Printer Friendly

Comparative Seasonal Haematology of Two Bat Species, Scotophilus heathii and Pipistrellus pipistrellus, in a Subtropical Area of Pakistan.

Byline: Nosheen Rashid, Muhammad Irfan, Muhammad Sajid Nadeem and Asghar Shabbir

Abstract

Various haematological parameters of two bat species belonging to the family Vespertilionidae (Scotophilus healthii and Pipistrellus pipistrellus) were examined on the seasonal basis. Blood samples were taken from 47 bats (23 S. heathii and 24 P. pipistrellus) captured from Potohar region. Results showed that P. pipistrellus exhibited significantly (P<0.05) higher mean counts of red blood cells (RBCs), white blood cells (WBCs), platelets, haemoglobin (Hb), and packed cell volume (PCV) as compared to S. heathii. However, mean corpuscular volume (MCV), mean corpuscular haemoglobin (MCH) and mean corpuscular haemoglobin concentration (MCHC) levels were significantly (P<0.05) higher in S. heathii as compared to P. pipistrellus.

Seasonal comparisons in both the species depicted lowest levels of RBCs, WBCs, MCV, MCH and PCV in spring when bats are least active just after hibernation. Highest mean estimates of RBCs, Hb, and PCV were observed in summer (bats are most active) in male and female bats belonging to both species. However, WBCs levels were at peak during autumn when bats are preparing to go into hibernation.

Key words: Seasonal variations, Haematological parameters, Vespertilionid bat, S. heathii.

INTRODUCTION

Microchiropterans particularly vespertilionid bats feed on insects and may play an important role in the agro-ecosystems of Pakistan. In spite of their usefulness, bats are symbol of fear and disgust in Pakistan and among the least studied mammals in Pakistan (Robert, 1997; Walker and Molur, 2003; Mahmood-ul-Hassan and Nameer, 2006). A few studies have been conducted on the ecology and distribution of bats in Pakistan (Mirza, 1967; Eates, 1968; Murray, 1884; Nadeem et al., 2013). A greater understanding of the biology of bats may be essential for the development of future management or conservation strategies. In this context, seasonal hematological studies are very important which are required for the differential diagnosis of normal and pathological conditions (Gulland and Hawkey, 1990; Campbell, 1992).

Blood profile also provides assistance in the studies based on nutritional status of animal populations, which are conducted for the evaluation of their physiological conditions (Dawson and Bortolotti, 1997; Heard and Whittier, 1997). The blood profile is affected by a number of factors which may be external such as the season, time of the day, food availability and quality as well as by age, gender, reproductive state and the changes in the concentration of different metabolites inside the body of an animal (Wolkers et al., 1994; Minemastue et al., 1995).

Keeping this in view we hypothesized that blood profile tends to change with the change of season, gender and species in microchiroptera. Furthermore, the time of activity may have an association with the levels of haematological parameters in the hibernating mammals. The present study was designed to investigate seasonal variations in haematological parameters of two species of vespertilionid bats; Scotophilus heathii and Pipistrellus pipistrellus, widely distributed in Pakistan . These species reproduce in spring and early summer (March to May) after arising from hibernation (January to February), and hibernate in winter (December to January).

MATERIALS AND METHODS

Study area

The present study was conducted in the Potohar plateau (32.5degN to 34.0degN Latitude and 72degE to 74degE Longitude), a subtropical arid region with a 350-500 mm/ annum rainfall, is forming the northern part of the province Punjab, Pakistan. The average temperature varies from 7.9oC in winter to 30.6oC in summer.

Sample collection

A total of 47 microbats belonging to two species, i.e. Scotophilus heathii (n=23; 12 male and 11 female) and Pipistrellus pipistrellus (n=24; 12 male and 12 female) were subjected to the present study. Bats were collected throughout the year from different areas in the Potohar region by using mist-net. As both the bat species are hibernating, specimens were not found during winter season (December to February) (Table I). After capturing, bats were immediately brought to the Wildlife Laboratory, Department of Zoology, Pir Mehr Ali Shah, Arid Agriculture University Rawalpindi and identified by using standard key (Bates and Harrison, 1997). The blood samples of the captured adult bats were taken in heparinized syringes through median venipuncture, and poured in the heparinized vacutainers.

