(DIGENEA: DIPLOSTOMIDAE) IN Phalacrocorax

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to Tylodelphys adulta Lunaschi and Drago, 2004 in shape of body, position and shape of the holdfast, position of ventral sucker and distribution of vitellaria.
Journal of Basic and Applied Research International 21(2): 85-91, 2017 ISSN: 2395-3438 (P), ISSN: 2395-3446 (O)

International Knowledge Press www.ikpress.org

NEW RECORD OF GENUS Tylodelphys DIESING, 1850 (DIGENEA: DIPLOSTOMIDAE) IN Phalacrocorax niger FROM PAKISTAN MUHAMMAD MOOSA ABRO1*, ALI MURTAZA DHAREJO2, MUHAMMAD MUNIF KHAN2, NADIR ALI BIRMANI2 AND FIDA AHMED2 1

Postgraduate Center, Government College Hyderabad, Hyderabad, Sindh, Pakistan. 2 Department of Zoology, University of Sindh, Jamshoro, Pakistan.

AUTHORS’ CONTRIBUTIONS This work was carried out in collaboration between all authors. Authors MMA and AMD designed the study, wrote the protocol and interpreted the data. Authors MMA and NAB anchored the field study, gathered the initial data and performed preliminary data analysis. Authors MMK and FA managed the literature searches and produced the initial draft. All authors read and approved the final manuscript.

Received: 23rd February 2017 Accepted: 24th March 2017 Original Research Article Published: 3rd April 2017 __________________________________________________________________________________ ABSTRACT A total of 11 Little Cormorants, Phalacrocorax niger, were examined in Sanghar District of Sindh province of Pakistan in October 2014 – December 2015. In the intestine of three hosts twenty trematodes of the genus Tylodelphys Diesing, 1850 were recorded. The description of the present specimens points out several different features from already known species of this genus. Therefore, these are described at the genus level. The Little Cormorant, Phalacrocorax niger is a new host record of the genus Tylodelphys Diesing, 1850. And Tylodelphys is reported for the first time from Pakistan. Keywords: Avian trematode; Tylodelphys; Little Cormorant; Phalacrocorax niger; Sindh; Pakistan.

1. INTRODUCTION Little Cormorant, Phalacrocorax niger is piscivorous and migratory bird and commonly found in the study area, Sanghar: a central district of Sindh province of Pakistan. The water bodies found in Sanghar district provide favourable habitats to the definitive as well as intermediate hosts of different parasites. Due to its feeding habit P. niger possesses a reasonable probability to acquire helminthic infection from their surrounding environment (water bodies). Tylodephys Diesing, 1850 is a cosmopolitan and well established genus belonging to the family

Diplostmidae. It completes its life cycle in three hosts: birds acts as definitive host and gastropods and fishes are intermediate hosts. In past, numerous species of genus Tylodelphys Diesing, 1850 have been described from a variety of avian hosts throughout the world [1-7]. In this study Tylodelphys sp is recovered from the intestine of P. niger in Pakistan. Since there is no published record of Tylodelphys from the study area. Moreover, reported are available in Pakistan on helminths of Phalacrocorax niger [8-18]. Hence, Phalacrocorax niger is the first host record while Pakistan is a new locality record for the genus Tylodelphys Diesing, 1850.

_____________________________________________________________________________________________________ *Corresponding author: Email: [email protected];

Abro et al.; JOBARI, 21(2): 85-91, 2017

length, 0.22-0.278 in width. Post-testicular space short, measuring 0.14-0.17 in length. Vitellaria follicular dispersed in hind-body, extended in last quarter of fore-body. Genital cone present. Eggs large, numerous, found in mid of hind-body, measuring 0.062-0.071 in length and 0.042 in width.

2. MATERIAL AND METHODS Eleven Little Cormorants, Phalacrocorax niger were captured alive between October 2014 and December 2015 from the study area (Sanghar district of Sindh province, Pakistan). Helminthological examination was done within 2 days following capture of Cormorants. Trematodes of genus Tylodelphys collected from the intestine of freshly killed Cormorants were initially washed with normal saline. For Morphotaxonomy these specimens were fixed, after a light compression, in 70% alcohol, stained with borax carmine, dehydrated through the graded series of alcohols, cleared in clove oil and xylene and finally mounted in Canada balsam. Diagrams were drawn with the help of mirror type Camera Lucida and photograph was taken with Nikon digital camera. Unless, otherwise stated all measurement are in millimeter. Trematodes were identified with the aid of keys [19,20] and relevant literature [21-23].

