corallobothrium solidum (cestoda: proteocephalidea) and...

REDESCRIPTION OF CORALLOBOTHRIUM SOLIDUM (CESTODA: PROTEOCEPHALIDEA)

AND ERECTION OF A NEW GENUS, ESSEXIELLA, FOR TAPEWORMS FROM CHANNEL

CATFISHES (ICTALURIDAE)

Tomas Scholz, Alain de Chambrier*, Jean Mariaux*, and Roman KuchtaInstitute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branisovska 31, 370 05 Ceske Budejovice,Czech Republic. e-mail: [email protected]

ABSTRACT: The proteocephalidean tapeworm, Corallobothrium solidum, type species of the genus, is redescribed on the basis ofthe examination of its type specimens and extensive material recently collected from Malapterurus electricus (type host). Somemorphological characteristics of taxonomic importance are reported for the first time, such as the presence of semispherical (U-shaped)sphincters on the external (outer) margin of the suckers, a vaginal sphincter, a well-developed seminal receptacle, and a uniquemorphology of the eggs. Corallobothrium solidum differs from the 2 remaining species of the genus, both parasitic in channel catfishes(Ictaluridae), in its scolex shape, morphology of its suckers, presence of longitudinal and transverse grooves on the body surface, densenetwork of excretory canals in the apical part of the scolex, morphology of the eggs, and uterine development. The non-monophyleticnature of Corallobothrium is further supported by molecular data (partial sequences of the 28S rRNA gene) because C. solidum and the2 remaining species from ictalurids do not form a monophyletic assemblage. Therefore, Essexiella n. gen. is proposed to accommodateEssexiella fimbriatum new comb. (type and only species; syn. Corallobothrium fimbriatum) from channel catfish. Essexiella n. gen.differs from Corallobothrium, Megathylacoides, and Megathylacus by the absence of a sphincter in the suckers, from Corallotaenia bythe shape of the scolex and the number and shape of proglottids, and from Paraproteocephalus by the structure of the uterus. Thediagnosis of Corallobothrium, which becomes monotypic and restricted to electric catfishes in Africa, is emended. The remainingspecies of Corallobothrium, Corallobothrium parafimbriatum, is tentatively transferred to Corallotaenia as Corallotaenia parafimbriatan. comb., based on molecular data, small size of the strobila, and shape of the scolex.

The cestode fauna of freshwater fishes in Africa is relatively

species poor and includes, besides species of other groups, 19

species of proteocephalideans (Khalil and Polling, 1997; de

Chambrier et al., 2009). Two species, Electrotaenia malopteruri

(Fritsch, 1886) and Corallobothrium solidum Fritsch, 1886,

parasitize the electric catfish, Malapterurus electricus (Gmelin)

(Khalil, 1971; Khalil and Polling, 1997; de Chambrier, Scholz,

and Ibraheem, 2004). Brunanska et al. (2004, 2005) provided data

on spermiogenesis and the ultrastructure of spermatozoa of the

latter species, which is the type species of Corallobothrium Fritsch,

1886 (Proteocephalidae: Corallobothriinae), but only limited

information exists on its general morphology.

The original description of C. solidum, which is based on poorly

preserved and fragmented material, is incomplete, and almost

no additional morphological data (illustrations, measurements,

photomicrographs) have been provided by subsequent authors

(Fuhrmann, 1916; Janicki, 1928; Khalil, 1963; Freze, 1965;

Ibraheem, 1998). A study of specimens of C. solidum collected

from the type host, the electric catfish, in Egypt (type locality)

and 4 additional African countries made it possible to provide

previously unreported morphological data and to discuss the

species composition of the genus. Scanning electron microscopical

(SEM) observations also enabled us to provide the first detailed

information on scolex morphology and surface structures.

Besides C. solidum, Corallobothrium currently includes 2

additional species, namely, Corallobothrium fimbriatum Essex,

1928, and Corallobothrium parafimbriatum Befus and Freeman,

1973, both from channel catfishes (Ictaluridae) in North America

(Schmidt, 1986). The Corallobothriinae Freze, 1965 is com-

posed of 5 genera (Corallobothrium; Corallotaenia Freze, 1965;

Megathylacoides Jones, Kerly, and Sneed, 1956; Megathylacus

Woodland, 1934; and Paraproteocephalus Chen, 1962), but

molecular data indicate that the subfamily may be paraphyletic

or polyphyletic with Megathylacus, which includes species

parasitic in catfishes in South America, being apparently unrelated

to the remaining genera (de Chambrier, Zehnder et al., 2004;

Hypsa et al., 2005).

