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Prevalence of Endo-parasites in Peafowls (Pavo cristatus) under Captivity Stress and Ameliorative Effect of Anti-Helminthic Drugs

PJZ_53_2_627-633

Prevalence of Endo-parasites in Peafowls (Pavo cristatus) under Captivity Stress and Ameliorative Effect of Anti-Helminthic Drugs

Arnab Tanveer, Shabana Naz*, Azhar Rafique and Asma Ashraf

Department of Zoology, Government College University, Faisalabad, Pakistan

ABSTRACT

A study was conducted to find the prevalence of endo-parasites in Pavo cristatus and the comparative efficacy of Albandazole and Levamisole against the endo parasites at three different locations viz. Jallo Wildlife Park Lahore, Wildlife Park Murree and Wildlife Park Bahawalnagar. Freshly dropped fecal sample were collected once before treatment with anthelminthic drug and twice after treatment and brought to laboratory for qualitative and quantitative analysis. Direct smear method and fecal floatation technique was used for isolation and identification of endo-parasites. Modified McMaster technique was used to calculate Eggs per gram. The data was subjected to ANOVA and Tukey-HSD (post hoc test). Six species of endo-parasites were identified from Jallo Wildlife Park. Eimeria (7500) and Ascaris (1100) were the most abundant. Murree Wildlife park had only two species i.e. Eimeria (3850) and Strongyloides (350). In Bahawalanagar Wildlife Park, 4 species of endo-parasites were found (Eimeria = 1450, Strongyloides = 550, Heterakis = 350 and Hymenolepsis = 550). Levamisole was more efficient against endo-parasites as compared to Albandazole. Efficacy of Levamisole at Lahore, Murree and Bahawalnagar wildlife parks after 15 days was 98.36%, 92.85% and 84.48% respectively as compared to Albandazole whose efficacy was 94.53%, 78.57% and 53.44%, respectively.


Article Information

Received 02 February 2019

Revised 16 May 2019

Accepted 13 November 2019

Available online 22 February 2021

Authors’ Contribution

AT collected the data and wrote the manuscript. SN designed the study. AR and AA analyzed the data.

Key words

Peafowls, Captivity stress, Endo-parasites, Albandazole, Levamisole, Anti-helminthic drug

DOI: https://dx.doi.org/10.17582/journal.pjz/20190202130259

* Corresponding author: drshabananaz@gcuf.edu.pk

0030-9923/2021/0002-0627 $ 9.00/0

Copyright 2021 Zoological Society of Pakistan



INTRODUCTION

A large number of wild animals and birds are kept in captivity. Captivity can be a zoo, wildlife park, sanctuary, breeding farm and privately owned farm. The purpose of keeping animals and birds in captivity can be conservation, recreation, economic benefits and research (Varadharajan and Kandasamy, 2000). Captivity produces stress in the birds which make them more susceptible to variety of infections as compared to their counterparts in the wild. Captivity stress could be limited space in the enclosures, overcrowding, unnatural habitat, unfriendly environmental conditions and suboptimal management (Athar et al., 2001; Parsani et al., 2003). Under captivity stress, birds also suffer from a number of behavioral problems, improper body functioning, reduced immunity, parasitism and stress-related health.

One of the major stress factors that reduce the performance of the birds is intestinal parasitism (Badran and Lukesova, 2006). Captive birds become susceptible to endo-parasites because of low space, over-crowded enclosures, poor hygiene, improper use of anti-helminthic drugs and finally poor and late health assessments. All these factors become the cause of easy transmission of endo-parasites from one bird to another (Pradeep et al., 2017). Consequently, the birds may suffer from subclinical conditions of anorexia, depression, emaciation, enteritis, and anemia (Forrester et al., 1978). The endo-parasites also damage the health of birds by consuming their nutrients leading to decreased feed utilization, intestinal obstruction and production of toxins and ultimately death may occur (Pradeep et al., 2017).