3.2 Taxonomic Summary of Tylodelphys sp Family Subfamily Genus No. of specimens recovered: No. of hosts found positive: Site of infection: Locality: Record:

Diplostomidae Diplostominae Tylodelphys Diesing, 1850 20 03 of Phalacrocorax niger Intestine Sanghar, Sindh, Pakistan New host and locality record

4. DISCUSSION

3. RESULTS

Present fluke belongs to genus Tylodelphys Diesing, 1850 of family Diplostomidae and has pseudosucker, holdfast as well as indistinctly bipartite body which parasitizes Falconiformes, Ciconiiformes, Gaviformes, Strigiformes, Podiciformes and Suliformes birds [21,24,23] (Table 1) Tylodelphys clavata is type species of this genus distributed worldwide and many species have been described on the basis of metacercie and adult form. However, more than 17 species of adult form of this genus are described from various avian hosts from different areas of world (Table 1).

Eleven hosts were examined and twenty specimens were collected from intestine of three hosts. The infection rate was 27.27%.

3.1 Description Body of the fluke is linguiform, indistinctly bipartite having slightly conical hind-body, measuring 0.810.93 in length and 0.32-0.37 in width in testicular zone. Fore-body 0.51-0.57 in length, longer than hindbody which is 0.31-0.37 in length. Oral sucker subterminal, measuring 0.025-0.028 in length and 0.0250.028 in width. Pharynx present. Esophagus short, bifurcated into intestinal ceca. The intestinal ceca are long and extending almost to the posterior end of the body. Pseudosuckers large, well developed and measuring 0.06-0.09 in length and 0.02-0.04 in width.

Present specime differ from many species of genus including T. clavata, T. xenopi in having vitellaria below ventral sucker. Furthermore, it is compared with T. adulta, T. brevis, T. elongata, T. americana (Table 2) on basis of the morphometric features. Present specimens differ from T. brevis, T. elongate and T. Americana in shape of body. T. Americana (0.9-2.4) and T. adulta closely resemble present specimen. The fore-body of present specimen is smaller than T. elongata, T. Americana and T. adulta and larger than T. brevis. The hind-body of present species is closely related to T. adulta and T. Americana but smaller than T. elonagta and larger than T. brevis. The oral sucker of specimen is smaller than rest of referred species. The ventral sucker is larger than T. Americana and T. brevis but smaller than T. elongate and T. adulta. The ovary is almost identical to T. adulta, T. elongate and T. americana. The size of testes is almost same in all except T. brevis. A total of 13 eggs are observed. The number of eggs, in present specimen is closely corresponding to T. elongata and T. adulta. The

Ventral sucker round, well developed, much larger than oral sucker measuring 0.04-0.05 in length, 0.0310.035 in width and situated in the mid of fore-body. Holdfast organ oval with narrow slit in center situated in last quarter of fore-body, slightly extended into hind-body measuring 0.09-0.118 in length and 0.070.09 in width. Hind-body conical shaped, shorter than fore-body, measuring 0.30-0.37 in length. Ovary oval, sub-median, pre-testicular, measuring 0.11-0.114 in length and 0.066-0.078 in width. Testes tandem, unequal, situated in mid of hind-body, overlapped by large eggs. Anterior testis wider than long, measuring 0.12-0.142 in length and 0.25-0.342 in width. Distance between anterior testis and anterior extremity of fore-body is 0.09-0.10 in length. Posterior testis smaller, measuring 0.075-0.085 in 86