Table I.- Bats (n=47) included in the present study

###S. heathii###P. pipistrellus

Season###(n=23)###(n=24)

###Male###Female###Male###Female

Spring (Mar-May)###3###3###5###4

Summer (Jun-Aug)###4###5###3###4

Autumn (Sep-Nov)###5###3###4###4

Winter (Dec-Feb)###---###---###---###---

Total###12###11###12###12

Blood cells counting

Red blood cells (RBC), white blood cells (WBC) and platelets were counted manually by using Neubauer haemacytometer by diluting the blood samples with solutions commercially available for RBC, WBC and platelet counting. The red cell indices, the mean corpuscular volume (MCV), mean corpuscular haemoglobin (MCH) and mean corpuscular haemoglobin concentration (MCHC) were calculated by using the standard formulae (Wintrobe, 1933).

Haemoglobin estimation and haematocrit

Haemoglobin (Hb) was measured by using Sahli's haemometer. For the estimation of hematochrit, plain microcapillary tubes were used. The tubes were centrifuged at 12000 rpm for five minutes in microhaematocrit centrifuge. Haematochrit readings were carried out by using a micro-haematocrit reader (NUVE, NF-048 Turkey).

Statistical analysis

The haematological parameters are shown as Mean+-S.E. Overall comparisons of haematological parameters in species were done by using student's t-test. However, seasonal comparisons were done by analysis of variance (ANOVA) following Duncan Multiple Range Test (MSTAT-C, 1991).

RESULTS

Inter-specific variations

P. pipistrellus had significantly (P<0.05) higher mean RBCs, WBCs, platelets, Hb, PCV levels as compared to S. heathii. However, mean values of MCV, MCH and MCHC were significantly (P0.05) different mean values of RBCs, WBCs, Hb, Platelets, PCV, MCV and MCH as compared to their female counterparts. However, MCH mean values were significantly (p<0.05) higher in female S. heathii as compared to male S. heathii (Table II).

Seasonal variations in haematological parameters

Bats belonging to both species showed distinct patterns of seasonal variation in various hematological parameters.

RBCs

S. heathii had lowest mean levels (3.94+-0.41x106/mm3) of RBCs in spring season which increased significantly (P<0.05) in summer (9.96+-0.46x106/mm3), and decreased significantly (P<0.05) in autumn (6.51+-0.40x106/mm3). Similarly, in spring, P. pipistrellus exhibited mean RBCs count of 8.87+-0.39x106/mm3, which increased significantly (P<0.05) in summer (12.28+-0.69x106/mm3), and decreased significantly (P<0.05) to 10.05+-0.40x106/mm3 in autumn (Table III). Male bats of both species had non- significantly (P<0.05) different mean RBCs indices than female counterparts in all three seasons (Table IV).

WBCs

Both bat species had lowest mean WBCs during spring. S. heathii showed 6.58+-0.62x103 cells/mm3 and P. pipistrellus had 9.09+-0.68x103 cells/mm3 in spring, which increased (P<0.05) to 15.93+-1.15 and 10.51+-0.58x103 cells/mm3 in summer and further increased (P<0.05) to 15.53+-1.43 and 19.80+-0.76x103 cells/mm3, respectively in winter (Table III). Male bats of both species had non-significantly (P0.05) different in both bat species with respect to season. In spring, S. heathii had mean platelets estimates of 6.02+-1.14, which changed non-significantly (P>0.05) in summer (5.60+-0.61) and autumn (6.56+-0.91). Similarly, P. pipistrellus had mean platelets estimates of 7.38+-1.15 in spring, which changed non-significantly (P>0.05) in summer (7.54+-1.00l) and autumn (7.64+-0.48) (Table III). The mean platelet counts were non- significantly (P>0.05) different in male and female S. heathii and P. pipistrellus when compared within species by season (Table IV).