MATERIALS AND METHODS

The following material of corallobothriine cestodes was examined: (1)C. solidum Fritsch, 1886, all from M. electricus—syntypes (5 whole-mounts with fragments of mature specimens, including 2 scoleces; 3 slideswith longitudinal sections, and 3 slides with cross sections) from the NileRiver in Egypt (exact locality not specified), deposited in the NaturalHistory Museum in Geneva (MHNG INVE 36374); vouchers (whole-mount of 1 mature specimen) from the Nile River in Khartoum, Sudan,collected by L. Khalil (MHNG INVE 34803; see Khalil, 1963); vouchers(whole-mounts of 7 mature specimens, 8 slides with cross sections ofproglottids, and 4 slides with longitudinal sections of the scolex) from theNile River in Luxor, Egypt (25u419N; 39u399W), collected by A. deChambrier in 2001 (MHNG INVE 31550, 32761–32763); vouchers (whole-mounts of 3 mature and 5 juvenile specimens, and 1 slide with crosssections) from the Nile River in El Minia, Egypt, collected by M.Ibraheem in 2002 (MHNG INVE 33997 and 36043); vouchers (whole-mounts of 8 specimens) from the Nile River in Khartoum and Omdurman,White Nile River in Kostı, Sudan, all collected by A. de Chambrier and T.Scholz in 2006 and M. Jirku in 2010, and from Al Kawa, Sudan, collectedby Z. N. Mahmoud in 2008 (MHNG INVE 63109–63111, 63197;helminthological collection of the Institute of Parasitology, CeskeBudejovice, Czech Republic, IPCAS C-507; The Natural HistoryMuseum, London, U.K., BMNH 2011.2.10.1; U.S. National ParasiteCollection, Beltsville, Maryland, USNPC 104286); vouchers (whole-mounts of 2 mature specimens) from Turkana Lake, Kenya, collectedby M. Jirku in 2009 (MHNG INVE 75469); vouchers (whole-mounts of 8mature specimens) from the Senegal River in Richard Toll, Dagana,Senegal (16u299N; 15u369W), collected by A. Sene (date not given; MHNGINVE 37857–37859); vouchers (whole-mounts of 3 mature specimens)from the Kwilu River in Bagata, Zaire (now Democratic Republic of theCongo; 4u499S; 18u469E), collected by A. Fain (date not given; MHNGINVE 55307); (2) Corallobothrium cf. solidum Fritsch, 1886—vouchers(whole-mounts of 6 mature specimens and 10 slides with cross sections)from Malapterurus gossei Norris, lower Congo River at Pioka, Demo-cratic Republic of the Congo, collected by M. Jirku in 2008 (MHNG

Received 26 November 2010; revised 14 June 2011; accepted 30 June2011.

* Department of Invertebrates, Natural History Museum, P.O. Box 6434,CH-1211 Geneva 6, Switzerland.DOI: 10.1645/GE-2705.1

