Overall parasitic prevalence
Out of the total 180
T. indica consisting of 79 males, 101 females, 58 mature and 122 immature ones trapped from crop fields, 33 (18.33%) were found infected with four species of nematode parasites
viz. Syphacia muris,
Trichuris muris,
Nippostrongylus brasiliensis and
Calodium hepticum. Maximum numbers of gerbils (13, 39.40%) were infected with
N. brasiliensis followed by
T. muris (7, 21.21%),
C. hepticum (7, 21.21%) and
S. muris (6, 18.18%). Out of total 173 nematode parasites found in the intestine of
T. indica, maximum number of parasites were of
S. muris (134, 77.46%) followed by
N.
brasiliensis (25, 14.45%) and
T. muris (14, 8.09%). Developmental stages of
C. hepticum were found infecting the liver. In contrast to present study,
Pakdel et al., (2013) found comparatively less infestation of
C. hepaticum (3.62%),
T. muris (14.49%) and
S. muris (2.89%) in wild rodent species. They did not report
N. brassiliensis infection.
Harandi et al., (2014), however, found 40% gerbils infected with nematodes in Iran. This variation can be due to the differences in climatic conditions of different study areas. In accordance with our findings,
Kataranovski et al., (2011) observed infection of
N. brassiliensis,
C. hepaticum,
T. muris and
S. muris alongwith
Heterakis spumosa in Norway rat,
Rattus norvegicus. Recently,
Mohtasebi et al., (2020) found wild rodent species,
Dryomys nitedula infected with
T. muris and a species of genus
Syphacia alongwith other helminthes.
Arzamani et al., (2017) identified
T. trichuris and
N. brassiliensis along with
Syphacia oblevata in rodents inhabiting Iran.
Morphometric analysis of eggs found in faecal samples
Faecal examination revealed the presence of eggs of three nematode species
i.e. S. muris, N. brasiliensis and
T. muris. The eggs of
S. muris were 72.50-82.25μm long and 22.00-36.50 wide. These were asymmetrical, slightly flattened on one side and curved on the other side (Fig 1a). The eggs of
T. muris were 67.50-70.75 µm in length and 35.00-40.50 µm in width having plugs at both the poles giving them acharacteristic bipolar shape (Fig 1b). The eggs of
N. brasiliensis were comparatively small and ellipsoidal inshape. They had a thin shell and measured 50.00-70.00 µm in length and 27.00-40.00 µm in width (Fig 1c). Eggs
C. hepaticum were not found in faeces but histopathology of infected liver revealed the presence of eggs entrapped in liver parenchyma. These were 55.00-72.50 μm in length and 32.50-40.00 μm in width. The parenchyma showed granular degeneration, necrosis and microgranulomas (Fig 1d). In contrary to present study,
Sharma et al., (2013) observed eggs of
C. hepaticum in faecal samples along with eggs of
S. muris, T. muris and other strongyle eggs.
Morphology and morphometery of adult worms
Length of the adult worm of
S. muris inhabiting the ceacum of
T. indica varied from 1.20-3.40 mm. They had characteristic oesophageal bulb at the anterior region (Fig 2a).
T. muris was a small nematode of 10.00-20.00 mm length with cylindrical non-segmented body in caecum (Fig 2b, c).
N. brasiliensis (10.50-20.00 mm in length) was found to inhabit small intestine and ceacum. The males were having characteristic bursa at the posterior end (Fig 2d).
C. hepaticum infection was found in the liver of
T. indica in the form of pale yellowish lesions on the surface of liver (Fig 3).
Community characteristics
Shannon-Weiner index and Species Evenness of different nematode species found in
T. indica were maximum in monsoon season (1.04 and 0.94, respectively) followed by winter (0.80 and 0.72, respectively) and summer seasons (0.45 and 0.40, respectively). Also these indices were more in female (0.77 and 0.70, respectively) and mature (1.01 and 0.91, respectively) gerbils as compared to male (0.70 and 0.63, respectively) and immature (0.43 and 0.39, respectively) gerbils. In all, nematode parasites were more diverse and evenly distributed in monsoon season as compared to summer and winter seasons. Overall Shannon-Weiner index (0.74) and Species Evenness (0.67) for nematode parasites were low in present study indicating less equitable distribution and abundance of species.
