both groups, suggesting that DMI is not influenced by work. Caanitz et al. (1991) also observed no effect of exercise on feed intake in horses. The DMI observed in present study was higher than that recorded by Clauss et al. (2003) in adult Asian elephants fed hay-based diets. In this experiment, sugarcane was the primary ingredient which is relished by elephants (Lihong et al. 2007). Further, elephants had access to foraging during which there is considerable scope for selection. Nevertheless, the DM intake was within the range of 1.5–1.9% BW (Sukumar 1989) reported for elephants. Distance covered by working elephants during foraging was more (P < 0.01) than nonworking elephants (18 ± 09 vs. 12 ± 05 km/d) as measured by pedometer.

Table 3. Feed consumption, diet digestibility and nutrient contents of diets fed to nonworking and working semicaptive Asian elephants.

	Groups
Parameters	Non-working	Working	P-value
Feed consumption (kg/d)
Sugarcane**	29.77 ± 0.57	26.61 ± 0.36	0.001
Sugarcane leaves**	8.35 ± 0.19	7.33 ± 0.11	0.001
Roti	3.79 ± 0.02	3.85 ± 0.03	0.086
Tree branches^a	8.38 ± 0.15	8.11 ± 0.09	0.132
Forages^b **	13.72 ± 0.38	16.71 ± 0.13	0.001
DMI	64.00 ± 1.03	62.61 ± 0.44	0.228
DMI (%BW)	1.88 ± 0.03	1.80 ± 0.02	0.059
Nutrient intake (g/kg BW^0.75)
DM*	143.52 ± 2.01	138.44 ± 1.37	0.049
OM	133.34 ± 1.81	129.14 ± 1.35	0.076
CP*	11.01 ± 0.09	11.33 ± 0.12	0.049
NDF	90.72 ± 1.31	87.63 ± 0.78	0.055
ADF*	65.62 ± 0.92	63.32 ± 0.55	0.044
Hemicellulose	25.10 ± 0.39	24.32 ± 0.24	0.100
Cellulose**	48.97 ± 0.85	45.73 ± 0.49	0.003
GE (kcal/kg BW^0.75)*	521.37 ± 6.97	503.97 ± 4.67	0.050
DE (kcal/kg BW^0.75)**	198.53 ± 4.63	216.22 ± 3.07	0.004
Digestibility of nutrients (%)
DM**	36.39 ± 0.50	38.91 ± 0.68	0.007
OM**	40.78 ± 0.45	43.23 ± 0.66	0.006
CP**	48.58 ± 0.87	52.44 ± 0.75	0.003
NDF**	33.83 ± 0.60	37.01 ± 0.74	0.003
ADF**	33.83 ± 0.52	36.78 ± 0.78	0.005
Hemicellulose**	33.84 ± 1.08	37.63 ± 0.94	0.015
Cellulose	36.62 ± 0.75	38.16 ± 0.89	0.200
GE**	38.05 ± 0.60	42.96 ± 0.83	0.001
Body weight (kg)	3408.00 ± 62.47	3474.00 ± 49.77	0.233

Note: Means ( ± standard error) with different *differ significantly *(P<0.05) and **(P<0.01). SEM, standard error of mean; DM, dry matter; OM, organic matter; CP, crude protein; NDF, neutral detergent fibre; ADF, acid detergent fibre; GE, gross energy; DE, digestible energy.

^a Tree branches of F. religiosa. Working elephants perform 4-h tourist safari (work) and nonworking elephants perform no work.

^b Intake was estimated using lignin as an internal marker.

Apparent digestibility (%) of DM, OM, NDF, ADF, hemicellulose, cellulose and GE was higher (P < 0.01) in working than nonworking elephants. This improvement in digestion might be due to retention of particulate matter for a longer time in working elephants. Increased MRT as a result of exercise has been reported in horses (Orton et al. 1985), ungulate herbivores (Illius & Gordon 1992), and human (Wolin 1981). Positive effects of exercise/work on food digestibility may also be due to the improvement of microbial profile. In the present study, relative population of fibre-degrading microbes was numerically increased in working elephants. Matthewman and Dijkman (1993) reported better mixing of digesta in working animals resulting in improvement in microbial profile and digestibility. Similar increase in digestibility of DM, OM and NDF was also reported in horses after endurance work (Goachet et al. 2010).