Haemoglobin

In spring, S. heathii had Hb estimates of 15.83 g/dl, changed non-significantly (P>0.05) in summer (19.44+-0.50 g/dl) and autumn (16.50+-0.33 g/dl). Similarly, P. pipistrellus had Hb estimates of 18.17+-0.40 g/dl in spring, changed non-significantly (P>0.05) in summer (21.22+-0.52 g/dl) and autumn (19.50+-0.38 g/dl) (Table III). Furthermore, mean Hb levels were non- significantly (P>0.05) different with respect to gender and seasons (Table IV).

Haematocrit/PCV

In spring, S. heathii had lower levels of PCV (11.67+-0.84%), which increased significantly (P<0.05) in summer (18.67+-1.85%) and then went down significantly (P<0.05) in autumn (13.38+-0.62%). Same seasonal variations of PCV had observed in P. pipistrellus (Table III). The gender based seasonal variations in PCV were non-significant (p<0.05) when compared within species (Table IV).

MCV

MCV levels in S. heathii during spring were highest (3.08+-0.28 fl) which decreased significantly (P0.05) in autumn (2.07+-0.04 fl). A non-significant (P>0.05) difference was observed in MCV of P. pipistrellus during different seasons (Table III). Furthermore, mean MCV estimates were non- significantly (P>0.05) different in male and female S. heathii and P. pipistrellus when compared within species in different seasons (Table IV).

Table II.- Comparison of haematological parameters (Mean+-S.E.) of S. heathii and P. pipistrellus.

###S. heathii###P. pipistrellus

###Male (n=12)###Female (n=11)###Male (n=12)###Female (n=12)

RBCs (106/mm3)###7.62+-0.78###6.72+-0.86###11.30+-0.69###9.86+-0.43

WBCs (103/mm3)###10.85+-1.51###10.78+-1.21###15.89+-1.56###15.50+-1.23

Platelets (102/mm3)###7.02+-0.68###4.98+-0.53###7.80+-0.70###7.24+-0.74

Hb (mg/dl)###17.67+-0.63###17.27+-0.71###20.50+-0.53###19.09+-0.41

PCV (%)###16.25+-1.69###13.64+-0.85###19.58+-1.36###19.55+-0.59

MCV (fl)###2.20+-0.14###2.30+-0.24###1.76+-0.11###2.02+-0.10

MCH (pg)###2.51+-0.19###3.03+-0.38*###1.85+-0.06###1.95+-0.04

MCHC (g/dl)###1.15+-0.06###1.29+-0.05###1.10+-0.08###0.99+-0.04

Table III.- Seasonal variations of haematological parameters (Mean+-S.E.) of S. heathii and P. Pipistrellus.

###S. heathii###P. pipistrellus

###Spring###Summer###Autumn###Spring###Summer###Autumn

RBCs (106/mm3)###3.94+-0.41c###9.96+-0.46a###6.51+-0.40b###8.87+-0.39Y###12.28+-0.69X###10.05+-0.40Y

WBCs (103/mm3)###6.58+-0.62###9.09+-0.68###15.93+-1.15###10.51+-0.58###15.53+-1.43###19.80+-0.76

Platelets (102/mm3)###6.02+-1.14###5.60+-0.61###6.56+-0.91###7.38+-1.15###7.54+-1.00###7.64+-0.48

Hb (mg/dl)###15.83+-0.95###19.44+-0.50###16.50+-0.33###18.17+-0.40###21.22+-0.52###19.50+-0.38

PCV (%)###11.67+-0.84b###18.67+-1.85a###13.38+-0.62b###17.17+-0.48y###21.00+-1.18x###19.75+-1.47xy

MCV (fl)###3.08+-0.28a###1.85+-0.10b###2.07+-0.04b###1.95+-0.10###1.73+-0.10###2.00+-0.18

MCH (pg)###4.19+-0.36a###1.97+-0.04c###2.58+-0.11b###2.06+-0.05x###1.75+-0.05y###1.95+-0.04xy

MCHC (g/dl)###1.37+-0.08a###1.09+-0.06b###1.25+-0.04ab###1.06+-0.04x###1.03+-0.05y###1.05+-0.13by

Table IV.- Gender based seasonal variations of haematological parameters (Mean+-S.E.) of Scotophilus heathii and Pipistrellus pipistrellus.

