Meggittina numida n. sp. (Cyclophyllidea: Catenotaeniidae),a parasite of the Shaw’s jird Meriones shawi (Duvernoy)(Rodentia: Gerbillinae) in Tunisia

Jamel Jrijer • Lassad Neifar

Received: 28 January 2014 / Accepted: 29 March 2014

� Springer Science+Business Media Dordrecht 2014

Abstract Meggittina numida n. sp. (Cyclophyllidea:

Catenotaeniidae: Skrjabinotaeniinae) is described

from the small intestine of the Shaw’s jird Meriones

shawi (Duvernoy) (Rodentia, Muridae, Gerbillinae)

trapped in central Tunisia. The new species can be

distinguished from the four other members of Meg-

gittina Lynsdale, 1953 by the high number of

proglottids (8–25 vs max. 6) and by the elongated

strobila (8.2–60 mm in length vs max. 5.6 mm). M

numida n. sp. further differs from M. cricetomydis

(Hockley, 1961) in the direction of gravid proglottids;

from M. baeri Lynsdale, 1953 in having narrower and

much longer strobila; from M. aegyptiaca (Wolfgang,

1956) in the greater number of testes and the larger

cirrus-sac; and from M. gerbilli in the position of the

genital pore. The diagnosis of Meggittina is amended

in order to include the most specific features of M.

numida n. sp. as follows: strobila consisting of a small

scolex, wide neck and one to twenty-five proglottids.

This is the first species of Meggittina described from

Tunisia. The taxonomic relationships of Meggittina

spp. are discussed in the light of the description of the

new species.

Introduction

Twenty-seven species of rodents are reported in

Tunisia (Bernard, 1970; Bernard & Ben Rachid

1969b; Gharaibeh, 1997; Aulagnier et al., 2009);

these are spread within over 12 genera belonging to

five families. The Muridae Illiger is the most diverse

family with eight genera and 21 species, most of them

belonging to the subfamily Gerbillinae Gray, small

mammals adapted to arid climate conditions (Carleton

& Musser, 1984). For a better understanding of the

biodiversity and ecosystem functioning in the arid

environment, helminths parasitising rodents should be

investigated (Behnke et al., 2000; Barnard et al. 2003).

In addition, the dependence of the parasites on their

hosts provides a useful research model in the fields of

ecology and evolutionary biology (Poulin, 2004;

Morand et al., 2006).

Most of the studies carried out on the helminths of

the Gerbillinae in North Africa are focused on

zoonotic parasites including species such as Echino-

coccus spp. and Leishmania spp. associated with

human health risks (Ghawar et al., 2011; Lahmar et al.,

2013). Some studies on the taxonomy of helminths

have also been carried out by Joyeux & Baer (1927,

1928), Bernard (1963, 1970, 1987), Bernard & Ben

Rachid (1969a) and Bernard et al. (1964).

In Tunisia, at least seven species of the Cyclo-

phyllidea Braun, 1900 are reported in hosts of the

Gerbillinae. These are Hymenolepis sp. and Hymenol-

epis dimunita Rudolphi, 1819 in Meriones shawi

J. Jrijer � L. Neifar (&)

Laboratoire de Biodiversite et Ecosystemes Aquatiques,

Faculte des Sciences de Sfax, Universite de Sfax,

BP 1171, 3038 Sfax, Tunisia

e-mail: lassad.neifar@fss.rnu.tn

123

Syst Parasitol (2014) 88:167–174

DOI 10.1007/s11230-014-9488-1

(Duvernoy) (see Joyeux, 1923), Raillietina trapezo-

ides (Janicki, 1904) in Psammomys obesus Cretzsch-

mar (see Fichet-Calvet et al., 2003), polycephalic

cysticerci of Taenia parva Baer 1924 and Taenia

endothoracicus Kirchenblatt, 1948 (see Bernard,

1963), cysticerci of Dipylidiinae Stiles, 1896 and

cysticerci of Joyeuxiella pasqualei (Diamare, 1893)

from the liver of Gerbillus pyramidum Geoffroy (syn.