Abro et al.; JOBARI, 21(2): 85-91, 2017

present specimens differ from Tylodelphys adulta Lunaschi and Drago, 2004 in body size, smaller oral as well as ventral suckers, ovary size, number of eggs and host species. At this stage, on the basis of such differentiating characters, it is not justifiable to designate present specimens as a new species. In our opinion, these differences from the original description of T. adulta and rest of species are needed to be properly addressed. Hence, the specimens described in the present paper are identified at genus level. Moreover, fresh material will be collected from same host and locality to identify it at species level. It is of interest to note that the genus Tylodelphys Diesing, 1850 is being reported for the first time from Pakistan whereas Little Cormorant, Phalacrocorax niger is a new host record.

distribution of vitellaria and position of holdfast is same like that of T. adulta in which it is distributed up to ventral sucker. However, in rest of species it is extended ahead of ventral sucker. It is, therefore evident that the present specimens of trematode cannot be assigned to any species of the genus Tylodelphys Diesing, 1850, for the reasons that it is dissimilar in morphometric features, host species and different geographical locality of the host (Tables 1 and 2). However, from a comparison of the data shown in Table 2, present specimens are most similar to Tylodelphys adulta Lunaschi and Drago, 2004 in shape of body, position and shape of the holdfast, position of ventral sucker and distribution of vitellaria up to ventral sucker. Inspite of these similarities,

A

B

Fig. 1. Tylodelphus sp. A. Drawing line of entire worm; B. Photograph of entire worm. Scale bar: A. 0.4 mm

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Abro et al.; JOBARI, 21(2): 85-91, 2017

Table 1. List of adult forms of genus Tylodelphys with their host and locality S. no 1 2

Name of species Tylodelphys adulta Lunaschi and Drago 2004 T. aegyptius El-Naffar, Khalifa and Sakla, 1980

Host Podiceps major Ardea goliath

Locality Argentina Africa

3 4 5 6 7

T. americana (Dubois, 1936) Dubois, 1937 T. azetecae Varela, 2015 T. brevis Lunaschi and Drago 2008 T. chandrapali Jain and Gupta, 1970 T. clavata (V.Nordmann, 1832) Dies, 1850

Brazil Mexico Argentina India Europe

8

T. conifera (Mehlis 1846)

Mycteria americana, Tantalus loculator Podilymbus podiceps Mycteria americana --Ardea cinerea, Circus aeruginosus, Ciconia, Platalea, Falco, Egretta, Fulica, Heliaetus, Botaurus, Archibuteo, Larus, Podiceps Podiceps cristatus, P. griseigena

9 10 11

T. darteri, Mehra, 1962 Syn T. Indiana Mehra, 1962, T. indica Gupta, 1962 T. dubosilla (Mehra, 1962) T. elongate (Lutz, 1928) Dubois, 1937

12

T. excavata (Rud., 1803) Szidat, 1935

13 14 15 16 17 18 19 20 21 22

T. glossoides (Dubois, 1928) T. immer Dubois, 1961 T. mashonesis Beverley-Burton 1963 T. podicipina Kozicka and Niewiadomska 1960 T. podicipina robrauschi Dubois,,1969 T. rauschi (Singh, 1956) T. spinata Gupta, 1962 T. strigicola Odening, 1962 T. xenopi Nigrelli and Maraventano 1944 Tylodelphys Sp

Anhinga melanogaster Anhinga melanogaster Podiceps dominicus, Mycteria americana Ciconia ciconia, C. nigra, Nycticorax, Anas platyrhynchos, Podiceps cristatus, Mergus merganser, Buteo buteo, Circus aeruginosus Colymbus asiaticus Gavia immer Ardea cinerea Podiceps Podiceps griseigena holboelli Dissoura espiscopus espiscopus Anastomus oscitans Strix aluco alco Anhinga melanogaster Phalacrocorax niger

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References Lunaschi -and Drago, [21] El-Naffar et al. [25] Blasco-Costa, [23] Yamaguti, [19] Varela, [7] Drago and Lunaschi, [22] Blasco-Costa, [23] Yamaguti, [19]

Switzerland Germany India

Yamaguti, [19]

India Brazil Venezuela Europe

Yamaguti, [19] Yamaguti, [19]

Switzerland North America Rhodeshia Poland Alaska India India Germany Africa Pakistan

Yamaguti, [19] Yamaguti, [19] Yamaguti, [19] Yamaguti, [19] Yamaguti,[19] Yamaguti, [19] Yamaguti ,[19] Yamaguti, [19] Blasco-Costa, [23] Present study