###Scotophilus heathil###Pipistrellus pipistrellus

###Gender###Spring###Summer###Autumn###Apring###Summar###Autumn

RBCs (106/mm3)###Male###4.59+-0.41###10.55+-0.97###7.10+-0.45###9.15+-0.43###13.83+-1.05###10.57+-0.51

###Female###3.29+-0.52###9.49+-0.26###5.52+-0.23###8.59+-0.70###11.03+-0.43###9.18+-0.19

WBCs (103/mm3)###Male###6.57+-0.39b###7.44+-0.93b###16.14+-1.55a###9.42+-0.44dz###16.64+-3.12wx###19.17+-0.98wv

###Female###6.59+-1.32b###10.42+-0.42b###15.58+-2.06a###11.59+-0.55y###14.64+-1.02w###20.86+-1.12v

Platelets (102/mm3)###Male###6.68+-2.12###6.89+-0.49###7.34+-1.24###7.98+-1.02###7.60+-2.00###7.85+-0.67

###Female###5.35+-1.24###4.57+-0.78###5.28+-1.18###6.78+-2.29###7.50+-1.10###7.28+-0.72

Haemoglobin (mg/dl)###Male###15.67+-0.33###20.00+-1.08###17.00+-0.32###18.67+-0.33###22.50+-0.65###20.00+-0.45

###Female###16.00+-2.08###19.00+-0.32###15.67+-0.33###17.67+-0.67###20.20+-0.37###18.67+-0.33

Haematocrit (%)###Male###12.33+-0.88###21.75+-3.82###14.20+-0.73###16.33+-0.33###23.25+-2.06###18.60+-2.25

###Female###11.00+-1.53###16.20+-0.37###12.00+-0.58###18.00+-0.58###19.20+-0.80###21.67+-0.67

MCV (fl)###Male###2.75+-0.38###2.02+-0.20###2.01+-0.03###1.79+-0.05###1.71+-0.19###1.78+-0.24

###Female###3.41+-0.38###1.71+-0.02###2.17+-0.03###2.12+-0.13###1.75+-0.11###2.36+-0.10

MCH (pg)###Male###3.46+-0.25b###1.92+-0.08e###2.43+-0.13d###2.05+-0.07xy###1.65+-0.09z###1.90+-0.05xy

###Female###4.91+-0.21a###2.01+-0.03e###2.84+-0.09c###2.07+-0.09x###1.84+-0.04yz###2.03+-0.04xy

MCHC (g/dl)###Male###1.28+-0.09###0.98+-0.13###1.21+-0.05###1.14+-0.02###1.65+-0.09###1.16+-0.19

###Female###1.47+-0.11###1.17+-0.01###1.31+-0.04###0.98+-0.02###1.06+-0.06###0.86+-0.02

MCH

S. heathii and P. pipistrellus bats had high levels of MCH in spring (4.19+-0.36 and 2.06+-0.05 pg, respectively) which significantly (P<0.05) decreased (1.97+-0.04 and 1.75+-0.05, respectively) in summer. In autumn, the values of MCH increased significantly (P0.05) in P. pipistrellus (1.95+-0.04 pg) (Table III). Male and female S. heathii showed significant (P0.05) difference in the summer (Table IV).

MCHC

In spring, S. heathii had MCHC estimates of 1.37+-0.08 g/dl, which decreased significantly (P0.05) in autumn (1.25+-0.04 g/dl). P. pipistrellus had non- significant (P>0.05) differences in MCHC in different seasons (Table III). Furthermore, MCHC estimates were non-significantly (P>0.05) different in male and female S. heathii and P. pipistrellus when compared within species in different seasons (Table IV).

Correlation of haematological parameters within gender and species

The haematological parameters of male bats of both species did not show any correlation in spring. However, a significant (p<0.05) positive correlation (r=0.98) between PCV and Hb, while a significant (p<0.05) negative correlation (r=-0.89) between MCHC and Hb were observed in the female S. heathii. Furthermore, in the female S. heathii, PCV was correlated (r=-0.98) with MCHC in spring. However, in female P. pipistrellus only PCV is significantly (p<0.05) correlated (r=-0.97) with MCH.