J. Parasitol., 97(6), 2011, pp. 1142–1151

F American Society of Parasitologists 2011

1142

INVE 63117); (3) Corallobothrium cf. fimbriatum Essex, 1928—vouchers(whole-mounts of 6 mature specimens and 4 slides with cross sections)from Ictalurus balsanus (Jordan and Snyder), Chontalcoatlan, Guerrero,Mexico, collected by J. M. Caspeta-Mandujano in 1997 (MHNG INVE32945); vouchers (3 whole-mounts of juvenile specimens) from Ictaluruspunctatus (Jordan and Snyder), Reelfoot Lake, Tennessee, collected by V.Tkach in 2002 (MHNG INVE 35380–35382), and from Clinton Lake,Kansas, and Knoxville, Tennessee (7 whole-mounted specimens), collectedby R. Kuchta in 2009 (MHNG INVE 75464); (4) C. parafimbriatum Befusand Freeman, 1973—vouchers (7 whole-mounted specimens) fromAmeiurus melas (Rafinesque), Ferrara, Italy, collected by H. Cappellaroin 1989 (IPCAS C-234); voucher (1 whole-mounted specimen) from A.melas, La Seymaz, Geneva, Switzerland, collected by C. Vaucher in 2002(MHNG INVE 32944); (5) Megathylacoides giganteum (Essex, 1928)Freze, 1965—vouchers (5 whole-mounted immature specimens) from I.punctatus, Reelfoot Lake, Tennessee, collected by V. Tkach in 2002(MHNG INVE 35373, 35377, 35383, 35384), and Clinton Lake, Kansas,and Knoxville, Tennessee, collected by R. Kuchta in 2009 (3 whole-mounted specimens and 30 slides of cross sections) (MNHG 75435, 75438,75439); (6) Megathylacoides lamothei (Garcıa-Prieto, 1990) Scholz, Rosas,Perez-Ponce de Leon, Choudhury, and de Chambrier, 2003—voucher(whole-mount of several gravid proglottids and 8 slides of cross sections)from I. balsanus, Mexico, collected by A. A. Rego (date not given; MHNGINVE 34867).

Tapeworms recently collected in Egypt, Kenya, the Sudan, and UnitedStates (most from live or fresh fish) were fixed in hot 4% neutralformaldehyde solution (with pieces of several worms placed in 99%molecular grade ethanol for DNA analysis) and then processed asdescribed elsewhere (e.g., de Chambrier et al., 2009; Oros et al., 2010). Allmeasurements are given in micrometers unless otherwise indicated.Abbreviations used in descriptions are as follows: x 5 mean, n 5 numberof measurements, CV 5 coefficient of variability (x/SD 3 100 [in %]).

For molecular analysis, DNA was extracted with a DNeasy Tissue kitE(Qiagen, Hilden, Germany) according to manufacturer instructions; PCRamplification of a 59 portion of the 28SrDNA molecule and its purificationwere conducted as previously described in Zehnder and Mariaux (1999).Sequencing was performed on an Applied Biosystems 3730xl (AppliedBiosystems, Foster City, California) through MacrogenTM (Korea). Thenew sequence (Corallobothrium cf. solidum from Congo) reported here isdeposited with Genbank under accession number JN005780.

Sequences of species of 4 genera of the Corallobothriinae (see Fig. 28for accession numbers) were compared. Since Megathylacus, whichincludes species parasitic in siluriform catfish in South America, isapparently unrelated to the 4 remaining genera of the Corallobothriinae(see de Chambrier, Zehnder et al., 2004; Hypsa et al., 2005), it was notincluded in analyses. Sequences were aligned directly with SequencherTM

v 4.1.2 (proprietary algorithm, GeneCodes Corp., Ann Arbor, Michigan),with minor corrections made by hand. Both parsimony (branch andbound option) and maximum likelihood phylogenetic analyses wereconducted using PAUP* v. 4.0b.10 (Swofford, 2002). The ML model wasselected using jModeltest v. 0.1.1 under standard AIC criterion (Guindonand Gascuel, 2003; Posada, 2008). Nodal support was estimated byperforming a parsimony bootstrap analysis (with 1,000 pseudoreplicates)and a ML bootstrap analysis (with 100 pseudoreplicates).

RESULTS

Redescription of Corallobothrium solidum Fritsch, 1886(Figs. 1–16, 19–27)

Redescription (based on 16 newly collected specimens from M.

electricus from Egypt and the Sudan; type specimens are strongly

contracted and thus their measurements could not be taken):

Proteocephalidae, Corallobothriinae. Testes, ovary, vitelline

follicles, and uterus medullary (Figs. 12–14). Strobila 38–57 mm

long and 1.7–2.6 mm wide, massive, acraspedote, covered with

papilliform filitriches, consisting of 92–116 proglottids: 61–71

immature, 11–17 mature, and 20–28 pregravid and gravid. Body

surface with deep longitudinal and transverse grooves (wrinkles)

forming rectangular network (Fig. 25).

Internal longitudinal musculature weakly developed, formed by

narrow band of isolated muscle fibers, more dense on lateral sides of

strobila (Figs. 12, 13). Osmoregulatory canals well developed, thin-

walled, forming dense network of thin canals in scolex (Figs. 4–6).