A broad range of drugs have been used against helminthes, however, resistance has been reported in small ruminants and other livestock animals (Saddiqi et al., 2006; Jabbar et al., 2008), probably affected by the intrinsic efficacy of the drug itself, pharmacokinetic properties, and susceptibility of the host animal and specificity of the parasite (Basit et al., 2014). The present study was conducted to determine the occurrence of endo-parasites in Indian peafowl kept in captivity and to find the efficacy of Albandazole and Levamisole against these endo-parasites at three different Wildlife Parks of Punjab.

 

MATERIALS AND METHODS

Study site

The present study was conducted at Jallo Wildlife Park, Lahore, Murree Wildlife Park and Bahawalnagar Wildlife Park to determine the rate of infestation by endo-parasites

 

Table I. Comparative pre-treatment EPG (mean±SE) and prevalence percentage of endo-parasites at Jallo Wildlife Park Lahore, Wildlife Park Murree and Wildlife Park Bahawalnagar.

Identified Endo-parasitic species

Quantitative analysis

Jallo Wildlife Park Lahore

Wildlife Park Murree

Wildlife Park Bahawalnagar

N

F

Level of

significance

Eimeria

EPG

250±71.99a

128.3±53.37b

48.33±22.9c

30

3.615

0.031

EPG

7500

3850

1450

Prevalence%

63.33

46.67

20

Ascaridia

EPG

3.33±3.33

00±00

00±00

30

1.00

0.372

EPG

100

0

0

Prevalence%

3.33

0

0

Strongyloides

EPG

1.67±1.66

11.67±5.71

18.97±8.38

30

2.180

0.119

EPG

50

350

550

Prevalence%

3.33

16.67

20

Ascaris

EPG

75±50.95

00±00

00±00

30

2.167

0.121

EPG

1100

0

0

Prevalence%

6.67

0

0

Heterakis

EPG

1.67±1.66

00±00

11.67±8.194

30

1.708

0.187

EPG

50

0

350

Prevalence%

3.33

0

6.67

Hymenolepsis

EPG

15±11.781

00±00

18.33±8.80

30

1.323

0.272

EPG

350

0

550

Prevalence%

10

0

13.33

Overall EPG

9150a

4200b

2900c

90

5.666

0.005

Overall prevalence%

70

56.67

46.67

 

EPG, Eggs per gram; SE, Standard Error; N, No. of birds; Means having different letters in a row are statistically significant (P<0.05).

 

at three different temperature ranges in the same season.

Treatment groups

For treatment of the peafowls with anthelminthic drugs, birds were randomly divided into two groups with 15 birds each. One group was given Albandazole (Group A) while other group was given Levamisole (Group L). Data was collected three times from the same site. Three treatment levels were set. Level 1 pre-treatment (Day 1), Level 2 post-treatment 1st (Day 7) and level 3 post-treatment 2nd (Day 15). Each post-treatment group was further divided into sub-groups for the treatment of Albandazole and Levamisole. Deworming was done after first sampling from all sites. Water was removed from peafowl cages one day before the administration of anthelminthic drugs. Drug was added to drinking water as per prescription on the label. It was given for three days. Water was changed daily and same process repeated again.

Collection of fecal samples

Freshly dropped fecal sample were collected in fecal cups and labeled properly (Keatts et al., 2016). Color, consistency, blood and mucus was noted for each fecal sample. Samples were stored in pack of handling bags with ice packs for safe transport. All samples were analyzed within 24 h of collection (Kathiravan et al., 2017).

Parasitological examination

Direct smear method and fecal floatation technique was used for qualitative analysis of gastrointestinal parasites (Hodgson, 1970; Fowler, 1978; Soulsby, 1982). Endo-Parasites were identified using identification keys by Jaiswal et al. (2013). Modified McMaster technique was used for quantitative analysis (Titilincu et al., 2009). Eggs per gram (EPG) was calculated by using formula: EPG= (Chamber 1 + Chamber 2) ×50 (Titilincu et al., 2009).

Drug efficacy

Drug efficacy was calculated using the following formula (Basit et al., 2014):

Table II. Comparative EPG and prevalence percentage of endo-parasitic species in Indian Peafowl at Wildlife Park of Lahore, Murree and Bahawalnagar.

