cestode in sabah fish 2006

7/30/2019 Cestode in Sabah Fish 2006

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A new species of Aberrapex Jensen, 2001 (Cestoda: Lecanicephalidea)from Taeniura lymma (Forsska l) (Myliobatiformes: Dasyatidae)

from off Sabah, Malaysia

K. Jensen*Department of Ecology and Evolutionary Biology and the Natural History Museum and Biodiversity Research

Center, University of Kansas, 1200 Sunnyside Ave., Lawrence, Kansas, 66045, USA

Accepted for publication 17th August, 2005

Abstract

A new lecanicephalidean species of Aberrapex Jensen, 2001 is described from the blue-spotted fantail ray

Taeniura lymma (Forsska l) collected off the eastern coast of Sabah in Malaysian Borneo. This is the first

record of a lecanicephalidean tapeworm from the island of Borneo and the first record of Aberrapex from

this host species. A. manjajiae n. sp. is easily distinguished from its two congeners, A. senticosus Jensen,

2001 and A. arrhynchum (Brooks, Mayes & Thorson, 1981) Jensen, 2001, based on its overall smaller size

(9281,971 vs 1,4856,333 and up to 3,350 lm long, respectively) and fewer testes (1019 vs 2040 and 18

25, respectively). In addition, A. manjajiae n. sp. is readily distinguished from A. senticosus based on a more

anteriorly positioned genital pore (7685 vs 5272% of proglottid length from posterior end) and its distal

bothridial microthrix pattern. A. manjajiae n. sp. can be further distinguished from A. arrhynchum based on

its smaller scolex (82101 119164 vs 177186 233326 lm). The host distribution of Aberrapex is

expanded from the Myliobatidae to include the Dasyatidae.

Introduction

Jensen (2001) erected Aberrapex Jensen, 2001 for

A. senticosus Jensen, 2001 from the bat eagle ray

Myliobatis californicus Gill (Myliobatiformes: My-

liobatidae) in the Gulf of California, Mexico. At

that time, she recognised a second member of the

genus, A. arrhynchum (Brooks, Mayes & Thorson,

1981) Jensen, 2001. This latter species was origi-nally described in Discobothrium van Beneden,

1870. A. arrhynchum was collected from the

southern eagle ray M. goodei Garman from the

Ro de la Plata estuary, Uruguay. A survey of

metazoan parasites of elasmobranchs from Malay-

sian Borneo resulted in the collection of specimens

of a new species of Aberrapex from the blue-

spotted fantail ray Taeniura lymma (Myliobatifor-

mes: Dasyatidae). This species is described here.

Materials and methods

Fifteen specimens of Taeniura lymma were col-

lected from Sabah (Malaysian Borneo) in the

Celebes Sea. These included 1 female off Kunak,

and 3 males and 1 female off Semporna in June

2002, and 5 males and 5 females off Pulau Mabul

in May 2003. Rays were collected using Hawaiian

slings. Each ray was opened with a ventral

longitudinal incision from the anus to the pericar-

dial chamber. The spiral intestine was removed

and opened with a longitudinal incision. A subset

of tapeworms was removed in the field and fixed in

10% formalin buffered with seawater. The spiral

intestines were subsequently placed in 10% for-

malin buffered with seawater for several weeks

before being transferred to 70% ethanol for

storage. The spiral intestines were examined for

additional tapeworms with a dissecting microscope

in the laboratory.*Author for correspondence (E-mail: [email protected])

Systematic Parasitology (2006) 64:117123 Springer 2006DOI 10.1007/s11230-005-9026-2


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Tapeworms were prepared for light andscanning

electron microscopy (SEM). Specimens prepared as

whole-mounts for light microscopywerehydrated in

a graded ethanol series, stained in Delafields

haematoxylin, dehydrated in a graded ethanol

series, cleared in methyl salicylate and mounted onglass-slides in Canada balsam. Specimens prepared

as histological sections were dehydrated in a graded

ethanol series, cleared in xylene and embedded in

paraffin according to conventional techniques.