In summer, RBCs counts were significantly (p<0.05) correlated with Hb (r=0.98), PCV (r=0.86), MCV (r=-0.99) and MCH (r=-0.92) in male S. heathii. Similarly, male P. pipistrellus had RBCs counts correlated with MCV (r=-0.983), MCH (r=-0.955) and MCHC (r=0.988). In male S. heathii, Hb levels were positively correlated with PCV (r=0.97) and negatively correlated with MCV (r=-0.92) and MCH (r=-0.99). Furthermore, PCV was correlated with MCV (r=-0.95) and MCH (r=-0.98) in male S. heathii. Similarly, in male P. pipistrellus, the PCV was correlated with MCV (r=0.98), MCH (r=0.97), and MCHC (r=-0.96) in summer. In female P. pipistrellus, RBCs are correlated with Hb (r=0.987) and MCH (r=-0.98) and Hb is correlated (r=-0.94) with MCH in summer.

In autumn, the male S. heathii had RBCs counts positively correlated with Hb (r=0.99), PCV (r=0.98), MCV (r=0.94) and negatively correlated with MCH (r=- 0.98) and MCHC (r=-0.98). Furthermore, Hb was positively correlated with PCV (r=0.98) and MCV (r=0.94) and negatively correlated with MCH (r=-0.98) and MCHC (r=-0.96) in male S. heathii. In male S. heathii, the PCV was also positively correlated with MCV (r=0.98) and negatively correlated with MCH (r=- 0.95) and MCHC (r=-0.97) in autumn. Similarly, in male P. pipistrellus RBCs counts were correlated with Hb (r=0. 92) and MCH (r=-0.96), and PCV was correlated (r=-0.97) with MCHC. In female P. pipistrellus only PCV and MCH were correlated (r=0.99) in autumn.

DISCUSSION

Seasonal hematological studies are required to reveal the physiological seasonal adaptations which also help in differential diagnosis of normal and pathological conditions (Gulland and Hawkey, 1990; Campbell, 1992; Dawson and Bortolotti, 1997; Heard and Whittier, 1997). The blood composition may vary with various internal and external factors i.e. age, gender, reproductive state, season, diurnal rhythm, pollution, food quality and availability (Westhuyzen, 1978; Hellgren et al., 1988; Wolkers et al., 1994; Minemastue et al., 1995). In addition to the seasonal changes, the blood profile changes due to capturing, handling and sampling stresses (Widmaier and Kunz, 1993; Koopman et al., 1995).

The oxygen carrying capacity of blood is dependent on the counts of erythrocytes increase during summer season to support the heightened activity of the bats (Arevalo et al., 1987; Korine et al., 1999). During the period of the lesser activity, bats do not feed or feed less which may result in a decrease of metabolic rates and RBCs. It has been observed that the concentrations of the blood components change when an animal gets exposed to low temperature (cold conditions) and low quality of food (Nieminen, 1979; Hellgren et al., 1988; Alfaro et al., 1994; DelGiudice et al., 1994; Wolkers et al., 1994).

WBCs levels were found lower during spring and summer seasons as compare to autumn because bats are involved actively in reproduction, and the resources required may be used more for reproductive success than survival through immunity (Roff, 1992; Stearns, 1992; Sheldon and Verhulst, 1996; Lochmiller and Deerenberg, 2000; Norris and Evans, 2000; Schmid-Hempel and Ebert, 2003; Harshman and Zera, 2006). Furthermore, reproductive success of animals depends on the survival of gametes, while, the autoimmunity is one of a major threats to gametes. In order to ensure gametes survival, immunity of bats may be down regulated during the reproductive season (Folstad and Skarstein, 1997; Kortet et al., 2004; Skau and Folstad, 2004). The higher WBCs counts may indicate presence of stress or infection (Pehlivanoglu et al., 2001).

Although, the present study reported almost similar levels of platelets in different seasons, but previous studies in human reported that in addition to genetic factors, gender, age and seasonal factors may regulate platelet counts. In contrast to our results, higher counts were observed in human females than in males (Biino et al., 2011). Seasonal variations in human platelet counts were observed with a peak during autumn and winter (Buckley et al., 2000).