Site

Species

Control

Albandazole

Levamisole

Day 7

Day 15

Day 7

Day 15

Jallo Wildlife Park, Lahore

Eimeria

EPG

7500

500

250

250

150

Prevalence%

63.33

53.33

20

33.33

20

Ascaridia

EPG

100

0

0

0

0

Prevalence%

3.33

0

0

0

0

Strongyloides

EPG

50

0

0

0

0

Prevalence%

3.33

0

0

0

0

Ascaris

EPG

1100

0

0

0

0

Prevalence%

6.67

0

0

0

0

Heterakis

EPG

50

0

0

0

0

Prevalence%

3.33

0

0

0

0

Hymenolepsis

EPG

350

0

0

0

0

Prevalence%

10

0

0

0

0

Wildlife Park Murree

Eimeria

EPG

3850

900

350

600

300

Prevalence%

46.67

33.33

33.33

33.33

26.66

Ascaridia

EPG

0

0

0

0

0

Prevalence%

0

0

0

0

0

Strongyloides

EPG

350

0

0

100

0

Prevalence%

16.67

0

0

33.33

0

Ascaris

EPG

0

0

0

0

0

Prevalence%

0

0

0

0

0

Heterakis

EPG

0

0

0

0

0

Prevalence%

0

0

0

0

0

Hymenolepsis

EPG

0

0

0

0

0

Prevalence%

0

0

0

0

0

Wildlife Park Bahawalnagar

Eimeria

EPG

1450

950

300

850

450

Prevalence%

20

20

33.33

20

20

Ascaridia

EPG

0

0

0

0

0

Prevalence%

0

0

0

0

0

Strongyloides

EPG

550

400

200

350

0

Prevalence%

20

13.33

20

20

0

Ascaris

EPG

0

0

0

0

0

Prevalence%

0

0

0

0

0

Heterakis

EPG

350

0

0

0

0

Prevalence%

6.67

0

0

0

0

Hymenolepsis

EPG

550

0

0

0

0

Prevalence%

13.33

0

0

0

0

 

Prevalence percentage

Prevalence percentage was calculated by using formula:

Data analysis

Results were analyzed using SPSS software. Normality and homogeneity of variances were checked for all variables. The data was subjected to one-way ANOVA. Tukey-HSD test was performed as a post hoc test for pairwise comparisons of means. Significance level was set at P < 0.05. Standard Deviation (SD) in post treatment analysis (Table IV) was greater than mean because data was widely distributed about mean. The SD is a description of data’s spread. Large SD indicates the data are more spread out while smaller SD shows that data clustered around the mean value. After treatment number of eggs per sample varied from zero (no eggs) to few hundreds (e.g. 200, 500 etc.). Since data had very vast spread about, it had larger SD than mean (Zar, 1999Isotalo, 2001).

RESULTS

The results of parasitic egg count of different gastrointestinal parasites in Jallo Wildlife Park Lahore, Wildlife Park Murree and Wildlife Park Bahawalnagar are given in Table I. Eimeria (Fig. 1A) was significantly high (P<0.05) in Jallo Wildlife Park compared to Wildlife Park Murree and Wildlife Park Bahawalnagar. Similarly, overall egg count was also significantly high at Jallo Wildlife Park Lahore as compared to the other two parks. There was no significant difference in Ascaridia (Fig. 1B), Strongyloides (Fig. 1C), Ascaris (Fig. 1D), Heterakis (Fig. 1E) and Hymenolepsis (Fig. 1F) in the three locations.


 

As shown in Table II and III, Levamisole was more effective than Albandazole at all three sites. Efficacy of Levamisole at Lahore, Murree and Bahawalnagar after 15 days was 98.36%, 92.85% and 84.48%, respectively as compared to Albandazole whose efficacy was 94.53%, 78.57% and 53.44%, respectively.