Serial cross-sections were cut at 67 lm intervals

using a TBS CUT 4060 Microtome, attached to

glass-slides by floating sections on 3% sodium

silicate, allowed to dry, dewaxed in xylene, hydrated

in a graded ethanol series, stained with Gills

haematoxylin, counterstained with eosin, dehy-

drated in a graded ethanol series, cleared in xyleneand mounted in Canada balsam. Specimens pre-

pared for SEM were hydrated in a graded ethanol

series, post-fixed in 1% osmium tetroxide overnight,

dehydrated in a graded ethanol series, transferred to

hexamethyldisilizane (HMDS) for 15 min, allowed

to air-dry and mounted on aluminum stubs on

double-sided adhesive carbon tape. Specimens were

sputter coated with c.300A of gold and examined

with a Hitachi S4700 field emission scanning elec-

tron microscope at the Microscopy and Imaging

Facility, American Museum of Natural History in

New York, New York, USA, or a Zeiss LEO 1550field emission scanning electron microscope at the

Microscopy and Electronic Imaging Laboratory,

University of Kansas, Lawrence, Kansas, USA.

Line drawings were prepared with the aid of a

drawing tube attached to a Zeiss Axioskop 2 Plus.

All measurements of reproductive organs were

taken from mature proglottids and are given in

micrometres (lm) unless specified otherwise. Mea-

surements are given as the range followed in

parentheses by the mean, standard deviation, the

number of worms examined and the total numberof measurements taken if greater than 1 measure-

ment was taken per worm. For two-dimensional

measurements, length is given before width.

Museum abbreviations used are as follows:

IPMB, Institut Penyelidikan Marin Borneo (Bor-

neo Marine Research Institute), Universiti Malay-

sia Sabah, Kota Kinabalu, Sabah, Malaysia; LRP,

Lawrence R. Penner Parasitology Collection,

Department of Ecology and Evolutionary Biology,

University of Connecticut, Storrs, Connecticut,

USA; MZUM (P), Muzium Zoologi, Universiti

Malaya, Kuala Lumpur, Malaysia; and USNPC,

United States National Parasite Collection, Belts-

ville, Maryland, USA. The elasmobranch classifi-

cation follows Carpenter & Niem (1999).

Aberrapex manjajiae n. sp.

Type-host: Taeniura lymma (Forsska l), the blue-

spotted fantail ray (Myliobatiformes: Dasyatidae).

Type-locality: Off Pulau Mabul (0415N, 11837E), Sabah, Malaysia, Celebes Sea.

Additional localities: Off Kunak (0441N, 118

15E), Sabah, Malaysia, Celebes Sea.

Site of infection: Spiral intestine.

Specimens deposited: Holotype (MZUM (P) No.

158) and 1 paratype (MZUM (P) No. 159); 3

paratypes (IPMB Nos 77.11.0103); 5 paratypes (4whole worms, 1 cross-sectioned worm) (USNPC

Nos 96992 & 96993); 8 paratypes (LRP Nos 3805

3808, 37933796); 3 paratypes (prepared for SEM)

(KUNHM, authors collection).

Etymology: This species is named after Dr Berna-

dette Mabel Manjaji Matsumoto for her valuable

collaboration on all aspects of the Sabah portion

of the metazoan parasite survey of the elasmo-

branchs of Malaysian Borneo.

Description (Figures 12)

(Based on 17 whole worms, 1 cross-sectioned

worm and 3 prepared for SEM). Worms 9271,971

(1,515261; 18) long; maximum width at terminal

proglottid; 2545 (305; 18) proglottids, euapo-

lytic. Scolex 82101 (916; 17) 119164

(13917; 17), consisting of 4 bothridia (also

referred to as acetabula or suckers). Each bothri-

dium cup-shaped, 6689 (776; 17; 34) 5479

(657; 17; 34). Apical modification of scolex

proper and apical organ absent. Distal and prox-imal surfaces of bothridia covered with large

blade-like spiniform microtriches and long filiform

microtriches (Figure 2C,D); blade-like spiniform

microtriches on distal surfaces restricted to central

bothridial region (Figure 2A,B). Scolex proper at

apex of scolex covered with long filiform micro-

triches only (Figure 2E).