Overall, CP contents of the consumed diets were 7.7% and 8.2% in nonworking and working elephants, respectively. Ullrey (1997) recommended 8% CP in the diet of adult elephants. Both the diets were adequate to meet maintenance requirements of CP for semicaptive Asian elephants. During exercise, wearing and tearing of muscle occurs, and nitrogen is also lost in sweat (Meyer 1987) which would increases CP requirement. To cope up with these losses, exercising animals generally increases the efficiency of utilisation of protein (Freeman et al. 1988). Increased absorption of protein was observed in present study, which could be beneficial for elephants. Similar observations have also been made earlier in horses and ponies (Orton et al. 1985; Pearson & Merritt 1991).

Digestibility of GE was higher in working than non-working elephants. Energy demand is increased due to work which causes animals to improve the energy absorption and utilisation (Fall et al. 1997). This is evident in the present study also as working elephants digested GE more efficiently than nonworking elephants. Energy requirement of elephant is not known. However, based on review of literature (Meyer & Coenen 2002; Clauss et al. 2005), DE requirements have been set at 144 kcal DE/kg BW^0.75 for maintenance, beyond which obesity was suspected. Further, 1.25 times maintenance DE has been recommended for working horses (NRC 1989). Using this estimate, DE requirement of working elephants would be 180 kcal DE/kg BW^0.75. Further, nonworking and working elephants were allowed to forage for 8 and 12 h, respectively. During that period, nonworking elephants and working elephants covered 12 ± 2 and 18 ± 3 km distance, respectively. Langman et al. (1995) reported that net energy (NE) expenditure in elephants during grazing was 0.186 cal/kg BW/m. Considering conversion factor of 0.80 from ME to NE (McDonald et al. 2002) and 0.90 from DE to ME (Reid & White 1978; Pagan & Hintz 1986; Robbins 1993), DE requirement for foraging elephants would be 0.258 cal/kg BW/m. Applying this factor to the BW of the animals in the present experiment, working and nonworking elephants will require 23.77 and 20.61 kcal DE/kg BW^0.75, respectively for foraging. In total, the DE requirement for nonworking and working elephants would be 164.61 (144 + 20.61) and 203.77 (180 + 23.77) kcal/kg BW^0.75, respectively. In the present experiment, DE intake in nonworking and working elephants was 198 and 216 kcal/kg BW^0.75, respectively. It is evident that nonworking and working elephants received 20.60 and 6.11% DE in excess of calculated requirements. We hypothesised that working elephants could burn more calories and may contribute to obesity reduction. Results of the present study show that physical work has got positive effect in restricting energy supply to semicaptive Asian elephants.

3.3. Blood biochemical and enzymatic profile

The levels of hemoglobin and blood glucose were similar between the groups (Table 4). Similarly, Gordon et al. (2006) reported that exercise has no effect on blood glucose levels in horses. The combined physiological response to maintain glucose levels is governed by hormonal regulation, autonomic nervous system and alterations in enzyme activities (Brooks et al. 2005). The glucose levels observed in the present experiment were similar with the levels recorded for Asian elephants fed on sugarcane stem and Pennisetum purpureum (Weerakhun et al. 2010). The concentrations of total protein, albumin, globulin, A:G ratio, urea, cholesterol and creatinine were not affected by work. Our findings are consistent with earlier findings in horses which indicate that serum concentration of total protein, albumin and creatinine remained same in working and nonworking animals (Graham-Thiers et al. 2000; Muhonena et al. 2008). Activity of ALT was higher (P < 0.01) in working elephants. Similar findings are also reported in rats (Wexler & Greenberg 1978). Increased ALT could indicate some amount of stress in working elephants; however, the values were within normal physiological range reported for Asian elephants (Ullrey & Allen 1986). Activities of AST and ALP were similar in both groups. Similarly, no significant change in serum AST (Anderson 1975) and ALP (Jackson et al. 2003) was observed in horses subjected to moderate exercise. The blood biochemical and enzymatic values were within normal physiological range reported for elephants (Ullrey & Allen 1986).

Table 4. Blood biochemical and serum mineral profile of nonworking and working semicaptive Asian elephants.