In post-treatment fecal analysis, only two species were found. That is why all null results were excluded from statistical analysis (Table IV). Eimeria and Strongyloides EPG varied significantly in post treatment levels (F=3.749, P=0.054; F=2.323, P=0.017) and at each site (F=3.141, P=0.046; F=5.086 P=0.07).

Table III. Drug efficacy of Albandazole and Lavamisole at Wildlife Park of Lahore, Murree and Bahawalnagar.

Anthelminthic drugs

Post treatment(7)

Post treatment(15)

EPG

Efficacy %

EPG

Efficacy %

Lahore

Albandazole

Levamisole

500

94.53

250

97.26

250

97.26

150

98.36

Murree

Albandazole

Levamisole

900

78.57

350

91.66

700

83.33

300

92.85

Bahawalnagar

Albandazole

Levamisole

1350

53.44

600

79.31

1200

58.62

450

84.48

 

EPG, Eggs per gram.

DISCUSSION

Qualitative and quantitative analysis of end parasites

It was observed that there is a strong correlation between the prevalence of end parasites and temperature of the areas of the study. A total of 30 samples were analyzed before treatment from each site. Overall prevalence of endo-parasites in Jallo Wildlife Park, Wildlife Park Murree and Bahawalnagar was 70%, 56.6% and 46.6%, respectively. Zamora-Vilchis et al. (2012) conducted a study on the prevalence of end parasites in lowland and upland areas and found that the parasites were more prevalent in the areas with higher temperature as compared to upland areas. Prevalence of End parasites in peafowls kept at Bhawalnager wildlife Park is less than that of Lahore which can be explained as the moist conditions favor the outbreak of end parasites (Card and Nesheim, 1972; Matter and Oester, 1989). These results are in accordance with results (56.32%.) of Basit et al. (2014). Results of current study also related to Lierz et al. (2002). He studied endo-parasites in 84 birds of prey and owls in Germany with overall prevalence of 58.3%. Similar trends can be seen in studies of Patel et al. (2000) who reported 48% overall prevalence, 68% was reported by Wojcik et al. (1999) and Varghese (1987) concluded 67.3%. Pal and Ahmed (1985) reported 69% overall prevalence whereas Kurt and Acici (2008) found prevalence percentage of 88%. Phiri et al. (2007) found that 95% of the study birds were infected. Eshetu et al. (2001) reported prevalence of 91.01% while Poulsen et al. (2000) reported 100% prevalence of endo-parasites.

 

Table IV. Comparative analysis of post-treatment EPG mean±SE of Eimeria and Strongyloides at Wildlife Park of Lahore, Murree and Bahawalnagar (n=45).

Eimeria

Strongyloides

PostA1

PostL1

PostA2

PostL2

PostA1

PostL1

PostA2

PostL2

L

33.3±1.1a-a

10± 0.7b-a

16.6±3.1c-a

10± 0.7b-a

00±00

00±00

00±00

00±00

M

60± 1.29a-b

40±1.6b-b

23.3±1.6c-b

20±1.4d-b

00±00a-a

6.6±1.5b-a

00±00a-a

00±00a-a

B

63.3±1.87a-c

56.6±1.7b-c

20±1.6c-c

30±1.9d-c

26.6±0.3a-b

23.3±1.5b-b

13.3±2.6c-b

00±00d-b

Total

52.2±1.8a-c

35.5±1.5b-d

20±3.9c-c

20±4.7c-d

8.8±2.5a-c

10±1.2b-c

4.4±1.9c-c

00±00d-c

 

N, Total no. of samples examined; Means having different letters in a row or in a column are statistically significant (P<0.05). PostA1, Post-treatment First, subgroup Albandazole; PostL1, Post-treatment First, subgroup Levamisole; PostA2, Post-treatment Second, subgroup Albandazole; PostL2, Post-treatment Second, subgroup Levamisole; L, Lahore; M, Murree; B, Bahawalnagar.

