Content uploaded by Ahmad Waheed
Author content
All content in this area was uploaded by Ahmad Waheed on Jul 03, 2022
Content may be subject to copyright.
hp://bdvets.org/javar/ 290
Tahir et al. / J. Adv. Vet. Anim. Res., 9(2): 290–294, June 2022
JOURNALOFADVANCEDVETERINARYANDANIMALRESEARCH
ISSN2311-7710(Electronic)
hp://doi.org/10.5455/javar.2022.i595June 2022
A periodical of the Network for the Veterinarians of Bangladesh (BDvetNET) VOL9,NO.2,PAGES290–294
ORIGINALARTICLE
Morphometric parameters and food preference in relaon to sex and reference
hematological values for Upupa epops from Pakistan
RidaTahir1,WardaZafar1,MuhammadWaseemAslam1,AhmadWaheed1,AliUmar1,SanaFama2,
TariqJaved1,TabishLiaqat3,AllahDia1,MuhammadAshfaq1,MuhammadZaman1,AliNawaz1,
TehminaKhan1,MuhammadWajid1,MuhammadSaleemKhan1
1DepartmentofZoology,FacultyofLifeSciences,UniversityofOkara,Okara,Pakistan
2DepartmentofZoology,WildlifeandFisheries,UniversityofAgriculture,Faisalabad,Pakistan
3DepartmentofFisheriesandAquaculure,FacultyofLifeSciences,UniversityofOkara,Okara,Pakistan
Correspondence MuhammadSaleemKhan samiikhan@uo.edu.pk DepartmentofZoology,FacultyofLifeSciences,Universityof
Okara,OkaraPakistan.
How to cite:TahirR,ZafarW,AslamMW,WaheedA,UmarA,FamaS,etal.Morphometricparametersandfoodpreferenceinrelaon
tosexandreferencehematologicalvaluesforUpupa epopsfromPakistan.JAdvVetAnimRes2022;9(2):290–294.
ABSTRACT
Objecve:Thestudywasconductedtoinvesgatethegutcontentandrecordmorphometricand
hematologicalparametersinthecommonhoopoe(Upupa epops).
Materials and Methods:Twentysamplesofhealthybirds(10fromeachsex)werecollectedfrom
dierentlocaonsinOkaraDistrict,Punjab,Pakistan,fromSeptember2020toMarch2021.Birds
werecapturedliveforbloodsamplesandmorphometricandgutanalyses.
Results:It wasrevealedthattheconcentraonsofdierenthematologicalparameterswereas
follows:hemoglobin,20.03g /dl;redblood cells,3.28 ×106/µl;whitebloodcells, 326.67×103/
µl;hematocrit, 56.47%;MCV,173.33 FL;MCH,57.4 pg;MCHC, 57.4pg; PLT,8.33/µl;andRDW,
8.33/µl.Thepercentagesofneutrophils,lymphocytes,monocytes,andeosinophilswere84.67%,
11.67%,2.00%,and1.67%,respecvely.Thegutcontentofthecommonhoopoemostlyconsisted
of Coleopteraand Acrididae lar vae.However,Lepidoptera, Gryllotalpidae, and sand were also
recorded,alongwithseedsofSalvadora persica.
Conclusions:TherewerenosignicantdierencesbetweenmaleandfemaleU. epopsinfeeding
content,totalweightofthegut,orweightoftheemptygut.Regardingthemorphometricparam-
eters,therewasa signicantdierenceinboth sexes’wingspan,bodylength,andbodyweight.
Malesweresignicantlyheavierthanfemales.
ARTICLE HISTORY
ReceivedMarch25,2021
RevisedMarch30,2022
AcceptedApril02,2022
PublishedJune27,2022
KEYWORDS
Commonhoopoe;gutcontents;
hematology;morphometry;Pakistan
Introducon
The common hoopoe (Upupa epops) is known by its Arabic
name, “Hudhud,” in Pakistan. It is a remarkable and unique
old-world bird that belongs to the family Upupidae. It has
its foraging style with special external features [1]. The
distribution ranges from Europe and North and sub-Sa-
haran Africa (including Madagascar) to Asia. They mainly
breed in Europe, Africa, Malaysia, the Middle East, China,
and Indonesia [2]. Most of the African and Southeast Asian
populations of common hoopoe remain in their native
areas in the winter and do not migrate [3].
They also migrate to the tropical region from North
Asia and Europe during the winter seasons [4]. This bird
the Karakoram and Sulaiman ranges and the Hindu Kush
beside the Indus River [5]. It is also a summer-breed vis-
itor in the northern Himalayas and Indus plains [2]. The
best living places are wooded steppes, savannas, grass-
lands, and forest glades. Deserts and natural forests are
avoided [2,6].