	Groups
Parameters	Nonworking	Working	P-value
Hemoglobin (g%)	10.34 ± 1.04	10.95 ± 0.66	0.628
Serum metabolites
Glucose (mg/dl)	108.50 ± 7.82	107.00 ± 11.47	0.916
Total proteins (g/dl)	6.13 ± 1.06	8.78 ± 0.21	0.064
Albumin (g/dl)	1.79 ± 0.18	1.79 ± 0.22	1.000
Globulin (g/dl)	4.34 ± 0.97	7.00 ± 0.38	0.078
A:G ratio	0.52 ± 0.11	0.27 ± 0.04	0.062
Urea (mg/dl)	48.16 ± 2.44	48.21 ± 3.05	0.991
Cholesterol(mg/dl)	69.62 ± 5.81	59.55 ± 4.57	0.203
Creatinine (mg/dl)	0.72 ± 0.04	1.09 ± 0.09	0.055
Serum enzymes
ALT (IU/l)**	22.50 ± 1.06	44.50 ± 3.44	0.001
AST (IU/l)	39.15 ± 1.67	42.53 ± 6.88	0.644
ALP (U/l)	68.43 ± 1.98	68.42 ± 4.28	0.999

Note: **Means (±standard error) differ significantly **(P < 0.01). SEM, standard error of mean; ALT, alanine transaminase; AST, aspartate transaminase; ALP, alkaline phosphatase.

Working elephants perform 4-h tourist safari (work) and nonworking elephants perform no work.

3.4. Gut microbial profile

The relative population of fibre-degrading bacteria and fungi was numerically higher in working than nonworking elephants (Table 5). Working animals retain digesta for longer period (Orton et al. 1985; Illius & Gordon 1992), which might have favored increased population of gut microbes in working elephants. This improvement in hind gut microbial profile was also reflected in improved digestibility of fibre components in working elephants. The microbial ecology of foregut fermenters is researched extensively (Sylvester et al. 2004; Denman & McSweeney 2006; Mosoni et al. 2007; Wanapat & Cherdthong 2009). However, the literature regarding microbial ecology of hindgut fermenters is limited to horses (Koike et al. 2000; Daly et al. 2001; Yamano et al. 2008). Results of present study serve as a baseline data for future research in this direction.

Table 5. Microbial expression and relative quantification of gut microbes of nonworking and working semicaptive Asian elephants.

	Groups
	Non-working	Working	SEM
Microbial expression
F. succinogenes	0.000238	0.005473	0.085755
R. flavefaciens	0.000019	0.000005	0.000005
Methanogens	0.000036	0.000055	0.000004
Total fungi	0.000291	0.000124	0.000113
Microbial population
Total bacteria	1.0	1.28
F. succinogenes	1.0	35.34
R. flavefaciens	1.0	2.37
Methanogens	1.0	0.52
Total fungi	1.0	1.65

Note: SEM, standard error of mean. Working elephants perform 4-h tourist safari (work) and nonworking elephants perform no work.

The major fibre degrading microbes in caecum of horses were R. flavefaciens, Ruminococcus albus and F. succinogenes (Lin & Stahl 1995; Julliand et al. 1999; Daly et al. 2001). Similar species of fibrolytic microbes were also observed in Asian elephants during the present study. utilisation of fibre is lower in elephants as comparison to horses (Clauss et al. 2003). As the concentration of total bacteria is similar between horses and elephants (Stevens & Hume 1995), it could be apprehended that proportion of fibrolytic bacteria is lower in elephants in comparison to horses. However, in this experiment, we observed that the relative proportion of F. succinogenes was maximal in comparison to other microbes. It seems unlikely that fibre degradation in elephant is less due to lower proportion of fibrolytic bacteria. Lower fibre digestibility in elephants could be mainly due to shorter MRT and faster passage rate (Weerasinghe et al. 1999; Loehlein et al. 2003).

4. Conclusion

Four hours of tourist work has no adverse impact on food consumption and blood metabolite profile of semicaptive Asian elephants, rather digestibility of nutrients was improved in working elephants. Work showed positive effect in restricting the calorie supply closer to requirement. It was concluded that 4 h of work is beneficial for captive Asian elephants.

Acknowledgements

Authors wish to thank the director, Jim Corbett National Park, staff of the park and the director, Indian Veterinary Research Institute, Izatnagar, for providing requisite facilities to conduct this study.

Notes

This article was originally published with errors. This version has been corrected. Please see Erratum (http://dx.doi.org/10.1080/09712119.2013.889909)