Gerbillus tarabuli Thomas) (see Bernard et al., 1964).

During a recent study on parasites of rodents of the

Gerbillinae in central Tunisia, we examined the

gastrointestinal tract of the Shaw’s jird Meriones

shawi (Duvernoy) and revealed the presence of a new

species of a cyclophyllidean cestode belonging to the

genus Meggittina Lynsdale, 1953 (Catenotaeniidae).

In the present paper, this new species is described and

the diagnosis of Meggittina is amended.

Materials and methods

The study was conducted during four sampling

campaigns between April 2011 and March 2012.

Sampling was conducted in the surroundings of

Mezzouna City in central Tunisia, an arid region

characterised by lower vegetation composed by

perennial halophyl grasses (Ouled Dhaou et al.,

2010). Rodents were captured alive in live traps

(Manufrance), which were placed selectively near

burrows showing signs of recent activities and gener-

ally under tufts of Chenopodiaceae. Traps were set out

and inspected after 24 hours during three days.

Thirty-three trapped Meriones shawi were brought

to laboratory, sacrificed, sexed, weighed and mea-

sured. The body cavity, liver and gastrointestinal tract

(stomach, small and large intestine and caecum) were

examined for helminths which were then washed in

physiological saline solution. Cestodes were fixed in

70% alcohol or Holland Bouin’s fixative, stained with

Semichon’s acetocarmine, dehydrated in a graded

ethanol series, cleared in clove oil and mounted in

Canada balsam.

Illustrations and measurements were made on

stained specimens using Leitz light microscope

equipped with a drawing tube. Illustrations were

scanned and redrawn using CorelDRAW software

(Corel Corporation). All measurements are given in

micrometres unless otherwise indicated as the range

followed by the mean ± standard deviation and the

number of measurements in parentheses. Taxonomic

terminology follows Tenora et al. (1980) and Khalil

et al. (1994).

Order Cyclophyllidea van Beneden in Braun,

1900

Family Catenotaeniidae Spasskii, 1950

Subfamily Skrjabinotaeniinae Genov & Tenora,

1979

Genus Meggittina Lynsdale, 1953

Meggittina numida n. sp.

Type-host: Meriones shawi Duvernoy (Gerbillinae).

Type-locality: Steppe land near Mezzouna City,

Tunisia (34�290N, 9�420E).

Site: Small intestine.

Infection details: Prevalence 48.5% (16 infected/33

examined); mean intensity 4.2 (1–13); mean abun-

dance 2.0 ± 3.1.

Etymology: The species is named after the Numidian

Berbers, the ancestors of the people of Mezzouna.

Type-material: Holotype (NHMUK 2014.3.13.2) and

three paratypes (NHMUK 2014.3.13.3-5) are depos-

ited in the Natural History Museum, London, UK.

Three paratypes are deposited in the Museum National

d’Histoire Naturelle, Paris (MNHN HEL424).

Description (Figs. 1–3)

[Measurements based on 24 whole mounted worms.]

Worms apolytic, with general appearance of an arrow.

Total body length 8.2–60 mm (29 ± 6 mm; n = 24)

measured from anterior end of scolex to middle of

posterior end of last proglottid; maximum width at last

proglottids, 3.2–7.3 mm (4.45 ± 0.36 mm; n = 24).

Gravid proglottid cut posteriorly by a longitudinal

fissure forming 2 lateral wings (Fig. 1A). Strobila

Fig. 1 Meggittina numida n. sp. A, Whole mount, ventral view;