Upupa epops is a small to medium-sized, slender-shaped
bird with a 29–31 cm body length and a 64–77 gm weight
in males and 57–69 gm in females [7]. The head is mainly
rufous orange to orange-brown or salmon pink in color,
with sticking black and white wings of an average length
of 13.6–15.3 cm [8]
alternative white and black bars. Upupa epops has a long,
©Theauthors.ThisisanOpenAccess
arcledistributedunderthetermsof
theCreaveCommonsAribuon4.0
License(hp://creavecommons.org/
licenses/by/4.0)
hp://bdvets.org/javar/ 291
Tahir et al. / J. Adv. Vet. Anim. Res., 9(2): 290–294, June 2022
thin, downcurved black bill of 5–6.3 cm and a squared
tipped, black and white striped tail of 9.8-10.9 cm [7]. Like
the erectile crest crown, the high black tip fan consists of
28 feathers (long, narrow, and orange) on the common
hoopoe’s head [9]-
wards in the narrow tail in the rest position, and in excited
or alarmed conditions, the crest is erect and fan-shaped
[2,7].
Avian hematology started early in the 1960s. In veter-
inary practice, hematology is vital, and changes in avian
blood’s morphology and composition help detect and
diagnose health issues [10]. The blood parameters change
in response to health status and migration. For example,
migratory period [11]. In many species, hemoglobin con-
adulthood [12]. Some species, along with heterophils,
respond to stress with lymphocytosis (increased lympho-
cytes). In the case of any chronic disease, the number of
monocytes increases, while in allergic or parasitic condi-
tions, the number of eosinophils increases [13]. Therefore,
building standard reference values is necessary for each
avian species.
The common hoopoe is mostly insectivorous; it
feeds on small worms (annelids), larvae of ant-lions
(Myrmeleonidae), Elaleid beetles Agrotis larvae, Hemiptera
bugs, etc. In some studies, small reptiles, frogs, and plant
matter were also recorded in the food [2,6]. Hoopoes
that inhabit farmland mainly feed on mole crickets
(Gryllotalpidae) and Lepidoptera larvae [14], whereas
hoopoes in pine plantations mainly feed on pupae of the
pine moth (Thaumetopoea pityocampa) [6,15]. During the
winter–autumn season, they feed on ants (Componotus
compressces). The primarily young feed on soil inverte-
brates [2,16]. The study was conducted to investigate the
gut content and record morphometric and hematological
parameters in common hoopoe (U. epops).
Materials and Methods
Ethical approval
All procedures carried out on the animals in this study
followed the rules set by the University of Okara’s Ethical
Committee (approval number: UO/DOZ/2020/misc.).
Study area and sampling
Samples of the common hoopoe were collected from the
grassy wooded steppes area of Renala Khurd (30.88°N,
73.60°E), Pipli Pahar (30.68°N, 73.43°E), and alongside
the Ravi river in Okara District. These places were vis-
ited in the morning and evening from December 2020 to
March 2021, twice a day for sampling. Twenty samples of
the common hoopoe (10 from each gender) were captured
with the help of local hunters using a net. After capture, we
anesthetized the birds by using a combination of ketamine
HCL (10 mg/kg) and diazepam (0.2 mg/kg) [17].
Blood sample analysis, gut content, and morphometry
Analyses of hematological and morphometric characteris-
tics and gut content of the common hoopoe were carried
out according to the methodology described by Aslam et
al. [18].
Stascal analysis
Data were analyzed through mean, standard deviation
(SD), standard error (SE), and range using GraphPad Prism
an unpaired t
Results and Discussion
Hematology
The hematological values are used to indicate the health
state of birds, as well as mammals. These are used for
diagnosing and monitoring diseases, evaluation of disease
therapy, or disease prognosis. These can also be used as
different bird species. Different physiological factors can
affect the hematology of healthy birds [19,20]. The pres-
ent study provides physiological reference values for nor-
mal values of the adult birds of this species (Table 1). No
Table 1. Hematologicalparametersofthecommonhoopoecollect-
edfromOkaraDistrict,Punjab,Pakistan.