Percent infection and risk assessment
Total six (3.33%) gerbils were found infected with
S. muris. Higher infection rate was found in immature (4.10%) and male (5.06%) gerbils during summer season (6.67%). However, statistically, season (c
2=3.10, P=0.21 and df=2), age (c
2=0.68, P=0.40 and df=1) and sex (c
2=1.3, P=0.25 and df=1) had no significant effect on the infectivity of
S. muris. Mean parasitic intensity and abundance were also more in summer season (24.75 and 1.65) in immature gerbils (23.60 and 0.96) indicating higher chances of infection of
S. muris from immature gerbils during summer season. The mean parasitic intensity was more in female (27.50) gerbils, while the mean parasitic abundance was more in male (1.00) gerbils. The relative risk of occurrence of
S. muris infection was more in summer season (3.99) through immature (2.38) and male gerbils (2.55) (Table 1).
Total seven (3.89%) gerbils were found infected with
T. muris. Higher rate of infection was observed in mature (5.17%) and female (4.95%) gerbils in summer season (3.33%). Mean parasite intensity was higher in male gerbils (4.50), while it was similar across the seasons and age groups. Mean parasite abundance of
T. muris was more during monsoon season in mature male gerbils (Table 1). Mature (1.58) and female (1.96) gerbils had relatively higher risk associated with them with respect to transmission of
T. muris infection in summer season (3.33) (Table 1). But, statistically, the season (c
2=0.29, P=0.86 and df=2), host age (c
2=0.37, P=0.53 and df=1) and sex (c
2=0.69, P=0.40 and df=1) had no significant effect on
T. muris infection.
Total thirteen (7.22%) gerbils were found infected with
N. brassiliensis with higher rate of infection in mature (15.52%) and male (10.13%) gerbils in monsoon and summer seasons (8.33% each). Statistically, the infestation of
N. brassiliensis was not found to be affected by season (c
2=0.66, P=0.71 and df=2) and sex (c
2=1.77, P = 0.18 and df=1) of the host. But age of the host significantly affected rate of
N. brassiliensis infection (c
2=8.78, P=0.003 and df=1). Mean parasitic intensity and abundance were highest in monsoon season (2.20 and 0.18, respectively). Mean parasitic infestation was higher in mature (0.31) male (0.18) gerbils.
Liver of seven (3.89%) gerbils was found infected with
C. hepaticum with higher infection in immature (4.92%) and female gerbils (4.95%) during summer season (10.00%). Statistically, it was observed that season had direct impact on the infestation of this nematode (c
2=9.21, P=0.01 and df=2). No significant difference was, however, observed for host age (c
2=1.07, P=0.30 and df=1) and sex (c
2=0.69, P=0.40 and df=1). Relatively higher risk of
C. hepaticum infection was found associated with immature (2.50) and female (1.96) gerbils during summer season (5.99). Liver of infected animals was found containing numerous eggs of this parasite, however, the adult parasites could not be retrieved. No
C. hepaticum infection was observed in winter season. In contrast to our study,
Kataranovski et al., (2011) observed
Capillaria sp. infection in rodents in winter season. Although rare,
C. hepaticum is responsible for hepatic capillariosis in humans from different parts of the world (Fuehrer 2014).
Similar to present study,
Moudgil et al., (2018) gave morpho-pathological description of fatal concurrent intestinal and renal parasitism in
Columba livia domestica in India
. In present study, a significant effect was observed of host age on
N. brassiliensis infection (being higher in mature gerbils) and season (being higher in summer season) on
C. hepaticum infection. This finding was seconded by the study of
Hernandez et al., (2020) conducted in Southern Guatemala who observed higher infection of
Nippostrongylus sp. in mature male rodents. However,
Kataranovski et al., (2011) did not find effect of host age on any of the nematode infections. Rather they found significant affect of sex on the prevalence of
T. muris and
C. hepaticum.
Coomansingh et al., (2009) reported that
N. brasiliensis infection in adult rodents was much more than any other endoparasite infection which is in agreement with our present study. With
N. brasiliensis infection, there is T-cell mediated immune response stimulation in the host resulting in expulsion of worms, however, this phenomenon fails to develop when infection occurs in rats having age less than 6 weeks and thus worms persist into adult life (Wakelin 1996). This could be the reason why
N. brasiliensis infection was more in mature gerbils. Overall, in present study, higher nematode infection was observed in summer season as compared to winter and monsoon season as also observed by
Kataranovski et al., (2011) which may be due to more foraging activity of rodents in summers thereby increasing their vulnerability to parasites (Eccard and Herde 2013;
Tijjani et al., 2020). On the other hand, higher prevalence of nematode parasites was observed in sheep during winter and monsoon than in summer season by
Pazhanivel et al., (2004). Pawar et al., (2020) have also reported higher nematode infestation (70.58%) in captive wild animals. The presence of these nematode parasites in gerbils suggests the potential risk of rodent-borne disease transmission.