B, Scolex; C, Mature proglottid; D, Terminal genitalia; E, Egg

from a gravid proglottid. Abbreviations: cgp, common genital

pore; cp, cirrus-sac; cr, cirrus; gp, gravid proglottid; im,

invaginated membrane; m, membrane; oc, oncosphere; os,

osmoregulatory system; ov, ovary; sc, scolex; sg, shallow

grooves; sk, sucker; sr, seminal receptacle; st, uterine stem; ts,

testis; ut, uterus; v, vagina; vg, vitelline gland. Scale-bars: A,

5 mm; B–D, 100 lm; E, 10 lm

c

168 Syst Parasitol (2014) 88:167–174

123

A

B

C

D

E

Syst Parasitol (2014) 88:167–174 169

123

acraspedote, thin, delicate, almost membranous, com-

prised of 8–25 proglottids (18 ± 2; n = 24), wider

than long at all stages of development, with following

arrangement (Fig. 1A): scolex followed by 3–7 imma-

ture proglottids, 2–8 mature proglottids, 2–6 pregravid

proglottids and 1–4 gravid proglottids.

Scolex triangular, with rounded anterior end, with-

out distinct neck, 245–375 (295 ± 16; n = 24) long,

460–680 (574 ± 26; n = 24) wide at level of poster-

ior margin of suckers (Fig. 1B), divided into 4 lobes

by shallow grooves. Remnant of apical sucker appear-

ing as evertible apical depression on scolex in juvenile

specimens (Fig. 2). Rostellum absent. Suckers 4,

unarmed, rounded, 90–165 (129 ± 6; n = 48) in

diameter. Osmoregulatory system complex, with net-

work of canals arising from scolex region from which

a group of longitudinal vessels leaves on two sides of

strobila (Fig. 1B).

Genital pores alternate irregularly, open at anterior

quarter of lateral proglottid margins. Testes numerous,

spherical, in two lateral fields surrounding female organs;

testes number 57–152 (111 ± 10; n = 35) in poral field,

65–160 (119 ± 10; n = 35) in antiporal field; Testes

diameter in mature proglottids 45–85 (59 ± 4; n = 48)

(Fig. 1C). Cirrus-sac elongate (Fig. 1D), with thick

muscular walls, opens close to vagina at genital pore,

130–355 (264 ± 18; n = 42) long, 35–55 (46 ± 2;

n = 42) wide. Cirrus unarmed. External vas deferens

loops twice and extends medially. Ovary compact, with

numerous dendritic branches, asymmetrical, situated

slightly porally. Vitelline gland with irregular shape and

lobed margins, deeply stained, located in poral half of

proglottid, between ovary and poral group of testes

(Fig. 1C). Vagina elongate, posterior to cirrus-sac, with

thin walls, ends in large seminal receptacle (Fig. 1D),

273–746 (555 ± 39; n = 42) long, 13–21 (18 ± 1;

n = 42) wide. Seminal receptacle ovoid or round, with

thick walls, with maximum diameter 104–284

(211 ± 15; n = 42) attained in mature and pregravid

proglottids. Seminal receptacle transparent in immature

proglottids, filled with spermatozoa and stained deeply in

mature and pregravid proglottids, gradually attenuated

and disappearing in last proglottids (Fig. 1A). Central

part of proglottids occupied by developing uterine loops

which occur as bundle of tubes with 4–6 branches arising

from very short basal stem located close to proglottid

margins; with further maturation, uterine branches

become progressively voluminous and elongated more

toward posterior margins than toward centre of

proglottids (Fig. 1A). Eggs biconvex, elongate, 15–38

(27 ± 2; n = 56) long, 10–17 (13 ± 1; n = 56) wide,

with thin external membrane invaginated medially;

oncosphere small, with thin envelope and 6 hooks 4–10

(8 ± 1; n = 56) long (Fig. 1E).

Remarks

Morphological features of this species such as the

ramified osmoregulatory system with network of

longitudinal canals, the shape of the gravid proglottids

widening to form two lateral wings, and the general

appearance of the worm with tendency to twist spirally

along the longitudinal axis, place this species in the

genus Meggittina (Cyclophyllidea, Catenotaeniidae,

Skrjabinotaeniinae). The taxonomy of Meggittina spp.

is challenging because they lack rostellum, hooks and

are otherwise anatomically uniform. Species delimi-

tation and identification have largely been based on the

number of proglottids (Table 1) and the shape of the

gravid proglottids (Mackiewicz, 2003) (Fig. 3).