Cephalic peduncle absent. Strobila covered

with long filiform microtriches (Figure 2H); fili-

form microtriches becoming shorter and more

triangular towards posterior margins of proglottid

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(Figure 2G). Proglottids craspedote. Immature

proglottids 2444 (295; 18) in number, initially

wider than long, becoming longer than wide

with maturity, laciniate; posterior-most immature

proglottid 116243 (18333; 18; 36) 113178

(145 18; 18; 36). Mature proglottids 1 in num-

Figures 1. AF. Line drawings of Aberrapex manjajiae n. sp. A. Whole worm (holotype, MUZM[P] No. 158). B. Scolex (paratype,USNPC No. 96992). C. Terminal mature proglottid (paratype, USNPC No. 96993). D. Detail of oo type (paratype, USNPC No.96993). E. Cross-section of mature proglottid between ovary and cirrus-sac (paratype, USNPC No. 96992). F. Cross-section of ma-ture proglottid at level of ovarian bridge (paratype, USNPC No. 96992). Note: only three of the four lobes are visible. Abbreviations:MG, Mehlis gland; OC, ovicapt; OV, ovary; T, testis; VD, vas deferens; VE, vas efferens; VG, vagina; U, uterus; UD, uterine duct.

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ber, 333674 (47582; 18) 148207 (17017;

18). Testes 1019 (152; 15; 25) in number, 1127

(184; 17) 4493 (6816; 17), in single field

extending from anterior margin of proglottid to

ovary, slightly overlapping anterior margin of

ovary, 12 irregular columns in frontal view, 1

Figures 2. AH. Scanning electron micrographs of Aberrapex manjajiae n. sp. A. Scolex. Letters correspond to the figures showing

enlarged views of these surfaces. B. Scolex showing the microthrix pattern on the distal bothridial surfaces. C. Distal bothridialsurface. D. Proximal bothridial surface. E. Apex of the scolex. F. Bothridial margin showing spiniform microtriches in profile andsensory cilia. G. Surface of proglottid at the posterior margin. H. Surface of a proglottid. Scale-bars: A, 30 lm; B, 20 lm; CH,1 lm.

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row deep in cross-section (Figure 1E). Vas efferen-

tia not observed. Vas deferens in maturing pro-

glottids in form of thin tube, extending submedially

in proglottid from posterior to Mehlis gland to

cirrus-sac, entering cirrus-sac at posterior margin;

vas deferens expanded to form conspicuous exter-nal seminal vesicle in fully mature proglottids in

which testes are usually degenerated. External

seminal vesicle extensive, saccate, extends more or

less along mid-line of proglottid from region

posterior to oo type to cirrus-sac. Internal seminal

vesicle absent. Cirrus-sac pyriform, 70112

(9013; 17) 2655 (388; 17), contains coiled

cirrus. Cirrus unarmed. Ovary H-shaped in frontal

view, tetralobed in cross-section (Figure 1F), 32

112 (7119; 18) 67124 (9214; 18), lobulate,

symmetrical; ovarian bridge in anterior half ofovary. Mehlis gland at posterior margin of ovary.

Vagina opens posterior to cirrus-sac into genital

atrium, extends submedially in proglottid from

genital atrium to oo type, coils between posterior

lobes of ovary; vaginal sphincter absent. Genital

pores lateral, irregularly alternating, 7685%

(812.0%; 18) of proglottid length from posterior

end. Uterus saccate, extends along mid-line

of proglottid from oo type region to posterior

margin of cirrus-sac; uterine duct enters uterus at

its anterior end. Vitellarium follicular; vitelline

follicles medullary, lateral, extends entire length ofproglottid, interrupted at level of ovary and on

poral side by cirrus-sac, 418 (113; 18; 54) 21

68 (3710; 18; 54); 2 vitelline follicles on each side

of proglottid in cross-section (Figure 1C,E). Single

pair of excretory ducts. Eggs not observed.