Bats have high haematocrit and haemoglobin levels than terrestrial mammals (Lewis, 1977; Jurgens et al., 1981; Wightman et al., 1987; Arevalo et al., 1987, 1992; Viljoen et al., 1997). In contrast to our results, previous studies reported that at the end of the resting phase (winter season) the haemoglobin and haematocrit levels of bats were higher as compared to the end of the activity phase (summer season) during which the values of both these parameters were low (Korine and Arad, 1993). However, high blood-oxygen requirement during activity is responsible for high haemoglobin concentrations and haematocrit values in small mammals with high metabolic rates (Arevalo et al., 1992).

The increase in MCV suggests an increase in the number of immature erythrocytes (Lurie, 1993; Kim et al., 2002). Haematocrit amount and MCV increased during the summer months and decreased during winter and spring months that is related to variations in activity of bats in these seasons (Arevalo et al., 1992; Korine et al., 1999). The higher MCH and MCHC values in spring may be a sign of an increase in erythropoietic activity of the bats related to increase in temperature and photoperiod leading to increase in erythrocyte count, haemoglobin and hematocrit (Rewkiewiccz, 1975). Furthermore, a positive correlation between PCV and Hb showed a constant Hb concentration in the RBCs. The positive correlation of RBCs with Hb and PCV, and negative correlation with MCV and MCH indicates the reduced size of RBCs with increasing number of cells. The positive correlation between RBCs, Hb and PCV showed that increasing cell numbers also increase Hb and PCV (Hardig and Hoglund, 1983).

The bats (Scotophilus healthii and Pipistrellus pipistrellus) showed interspecific and gender based intraspecific haematological variations. The seasonal fluctuations in haematological parameters were also observed in the bats studied. P. pipistrellus had higher counts of RBCs, WBCs, platelets, Hb and PCV as compared to S. heathii. The higher levels of RBCs, Hb and PCV of the bat species were associated with a higher activity season, i.e., summer and higher levels of WBCs were associated with less activity season, i.e. autumn.

ACKNOWLEDGMENTS

This work was supported by Pir Mehr Ali Shah, Arid Agriculture University Rawalpindi under Grant No. PMAS-AAUR/DR 454.

Statement of conflict of interest

Authors have declared no conflict of interest.

REFERENCES

Alfaro, V., Peinado, V.I. and Palacios, L., 1994. Changes in plasma glucose, lactate, triglycerides and some non- protein nitrogen components induced by short-term hypothermia in the conscious rat. Comp. Biochem. Physiol. A., 107: 149-155.

Arevalo, F., Parez, S.G. and Lopez, L.P., 1992. Seasonal changes in blood parameters in the bat species Rhinolophus ferrumequinum and Miniopterus schreibersi. Arch. Physiol. Biochem., 100: 385-387.

Arevalo, F., Parez, S.G. and Lopez, L.P., 1987. Haematological data and haemoglobin components in bats (Vespertilionidae). Comp. Biochem. Physiol. A., 88: 447-450.

Bates P.J. and Harrison, D.L., 1997. Bats of the Indian subcontinent. Harrison Zoological Museum Publication, UK.

Biino, G., Balduini, C., Casula, L., Cavallo, P., Vaccargiu, S. and Parracciani, D., 2011. Analysis of 12,517 inhabitants of a Sardinian geographic isolate reveals that predispositions to thrombocytopenia and thrombocytosis are inherited traits. Haematologica, 96: 96-101.

Buckley, M.F., James, J.W., Brown, D.E., Whyte, G.S., Dean, M.G., Chesteman, C.N. and Donald, J.A., 2000. A novel approach to the assessment of variations in the human platelet count. Thromb. Haemost., 83: 480-4.

Campbell, T.W., 1992. Avian hematology and cytology. Iowa State University Press, U.S.A.

Dawson, R.D. and Bortolotti, G.R., 1997. Variation in hematochrit and total plasma proteins of nestling American Kestrels (Falco sparverius) in the wild. Comp. Biochem. Physiol. A., 117: 383-390.