Yamaguti,[19]

Yamaguti, [19]

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Table 2. Comparison of various species of Tylodelphys with present form Name of organ

Forebody Hindbody Oral sucker Ventral Sucker Prepharynx Pharynx Esophagus Pseudosucker Holdfast Anterior Testes Posterior testis Ovary Cirrus sac Eggs No. eggs Vitellaria Host

Tylodelphys sp Present study Indistinctly bipartite, 0.81-0.930 0.51-0.570 X 0.31-0.362 0.30-0.378 X 0.30-0.370 0.025-0.028 X 0.025-0.028 0.04-0.05 X 0.031-0.035 Absent 0.024-0.028 0.037-0.042 0.06-0.09 X 0.02-0.04 0.09-0.118 X 0.07-0.09 0.12-0.142 X 0.25-0.342 0.075-0.085 X 0.22-0.278 0.11-114 X 0.066-0.078 Absent 0.062-0.071 X 0.0 42 8-13 Present Phalacrocorax niger

T. adulta Lunaschi and Drago, Indistinctly bipartite, 1.12-1.44 0.72-0.95 X 0.43-0.59 0.269-0.528 X 0.394-0.557 0.071-0.097 X 0.083-0.103 0.060-0.080 X 0.078-0.077 Absent 0.071-0.110 X 0.053-0.074 0.025 0.145-0.216 X 0.074-0.126 0.195-0.250 X 0.178-0.274 0.120-0.121 X 0.216-0.294 0.115-0.168 X 0.211-0.427 0.073-0.083 X 0.073-0.097 Absent 0.087-0.099 X 0.051-0.059 1-20 Present Podiceps major

T. brevis Drago and Lunaschi, Indistinctly bipartite, 0.57-0.85 0.371-0.507 X 0.202-0.280 0.174-0.343 X 0.169-0.275 0.040-0.067 X 0.044-0.060 0.024-0.036 X 0.027-0.054 Absent 0.045-0.057 X 0.022-0.031 0.010-0.015 0.048-0.074 X 0.029-0.059 0.069-0.131 X 0.050-0.102 0.041-0.071 X 0.133-0.226 34-83 X 121-202 0.034-0.053 X0.0 29-0.078 Absent 0.083-0.102 X 0.054-0.064 15 Present M. americana

Location Locality

Intestine Pakistan

-Argentina

Intestine Argentina

Body

89

T. elongata (Lutz, 1928) Dubois, 1937 Indistinctly bipartite, 1.50-2.03 0.800-1.120 X 0.450-0.520 0.450-0.650 X 0.430-0.4352 0.080-0.100 X0.0 90-0.104 0.070-0.090 X0.0 99-0.110 Absent 0.063-0.073 X 0.060-0.068 -----0.110-0.210 X0.0 80-0.130 0.160-0.210 0.100-0.104 X 0.445-0.460 0.110-0.180 X 0.400-0.445 0.075-0.125X0.0 95-0.200 Absent 0.090-0.097 X0.0 60-0.066 30 Present M. americana J. mycteria Intestine Brazil, Venezuela and Cuba

T. americana Dubois, 1937 Indistinctly bipartite, 0.90-2.40 0.55-1.50 X 0.29-0.78 0.310-0.900 X0. 250-0.650 0.048-0.087 X 0.048-0.095 0.033-0.076 X 0.036-0.108 0.012 0.049-0.080 X0.0 33-0.072 0.040 0.050-0.122 X0.0 68-0.080 0.115-0.390 X 0.110-0.510 0.110-0.300 X 0.270-0.575 0.110-0.290 X0. 240-0.520 0.063-0.135 X 0.080-0.090 Absent 0.084-0.103 X 0.053-0.063 Present M. americana J. mycteria Intestine Brazil, Venezuela and Mexico

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5. CONCLUSION The trematodes of genus, Tylodelphys Diesing, 1850 were recorded from the intestine Phalacrocorax niger. These are described at genus level. Tylodelphys is being reported for the first time from the avian host in Pakistan.

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COMPETING INTERESTS

11.

Authors have declared that no competing interests exist.

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