Remarks

This species belongs in the lecanicephalidean genus

Aberrapex, because it possesses a vagina extending

along the lateral margin of the proglottid anteri-orly from the ovary and entering the genital pore

posterior to the cirrus-sac, an extensive vas defer-

ens in the form of an external seminal vesicle

originating at the level of the ovary and a scolex

lacking both an apical modification of the scolex

proper and an apical organ. The genus contains

only 2 other species, A. senticosus and A. arrhyn-

chum. A. manjajiae n. sp. can be distinguished

from A. senticosus based on its smaller overall size

(9281,971 vs 1,4856,333 lm), shorter mature

proglottids (333674 vs 8081,973 lm), its

possession of fewer testes (1019 vs 2040), testic-

ular arrangement (in 12 columns rather than 34

columns) and its possession of a genital pore

positioned more anteriorly in the proglottid (7685

vs 5272% of proglottid length from the posterior

end). In addition, the uterus stops short of thecirrus-sac in A. manjajiae, whereas it extends well

anterior to the cirrus sac in A. senticosus. Finally,

while the entire distal bothridial surfaces of

A. senticosus are covered with large blade-like

microtriches, these blade-like microtriches on the

distal bothridial surfaces of A. manjajiae are

restricted to a central region of the bothridia;

these structures are absent from the anterior-

and posterior-most regions of the bothridia of

A. manjajiae. A. manjajiae most closely resembles

A. arrhynchum. It can be distinguished fromA. arrhynchum, however, based on its smaller

overall size (9281,971 vs up to 3,350 lm long)

and its possession of fewer testes (1019 vs 1825).

In addition, the scolex of A. manjajiae is smaller

than that of A. arrhynchum (82101 119164 vs

177186 233326 lm), as are the bothridia

(6689 5479 vs 132216 120256 lm).

Furthermore, while an expansion of the vas

deferens to form an external seminal vesicle was

not observed in any of the 22 paratypes of

A. arrhynchum examined (Jensen, 2001), a con-

spicuous seminal vesicle was observed in theterminal proglottids of approximately 50% of the

specimens in the type-series of A. manjajiae.

Aberrapex manjajiae was present in rays from

all three localities, with an overall prevalence of

30% (i.e. in 5 of 15 host individuals examined).

Discussion

Prior to this study, the known host associations

and geographical distribution of Aberrapex werelimited. Species of Aberrapex had been reported

only from eagle rays of the genus Myliobatis

(Jensen, 2001; Jensen, 2005). With inclusion of

A. manjajiae, the known host distribution of

Aberrapex can be expanded from the family

Myliobatidae to include the Dasyatidae, both of

the order Myliobatiformes. Previously known

only from the Gulf of California and the

southwestern Atlantic Ocean, the geographical

distribution of the genus now includes the Celebes

Sea. This is the first record of Aberrapex from off

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Southeast Asia and the first record of a lecani-

cephalidean tapeworm from an elasmobranch

from off Borneo.