VariableSE Mean ± SD
HGB(gm/dl) 2.16 20.03±3.73
WBC(×103/µl) 2.88 326.33±3.33
RBC(×106/µl) 0.22 3.28±0.37
HCT(%) 0.41 56.47±0.70
MCV(FL) 0.72 173.33±1.25
MCH(pg) 0.71 58.97±1.23
MCHC(gm/dl) 1.66 34.33±2.87
PLT(×103/µl) 1.19 8.33±2.05
RDW 1.28 75.00±2.21
Neutrophils 2.60 84.67±4.50
Lymphocytes 3.31 11.67±5.73
Monocytes 0.47 2.00±0.82
Eosinophils 0.27 1.67±0.47
SE=Standarderror;SD=Standarddeviaon.
hp://bdvets.org/javar/ 292
Tahir et al. / J. Adv. Vet. Anim. Res., 9(2): 290–294, June 2022
Figure 1. Comparison of body length, wingspan, and weight of both sexes of U. epops (*p < 0 .05;
**p < 0.01)
Table 2. ComparisonofmorphometriccharacteriscsbetweenmaleandfemaleUpupa epopscollectedfromOkaraDistrict,Punjab,
Pakistan.
Characters Sex(n = 10 each) SE Mean Range p-value
Bodyweight(gm) Male 2.07 64.03 57.70–68.00 0.01*
Female 1.04 54.35 52.60–57.70
Bodylength(cm) Male 0.12 27.88 27.50–28.10 0.01*
Female 0.21 26.23 26.40–27.50
Taillength(cm) Male 0.14 11.18 10.80–11.50 0.175NS
Female 0.11 10.85 10.50–11.10
Wingspan(cm) Male 0.06 43.70 43.60–43.90 <0.01**
Female 0.03 43.05 43.00–43.10
Winglength(cm) Male 0.13 18.85 18.40–19.10 0.142NS
Female 0.08 18.55 18.40–18.70
Longestprimaryfeather(cm) Male 0.12 13.53 13.20–13.90 0.518NS
Female 0.02 13.43 13.40–13.50
Tarsus(cm) Male 0.12 2.40 2.00–2.60 0.115NS
Female 0.05 2.13 2.00–2.30
Centraltoelength(cm) Male 0.03 2.15 2.10–2.20 0.228NS
Female 0.04 2.08 2.00–2.20
Headlengthwithoutbill(cm) Male 0.08 3.25 3.10–3.50 0.085NS
Female 0.14 2.88 2.60–3.20
Headlengthwithbill(cm) Male 0.01 8.75 8.60–8.90 0.055NS
Female 0.13 8.35 8.10–8.60
Billlength(cm) Male 0.04 5.50 5.40–5.60 0.620NS
Female 0.02 5.48 5.40–5.50
Chestcircumference(cm) Male 0.17 13.78 13.40–14.20 0.007NS
Female 0.09 12.90 12.60–13.10
*p<0.05;**p<0.01;NS=Nonsignicantdierence(p-value>0.05).
hp://bdvets.org/javar/ 293
Tahir et al. / J. Adv. Vet. Anim. Res., 9(2): 290–294, June 2022
previous comparable records are present for the species in
the present analysis.
Morphometry
weight, and body length (Fig. 1), while all other morpho-
Table 2).
Morphological analysis helps understand the evolution-
ary processes [21,22]. The present study was similar to
David [23] and Roberts [2] in the morphometric measure-
ment of body weight, body length, wingspan, and length
of the longest primary feather of male and female com-
mon hoopoes. In the case of bill length, similar values to
our study were also reported by van Wijk et al. [7], Elshaer
[24], and Roberts [2]. At the same time, all other remaining
in the present study.
Food preferences
of the gut, weight of the food content, and weight of the
empty gut for both sexes (Table 3). The gut analysis shows
that the common hoopoe feeds mainly on Coleoptera and
Acrididae larvae. However, Lepidoptera, Gryllotalpidae,
and sand were also found. The seed of Salvadora persica
was found in the gut. The difference in feeding content
Table 4).
The study of feed preference is important from ecologi-
cal and conservation perspectives [25]. The gut content of
U. epops consisted of larvae of Lepidoptera, Gryllotalpidae
and Acrididae, Coleoptera, and sand, which were also
reported by Kristin [6] and Roberts [2]. We also found
some plant matter, i.e., seeds of S. persica, in the gut of U.
epops, which Fournier and Arlettaz [14] also reported.
However, our outcomes differed from Roberts [2] in the
these in the gut content of U. epops. Namma and Rao [26],
Myo et al. [27], and Tomás et al. [28] reported that U. epops
preferred to eat insects. This difference might be due to the
difference in habitat or food availability.