Delgiudice, G.D., Mech, L.D. and Seal, U.S., 1994. Undernutrition and serum and urinary urea nitrogen of white-tailed deer during winter. J. Wildl. Manage., 58: 430-436.

Eates, K.R., 1968. An introduction to the vertebrate fauna of Sind and Khairpur State. Mammalia. West Pakistan Gazetter, Sind Region, Government of West Pakistan, pp. 33-52.

Folstad, I. and Skarstein, F., 1997. Is male germ line control creating avenues for female choice? Behav. Ecol., 8: 109-112.

Gulland, F.M.D. and Hawkey, C., 1990. Avian hematology. Vet. Annul., 30: 126-136.

Hardig, J. and Hoglund. L., 1983. On accuracy in estimating fish blood variables. Comp. Biochem. Physiol., 75: 35-40.

Harshman, L.G. and Zera, A.J., 2006. The cost of reproduction: the devil in the details. Trends Ecol. Evol., 22: 80-86.

Heard, D.J. and Whittier, D.A., 1997. Hematological and plasma biochemical reference values for three flying fox species (Pteropus sp.). J. Zoo. Wildl. Med., 28: 464-470.

Hellgren, E.C., Vaughan, M.R. and Krikpatrick, R.L., 1988. Seasonal patterns in physiology and nutrition of black bears in Great Dismal Swamp, Virginia and North Carolina. Can. J. Zool., 67: 1837-1850.

Jurgens, K.D., Bartels, H. and Bartels, R., 1981. Blood oxygen transport and organ weights of small bat and non flying- mammals. Resp. Physiol., 45: 243-260.

Kim, J.C., Yun, H.I., Cha, S.W., Kim, K.H. and Koh, W.S., 2002. Haematological changes during normal pregnancy in New Zealand white rabbits. Comp. Clin. Pathol., 11: 98-106.

Koopman, H.N., Westgate, A.J., Read, A.J. and Gaskin, D.E., 1995. Blood chemistry of wild Harbor porpoises, Phocoena phocoena (L.). Mar. Mammal Sci., 11: 123-135.

Korine, C. and Arad, Z., 1993. Effect of water restriction on temperature regulation of the fruit bat Rousettus aegyptiacus. J. Therm. Biol., 18: 61-69.

Korine, C., Zinder, O. and Arad, Z., 1999. Diurnal and seasonal changes in blood composition of the free-living Egyptian fruit bat (Rousettus aegyptiacus). Comp. Biochem. Physiol. B., 169: 280-286.

Kortet, R., Vainikka, A., Rantala, M.J. and Taskinen, J., 2004. Sperm quality, secondary sexual characters and parasitism in roach (Rutilus rutilus L.). Biol. J. Linn. Soc., 81: 111-117.

Lewis, J.N., 1977. Comparative haematology: studies on Chiroptera (Pteropus giganteus). Comp. Biochem. Physiol. B., 58: 103-107.

Lochmiller, R.L. and Deerenberg, C., 2000. Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos, 88: 87-98.

Lurie, S., 1993. Changes in age distribution of erythrocytes during pregnancy: a longitudinal study. Gynecol. Obstet. Invest., 36: 141-144

Mahmood-ul-Hassan and Nameer, P.O., 2006. Diversity, role and threats to the survival of bats in Pakistan. J. Anim. Pl. Sci., 16: 38-42.

Minemastue, S., Watanabe, M., Tsuchiya, N., Watanabe, M. and Amagaya, S., 1995. Diurnal variations in blood chemical items in Sprague-Dawley rats. Exp. Anim. Tokyo, 44: 223-232.

Mirza, Z.B., 1967. Notes on the ecology and distribution of fruit bats Rousettus leschenaultii leschenaultii in West Pakistan. Pakistan J. Sci., 19: 193-4.

Mstat C., 1991. Manual. Microstatistical programme. Michigan State University, USA.

Murray, J.A., 1884. The vertebrate zoology of Sindh. Richardson and Co., Pall Mall, London, pp. 476.