The tapeworm fauna of Taeniura lymma has

been investigated in some detail previously from

several localities throughout its distribution in theIndian and Western Pacific Oceans (south of

Taiwan). Specimens of T. lymma collected from

the Red Sea off Egypt (Saoud, 1963; Hassan, 1982;

Saoud et al., 1982; Ramadan, 1984; Ramadan,

1986), the Gulf of Carpentaria off the Northern

Territory, Australia (Tyler, 2001), the Coral Sea

off Queensland, Australia (Williams, 1964) and the

Indian Ocean off Java, Indonesia (Palm, 2004)

have been examined for cestodes. A total of 11

species of tapeworms have been described from

T. lymma to date. These are the trypanorhynchsMecistobothrium pauciortesticulatum Palm, 2004

and Parachristianella indonesiensis Palm, 2004 (see

Palm, 2004), the diphyllideans Echinobothrium

n. sp. (see Tyler, 2001), E. helmymohamedi Saoud,

Ramadan & Hassan, 1982 and E. heroniense

Williams, 1964 (see Williams, 1964; Saoud et al.,

1982; Tyler, 2001), the tetraphyllideans Anthoboth-

rium sexorchidum Williams, 1964, A. taeniurae

Saoud, 1963, Rhinebothrium ghardaguensis

Ramadan, 1984 and R. taeniurae Ramadan, 1984

(Saoud, 1963; Williams, 1964; Ramadan, 1984),

and the lecanicephalideans Cephalobothrium tae-niurai Ramadan, 1986 and Polypocephalus saoudi

Hassan, 1982 (see Hassan, 1982; Ramadan, 1986).

In 1964, Williams commented on the non-

overlap of tapeworm species reported from

specimens of T. lymma taken from Australia and

the Red Sea. He noted that different species of

Anthobothrium van Beneden, 1850 and Echino-

bothrium van Beneden, 1849 parasitised T. lymma

in these disparate localities. In an attempt to

explain the different cestode faunas, Williams

(1964) suggested that either specimens ofT. lymmahad been misidentified in one of the localities or

that T. lymma from Australia might be a distinct

subspecies (Whitley, 1940 in Williams, 1964) from

that in the Red Sea. Misidentification of T. lymma

is unlikely due to its conspicuous colour pattern

and its tail morphology, which is unusual for

dasyatids. However, distinct subspecific status of

T. lymma from Australia has not been supported

in recent taxonomic work on the elasmobranchs

of the Australian region (Last & Stevens, 1994;

Compagno & Last, 1999). Williams (1964) went on

to say that collections from India, Sri Lanka and

the Malay Archipelago had the potential to

contribute to our understanding of this system.

Aberrapex manjajiae is only one among, conser-vatively, 30 species of tapeworms that were found

to parasitise T. lymma off Sabah, Malaysia (Caira

& Jensen, unpublished data) including lecaniceph-

alideans, tetraphyllideans, diphyllideans and try-

panorhynchs. Most of these species are new to

science, and descriptions of which are beyond the

scope of the present study. Interestingly, some of

these species represent genera that have not

previously been described from this host species.

For example, specimens of T. lymma from Sabah

are parasitised by lecanicephalideans representingtwo new genera, in addition to Aberrapex and

others. These preliminary data from a third

geographical region suggest that T. lymma may

indeed host different parasite faunas in different

geographical areas.

Acknowledgements

I thank Rayner Datuk Stuel Galid, Director of

the Department of Fisheries, Sabah, Malaysiafor his logistical assistance, as well as Mohd.

Tahir Hj. Ahmad, Mohamad Sappan, Aldam

Jalil and Maidin Osman from the Semporna

Office of the Department of Fisheries, Sabah,

Malaysia for their valuable assistance in obtain-

ing specimens. I am particularly grateful to

Dr Janine Caira for organising the collecting in

Sabah and for her participation in the fieldwork

conducted for this study. I am also grateful to

Loren Caira and Dr Gavin Naylor for the collec-

tion of the hosts, and to Garrett Call for his

assistance with specimen preparation. Thesecollections were conducted under permit No.

UPE:40/200/19SJ.925 from the Economic Plan-

ning Unit in Kuala Lumpur and permit No.

JKM 10024/13/1/223(59) from the Chief

Ministers Department, Kota Kinabalu, Sabah,

Malaysia. This work was supported with funds

from NSF BS&I grant No. DEB 0103640 to J.

N. Caira, G. Naylor, P. Last, J. Stevens and KJ.

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