In the present study prevalence of Heterakis in two sites was very low compared to other studies. Heterakis prevalence was 3.33% in Jallo, and 6.67% in Bahwalnagar while in fecal samples from Muree Wildlife Park no Heterakis was found. On the contrary in a study by Basit et al. (2014), relative prevalence of Heterakis was 36.73% and 29% was reported by Kurt and Acici (2008) in a study on chicken. Prevalence of Ascaridia in current study was 3.33% and it was found only in Jallo Wildlife Park. Contradicting results are seen in study by Basit et al. (2014) who found 26.53% prevalence of Ascaridia and 28.8% was reported by Phiri et al. (2007).

Relative prevalence of endo-parasites in Indian Peafowl at Jallo Wildlife Park was maximum i.e. 70% followed by 56.67% in Murree and 46.67% in Bahawalnagar Wildlife Park (Table I). Number of infected birds were more at Jallo Wildlife Park (21) and Wildlife Park of Murree (21) as compared to Bahawalnagar (14). It is established fact that better management conditions lessen the chances of parasitic infections. This claim is also supported by Sascnyanga (1982) where he reported the infestation by Ascaridia galli was more (49%) in birds kept under ordinary conditions and only 8% A. galli were found in birds under good conditions. He further added that changes in prevalence of endo-parasites at various localities might be due to changed climatic conditions and management practices. Higher prevalence rate like 88%, 95.2% 91.01% and even 100% is reported by Kurt and Acici (2008), Phiri et al. (2007), Eshetu et al. (2001) and Poulsen et al. (2000) respectively.

Drug efficacy

In present study it was found that Levamisole was more effective than Albandazole at all the three sites. Efficacy of Levamisole at Jallo Wildlife Park Lahore, Murree Wildlife Park and Bahawalnagar Wildlife Park after 15 days was 98.36%, 92.85% and 84.48% respectively compared to Albandazole with efficacy of 94.53%, 78.57% and 53.44% in respective Wildlife Parks and are in accordance with Basit et al. (2014) who found the efficacy of Albandazole being 94.92% at 10th day. Ashraf et al. (2002) observed 95.79% efficacy of Albandazole against endo-parasitic nematodes. Similar trend was observed by Villanua et al. (2007). In a study on Red Legged Partridges, efficacy of Albandazole against endo-parasites was only 38.8%. Khan et al. (2010) concluded that Albandazole was more effective (96.33%) than Levamisole (84.90%). However, a study by Sharma et al. (1989) and Clarkson and Beg (1970) reported results similar to current study. They stated that Levamisole was 100% effective against endo-parasites as it inhibits activity of malate dehydrogenase.

In present study Albandazole and Levamisole were 100% efficient against all endo-parastites except Eimeria. Jiang and Li (1985) found 100% efficacy of Albandazole against A. galli. Albandazole was 100% effective against Strongyloides in both sites except in Wildlife Park Bahawalnagar where after 15 days prevalence of Strongyloides was 20% with EPG of 200. This anomaly in efficacy may be attributed to genetic resistant of namatodes against repetitive use of Albandazole. Schou (2003) also observed a similar trend. He reported that nematodes in cattle showed resistance to use of Albandazole as dewormer especially A. galli.

CONCLUSION

Levamisole has better effect against gastrointestinal parasites as compared to Albandazole. Albandazole is a commonly used dewormer and endo-parasitic species are developing resistance against it. So it is recommending that with proper hygiene measures, good management practices and use of different dewormers, especially with Levamisole, we may be able to reduce the infestation of animals and birds in captivity by endo-parasites and reduce economic loss.

ACKNOWLEDEMENT

We are thankful to Higher Education Commission (HEC) of Pakistan for providing financial support to this research work under the Project No. 5656/Punjab/NRPU/R&D/HEC/2016. Thanks are also extended to Mr. Kahlid Ayas, Dr. Zahid Farooq, Mr. Zahid Ali and Mr. Muhammad Abrar, Punjab Wildlife Department for granting permission and technical assistance to conduct this research. We are also grateful to Dr. Rifat Ullah Khan, Department of Animal Health, The University of Agriculture Peshawar, for editing this paper.

Statement of conflict of interest

Authors have declared no conflict of interest

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Pakistan Journal of Zoology

February

Vol. 53, Iss. 1, Pages 1-400

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