Conclusion
The morphometries of both sexes of the common hoopoe
(except for body weight, body length, and wingspan), gut
weight, and gut content were similar. Males were larger and
heavier as compared to females. The gut analysis shows
that the common hoopoe feeds on Coleoptera, Acrididae
larva, Lepidoptera, Gryllotalpidae, sand, and seeds of dif-
ferent plants, such as S. persica. This study discusses all
Table 3. Weightofgutvariablesinmaleandfemalecommonhoopoes.
CharactersGender NMean SD SE t-value p-value
Totalweightofgut(gm) Male 10 2.30 0.62 0.36 0.01 0.9512NS
Female 10 2.33 0.37 0.22
Weightoffoodmaterial(gm) Male 10 1.06 0.49 0.28 0.02 0.9052NS
Female 10 1.01 0.33 0.11
Weightofemptygut(gm) Male 10 1.24 0.13 0.07 0.74 0.4163NS
Female 10 1.32 0.04 0.33
NS=Nonsignicantdierence(p-value>0.05).
Table 4. Gutcontentofmaleandfemalecommonhoopoes.
Type of FoodWeight of dierent gut contents (%)
p-value
Male Female
Lepidoptera 0.00 10.33 0.3090NS
Gryllotalpidae 0.00 4.00 0.3739NS
S. persica 15.33 18.33 >0.9999NS
Acrididae 0.00 2.67 0.3739NS
Coleoptera 61.67 24.00 0.0866NS
Sand 0.00 5.33 0.3739NS
Digestedmaterial 23.00 35.33 0.4012NS
NS=Nonsignicantdierence(p-value>0.05).
hp://bdvets.org/javar/ 294
Tahir et al. / J. Adv. Vet. Anim. Res., 9(2): 290–294, June 2022
List of abbreviaons
HGB, Hemoglobin; WBC, White blood cells; RBC, Red blood
cells; HCT, Hematocrit; MCV, Mean corpuscular volume;
MCH, Mean corpuscular hemoglobin; MCHC, Mean corpus-
cular hematocrit; PLT, Platelets; RDW, Red cell distribution
width.
Acknowledgment
Not applicable.
Conict of interest
Authors’ contribuons
RT, MW, and WZ designed the study. AD, TK, and MA inter-
preted the data. AW and AU drafted the manuscript. MWA,
MZ, AN, TJ, TL, and SF were involved in the collection of data
and also contributed in manuscript preparation. MSK took
part in preparing and critically checking this manuscript.
References
[1] Mahmoud FA, Gadel-Rab AG, Shawki NA. Functional morphologi-
cal study of the choana in different bird species. J Basic Appl Zool
2018; 79(1):11; https://doi.org/10.1186/s41936-018-0026-6
[2] Roberts TJ. Birds of Pakistan, vol. 2, Oxford University Press,
Oxford, UK, 1992.
[3] Hewitt GM. Some genetic consequences of ice ages, and their role
in divergence and speciation. Biol J Linnean Soc 1996; 58 (3):247–
76; https://doi.org/10.1111/j.1095-8312.1996.tb01434.x
[4] Reichlin TS, Schaub M, Menz MHM, Mermod M, Portner P, Arlettaz
R, Jenni L. Migration patterns of Hoopoe Upupa epops and Wryneck
Jynx torquilla: an analysis of European ring recoveries. J Ornithol
2008; 150 (2):393; https://doi.org/10.1007/s10336-008-0361-3
[5] Altaf M, Javid A, Munir MA, Ashraf S, Iqbal KJ, et al. Diversity, dis-
Punjab, Pakistan. Biologia 2013; 59(1):131–7.
[6] Kristin A.Family Upupidae (Hoopoe), Handbook of the birds of the-
world. vol.6,Lynx Edicions,Barcelona,Spain, 2001.
[7] van Wijk RE, Schaub M, Hahn S, Juarez-Garcia-Pelayo N, Schafer B,
Viktora L, et al. S Bauer. Diverse migration strategies in hoopoes
(Upupa epops) lead to weak spatial but strong temporal connec-
tivity. Naturwissenschaften 2018; 105(7–8):42; https://doi.
org/10.1007/s00114-018-1566-9
Bali: the Greater Sunda Islands. Oxford University Press, Oxfor, UK,
1993.
[9] Nicoll MJ, Handlist of the birds of Egypt. Government Press, Egypt,
1919; https://doi.org/10.5962/bhl.title.14405
[10] Mitchell EB, Johns J. Avian hematology and related disorders. Vet
Clin North Am Exot Anim Pract 2008; 11(3):501–22; https://doi.
org/10.1016/j.cvex.2008.03.004
[11] Piersma T, Everaarts JM, Jukema J. Build-up of red blood cells in refu-
elling bar-tailed godwits in relation to individual migratory quality.