The new species can be readily distinguished from the

other members of the genus by the greater number of the

proglottids varying from eight to 25 in comparison with a

reduced strobila consisting of one to six proglottids in the

other species (Table 1). M. numida n. sp. can also be

Fig. 2 Meggittina numida n. sp. immature cestode. Abbrevia-

tions: cgp, common genital pore; ra, remnant of apical sucker;

sk, sucker; ts, testes; ut, uterus; vg, vitelline gland. Scale-bar:

200 lm

170 Syst Parasitol (2014) 88:167–174

123

distinguished from its congeners as follows. From M.

cricetomydis (Hockley, 1961), a parasite of Cricetomys

gambianus Waterhouse in Nigeria, it differs in the

direction of the gravid proglottid, backward in the new

species and forward in the latter (Hockley, 1961). From

M. baeri Lynsdale, 1953, a parasite of rats in Zimbabwe

(Lynsdale, 1953; Quentin, 1971), it can be differentiated

on the basis of the length of the strobila (1–2 mm in

M. baeri vs 8.2–60 mm in M. numida).

In the irregular alternate position of the genital

pores, the new species is similar to M. aegyptica

(Wolfgang, 1956) described from Meriones sp.,

Gerbillus gerbillus (Olivier) and Acomys cahirinus

(Desmarest) in Egypt. However, it differs in having a

greater number of proglottids (8–25 vs 4–6) and testes

(112–312 vs 93–197), a larger cirrus-sac (130–355 vs

180–280 lm) and larger eggs (15–38 vs 10–14 lm).

Meggittina numida n. sp. also differs from M. gerbilli

(Wertheim, 1954) in the position of the genital pore,

irregularly alternating in the former and regularly

alternating in the latter, and in having a longer strobila

(8.2–60 mm vs 4.5–5 mm) (Table 1).

Several authors have indicated the presence of a

remnant of the apical sucker in juvenile cestodes of the

family Catenotaeniidae (see Wolfgang, 1956; Quen-

tin, 1994). Joyeux & Baer (1945) have demonstrated

that the apical sucker is functional in metacestodes of

Catenotaenia pusilla (Goeze, 1782) but degenerates in

adult specimens. The remnant of the apical sucker in

M. numida n. sp. appears as an evertible apical

depression clearly observed in the scolex of immature

cestodes (Fig. 2). The apical sucker allows the

attachment of cestode to the internal membrane of

the host intestine in the early stages of development

when the suckers are not developed. In the final stage

of scolex morphogenesis, differentiation of the suck-

ers occurs and the apical sucker degenerates (Joyeux

& Baer, 1945). The apical sucker is not always

observed in species of the Catenotaeniidae and is not

considered to be of taxonomic value (Haukisalmi

et al., 2010).

Discussion

The genus Meggittina was erected for M. baeri

described from ‘‘house rat’’ and ‘‘native granary rat’’

in Zimbabwe (Lynsdale, 1953). Wertheim (1954) did

not recognise the genus and synonymised it with

Rajotaenia (Wertheim, 1954), within the subfamily

Catenotaeniinae Spassky, 1949. Wolfgang (1956)

described Catenotaenia aegyptica Wolfgang, 1956

based on material from rodents in Egypt. He consid-

ered that the subfamily Catenotaeniinae is composed

of two genera, Catenotaenia Janicki, 1904 (syn.

Meggittina) and Skrjabinotaenia Akhuman, 1946.

On the basis of the position of the genital organs,

Tenora (1959) subdivided the genus Catenotaenia into

three subgenera: Catenotaenia, Spasskijela Tenora,

1959 and Meggittina.

A

B

C

D

E

Fig. 3 Shape of the strobila of Meggittina spp. A, M. numida n.

sp.; B, M. cricetomydis; C, M. baeri; D, M. aegyptica; E, M.

gerbilli. Scale-bar: 5 mm. Redrawn after original drawings

(Global Cestode Database; http://tapewormdb.uconn.edu/)

Syst Parasitol (2014) 88:167–174 171

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172 Syst Parasitol (2014) 88:167–174

123

Genov & Tenora (1979) defined Skrjabinotaeniinae

Genov & Tenora, 1979 as a new subfamily within the

Catenotaeniidae to include a single genus, Skrjabino-

taenia, with Rajotaenia and Meggittina as synonyms.