Nadeem, M.S., Zafar, S., Kayani, A. R., Mushtaq, M., Beg, M.A. and Nasir, M.F. 2013. Distribution and roosting habitats of some microchiropteran bats in Rawalpindi District, Pakistan. Pakistan J. Zool., 45: 565-569

Nieminen, N., 1979. Nutritional and seasonal effects on the haematology and blood chemistry in reindeer (Rangifer tarandus tarandus L.). Comp. Biochem. Physiol. B., 66: 399-413.

Norris, K. and Evans, M.R., 2000. Ecological immunology: life history trade-offs and immune defence in birds. Behav. Ecol., 11: 19-26.

Pehlivanoglu, B., Balkanci, Z.D., Ridvanagaoglu, A.Y., Durmazlarn, Ozturk, G., Erbas, D. and Okur, H., 2001. Impact of stress, gender and menstrual cycle on immune system: possible role of nitric oxide. Arch. Physiol. Biochem., 109: 383-387.

Rewkiewiccz, A.D., 1975. Seasonal changes in hemoglobin and erythrocyte indices in Microtus arvalis. B. Pol. Acad. Sci- Biol., 23: 481-486.

Roberts, T.J., 1997. Mammals of Pakistan. 2nd Ed. Oxford University Press, Oxford.

Roff, D.A., 1992. The evolution of life histories: theory and analysis. Chapman and Hall, New York.

Schmid-Hempel, P. and Ebert, D., 2003. On the evolutionary ecology of specific immune defence. Trends Ecol. Evol., 18: 27-32.

Sheldon, B.C. and Verhulst, S., 1996. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol., 11: 317-322.

Skau, P.A. and Folstad, I., 2004. Does immunity regulate ejaculate quality and fertility in humans? Behav. Ecol., 16: 410-416.

Stearns, S.C., 1992. The evolution of life histories. Oxford University Press, Oxford.

Viljoen, M., Merwe, M.V., Bower, G., Levay, P.E. and Grobler, A.S., 1997. Peripheral blood characteristics of gravid Schreiber's long-fingered bats, Miniopterus schreibersii natalensis. S. Afr. J. Sci., 93: 414-418.

Walker, S. and Molur, S., 2003. Summary of the status of the South Asian Chiroptera. Extracted from C. A.M. P. 2002 Report. Zoo Outreach Organization. CBSG South Asia and Wild. Coimbator, India, pp. 23-45.

Westhuyzen, J., 1978. The diurnal cycle of some energy substrates in the fruit bat (Rousettus aegyptiacus). S. Afr. J. Sci., 74: 99-101.

Widmaier, E.P. and Kunz, T.H., 1993. Basal, diurnal and stress- induced levels of glucose and glucocorticoids in captive bats. J. exp. Zool., 265: 533-540.

Wightman, J., Roberts, J., Chaffey, G. and Agar, N.S., 1987. Erythrocyte biochemistry of grey-headed fruit bat (Pteropus poliocephalus). Comp. Biochem. Physiol. B., 88: 305-307.

Wintrobe, M.M., 1933. Variations in size and haemoglobin concentration of erythrocytes in the blood of various vertebrates. Folia Haematol., 51: 32-49.

Wolkers, H., Wensing, T. and Schonewille, J.T., 1994. Effect of under nutrition on hematological and serum biochemical characteristics in red deer (Cervus elelphus). Can. J. Zool., 72: 1291-129.
COPYRIGHT 2016 Asianet-Pakistan
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2016 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Rashid, Nosheen; Irfan, Muhammad; Nadeem, Muhammad Sajid; Shabbir, Asghar
Publication:Pakistan Journal of Zoology
Article Type:Report
Geographic Code:9PAKI
Date:Oct 31, 2016
Words:5241
Previous Article:Isolation, Identification and Cadmium Processing of Pseudomonas aeruginosa (EP-Cd1) Isolated from Soil Contaminated with Electroplating Industrial...
Next Article:Role of Physio-Morphic Characters of Different Genotypes of Eggplant, Solanum melongena L. and its Association with the Fluctuation of Jassid,...
Topics:

Terms of use | Privacy policy | Copyright © 2019 Farlex, Inc. | Feedback | For webmasters