Condor 1996; 98 (2):363–70. https://doi.org/10.2307/1369154
[12] Samour J, Naldo J, Libanan N, Rahman H, Sakkir M. Age-related
hematology and plasma chemistry changes in captive Masai
ostriches (Struthio camelus massaicus). Comp Clin Path 2010;
20(6):659–67; https://doi.org/10.1007/s00580-010-1054-x
[13] DeNicola DB. Advances in hematology analyzers. Top Companion
Anim Med 2011; 26(2):52–61; https://doi.org/10.1053/j.
tcam.2011.02.001
[14] Fournier J, Arlettaz R. Food provision to nestlings in the Hoopoe
Upupa epops: implications for the conservation of a small endan-
gered population in the Swiss Alps. Ibis 2001; 143(1):2–10;
https://doi.org/10.1111/j.1474-919X.2001.tb04163.x
[15] Barbaro L, Couzi L, Bretagnolle VN, Vetillard F. Multi-scale hab-
itat selection and foraging ecology of the eurasian hoopoe
(Upupa epops) in pine plantations. In Brockerhoff EG, Jactel H,
Parrotta JA, Quine CP, Sayer J, Hawksworth DL (eds.), Plantation
forests and biodiversity: oxymoron or opportunity? Springer,
Dordrecht, The Netherlands, pp 149–163, 2007; https://doi.
org/10.1007/978-90-481-2807-5_8
[16] Martín-Vivaldi M, Palomino JJ, Soler M, Soler JJ. Determinants of
reproductive success in the Hoopoe Upupa epops, a hole-nesting
non-passerine bird with asynchronous hatching. Bird Study 1999;
46(2):205–16; https://doi.org/10.1080/00063659909461132
[17] Abbas SW, Ali MN, Abbas G, Safwan HM, Sajid M, Mehmood M.
Comparative effectiveness of general anesthesia in doves using
a combination of ketamine and diazepam. Adv Zool Bot 2018;
6(4):95–100; https://doi.org/10.13189/azb.2018.060401
[18] Aslam, MW, M Wajid, A Waheed, S Ahmad, K Jafar, H Akmal, et al.
Revision of some mensural measurements, food preference, and
haematological parameters in breeding pairs of blue rock pigeon,
Columba livia sampled from punjab Pakistan. Braz J Biol 2021; 83;
https://doi.org/10.1590/1519-6984.252059
E, et al. Haematological indicators in hybrid mallard ducks (Anas
platyrhynchos) with regard to the use of meal from whole white
lupin seeds in their diet. Acta Vet Brno 2017; 86 (3):309–15;
https://doi.org/10.2754/avb201786030309
[20] Kral I, Suchý P. Haematological studies in adolescent breed-
ing cocks. Acta Vet Brno 2000; 69(3):189–94; https://doi.
org/10.2754/avb200069030189
[21] Anthwal N, Tucker AS. Q&A: Morphological insights into evo-
lution. BMC Biol 2017; 15(1):83; https://doi.org/10.1186/
s12915-017-0425-z
[22] Aaron E, Hawthorne-Madell J, Livingston K, Long JH. Morphological
evolution: Bioinspired methods for analyzing bioinspired robots.
Front Robot AI 2021; 8:717214; https://doi.org/10.3389/
frobt.2021.717214
[23] David A. Hoopoes and Acacias: decoding an Ancient Egyptian
Funerary Scene. J Near East Stud 2014; 73(2):235–52; https://doi.
org/10.1086/677251
[24] Elshaer F. Comparative morphometric studies of the cranium in the
three types of birds with different feeding behaviors. Egypt Acad
J Biol Sci B. Zool 2019; 11(1):47–57; https://doi.org/10.21608/
eajbsz.2019.29471
[25] Tryjanowski P, Møller AP, Morelli F, Indykiewicz P, Zduniak P,
a large-scale experiment. Avian Res 2018; 9(1):1–6; https://doi.
org/10.1186/s40657-018-0111-z
pests of castor Ricinus communis l. Indian J Entomol 2020; 82(1):29–
31; http://dx.doi.org/10.5958/0974-8172.2020.00006.1
[27] Myo Y, Zin T, Htay SS. Different types of foods foraged by various
bird species in Pakokku environs, magway region. Myanmar Acad
Arts Sci 2020; 18(3):187–97.
[28] Tomás G, Zamora-Muñoz C, Martín-Vivaldi M, Barón MD, Ruiz-
Castellano C, Soler JJ. Effects of chemical and auditory cues of
hoopoes (Upupa epops) in repellence and attraction of blood-feed-
fevo.2020.579667