Tenora et al. (1980) resuscitated Meggittina and

placed the species Catenotaenia aegyptica, Rajotae-

nia gerbilli and Skrjabinotaenia cricetomydis in the

latter genus. They proposed a new classification for the

Catenotaeniidae that includes the Catenotaeniinae and

the Skrjabinotaeniinae. The latter subfamily consists

of two genera, Meggittina (syn. Rajotaenia) and

Skrjabinotaenia. This classification was adopted by

Quentin (1994) and Haukisalmi et al. (2010). Phylo-

genetic analyses based on sequences of the 28S

ribosomal RNA gene of the Catenotaeniidae, support

the monophyly of the Skrjabinotaeniinae (Haukisalmi

et al., 2010).

Meggittina numida n. sp. collected in our study from

the small intestine of Meriones shawi resembles

closely M. gerbilli and M. aegyptica, which are all

parasites of African Gerbillinae, and present more

anatomical differences with M. baeri and M. criceto-

mydis, which are parasites of Murinae, Nesomyinae

and Cricetinae. Quentin (1971, 1978) suggested that

Meggittina spp. may have originated from a cateno-

taeniid parasite of Holarctic rodents. Haukisalmi et al.

(2010) supposed that the African Skrjabinotaeniinae

are derived from the Catenotaeniidae, parasites of

Murinae, and this has led to the divergence of

Skrjabinotaenia and Meggittina comprised of parasites

of Muridae, Cricetidae and Nesomydae. Characters of

M. numida n. sp., such as the bifurcal shape of the last

proglottid and the elongate strobila with more than six

proglottids, can be considered ancestral anatomic

characters as hypothesised by Quentin (1978) and

Tenora et al. (1980). Our study appears to support the

hypothesis of Quentin (1978), Tenora et al. (1980) and

Haukisalmi et al. (2010) that the divergence from the

Catenotaeniinae to the Skrjabinotaeniinae has resulted

in reduced size of the strobila, reduced number of

proglottids and transverse elongation of gravid pro-

glottids. Therefore, in relation to the classification of

the Skrjabinotaeniinae, we assume that probably M.

numida may be considered as closest to the ancestor

form of the genus Meggittina. Further phylogenetic

analyses addressing the diversity of rodent catenota-

eniids and the phylogeny of Meggittina spp. along with

their morphological evaluation, are necessary for the

construction of a taxonomic system for these cestodes.

Following the description of M. numida n. sp., we

have amended the diagnosis of the genus as defined by

Quentin (1994) as follows.

Meggittina Lynsdale, 1953

Diagnosis

Skrjabinotaeniinae. Strobila acraspedote, consisting of

small scolex, wide neck and 1–25 proglottids. Genital

pores alternating regularly or irregularly. Gravid

proglottid transversely elongated, deeply cut posteri-

orly by a longitudinal fissure to form two lateral wings.

Ovary branched, poral. Vitelline gland poral. Cirrus-

sac shorter than vagina. Testes numerous, in two

lateral groups or in two groups anterior to female

organs. Median longitudinal stem of uterus very short,

lateral uterine branches not numerous, each with

secondary branches from their inner sides. Parasites of

African and Malagasy Muridae, Nesomyidae and

Cricetidae. Type-species: M. baeri Lynsdale, 1953.

Acknowledgement We would like to thank Professor Serge

Morand from CNRS Institute des Sciences de l’Evolution,

Montpellier 2 University, for his helpful comments. We are also

grateful to the anonymous reviewers for their constructive

comments on the manuscript. This work was partially funded by

the National Science Foundation, USA (PBI grants DEB

0818696 and 0818823 coordinated by J. Caira, University of

Connecticut).

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