Foramina secundaria described by Janicki (1928) not observed in cross

sections (Figs. 12–14). Ventral canals lateroventral to testes; dorsal

canals dorsal to vitelline follicles and dorsolateral to testes. Dorsal

canals situated more laterally than ventral ones (Figs. 8, 12, 13).

Scolex large, 1,060–1,660 (x 5 1345; n 5 8) long by 2,260–3,230 (x

5 2,655, n 5 8) wide, with well-developed metascolex, much wider

than proliferative zone (neck) (Figs. 1, 2, 19–21). Scolex umbrella-

shaped, with widely pyramidal apex and well-developed metascolex,

which forms folded collar surrounding suckers (Figs. 1, 19–21).

Scolex wider laterally than dorsoventrally (Figs. 20, 23). Suckers

large, uniloculate, deeply embedded, 450–595 (x 5 510, n 5 20) long

by 325–455 wide (x 5 395, n 5 20) (Figs. 4–6, 19–23); external (outer)

margins of suckers with semispherical (U-shaped, i.e., interrupted

anteriorly) musculature serving as sphincter (Figs. 1–3, 5, 6). Sucker

cavity covered with thin valve-like structure (velum) with slit-like

opening (Figs. 1, 3, 19, 22, 23). Proliferation zone 895–1,365 wide.

Testes medullary, spherical to oval, 40–70 in diameter, 224–281

in number (x 5 244, n 5 5, CV 5 11%), in 2 irregular (incomplete)

layers (Figs. 8, 11–13), in 2 lateral fields connected anteriorly

(Fig. 8). External sperm duct (vas deferens) winding, reaching to

median line of body (Figs. 8, 10). Cirrus-sac gradually narrowing

to distal end, thick-walled proximally (Fig. 15), 240–450 long by

95–200 wide, representing about 16–24% of proglottid width (x 5

20%, n 5 22, CV 5 11%). Internal sperm duct thick-walled,

forming several loops in proximal third or half of cirrus-sac. Cirrus

straight, long, about 2/3 of cirrus-sac length. Genital pores

irregularly alternating, close to anterior margin of proglottids,

situated at 19–36% (n 5 25; CV 5 17%) of proglottid length from

anterior end. Genital atrium deep (Fig. 15), 55–250 in depth.

Ovary medullary, compact, with small follicles on surface

(Figs. 8, 11), bilobed, with short and wide lateral lobes connected

by ventrally situated isthmus (Figs. 8–11). Length of ovary 215–

440; total width of ovary 545–830, representing 40–52% (n 5 25,

CV 5 8%) of proglottid width. Mehlis’ glands slightly posterior to

ovarian isthmus, about 70–110 in diameter, representing 4–6% of

proglottid width (Figs. 8–10).

Vaginal canal narrow, almost straight or slightly sinuous, thick-

walled and lined with chromophilic cells, usually posterior to

cirrus-sac (80%, n 5 257). Terminal (distal) part of vaginal canal

with small vaginal sphincter near genital atrium, formed by

diffuse muscle fibers (Fig. 15). Seminal receptacle small, dorsal to

ovarian isthmus (Fig. 11), observed also in type material.

Vitelline follicles medullary, small, arranged in 2 narrow lateral

bands starting at distance from anterior margin of proglottid

(Figs. 8–10), widened posteriorly and bent inward near posterior

margin of proglottid (parallel to posterior edge of proglottid),

usually reaching medially to ovarian lobes (Figs. 8–10). Total

length of bands of follicles represents 66–86% (poral) and 75–95%

(aporal) of proglottid length. Poral band interrupted ventrally

(Fig. 8), with follicles dorsal to cirrus-sac (Figs. 9, 15).

Uterus medullary, type 1 development (de Chambrier, Zehnder

et al., 2004): uterine stem with numerous intensely-staining cells

concentrated along its wall in immature proglottids. Uterine lumen

appears in last immature proglottids simultaneously with dorsolateral

outgrowths (diverticula); lateral branches (diverticula) asymmetrical,

occupying up to 71% of width of gravid proglottids (Fig. 9).

SCHOLZ ET AL.—ESSEXIELLA N. GEN. 1143

FIGURES 1–11. Corallobothrium solidum Fritsch, 1886, from Malapterurus electricus. (1, 2) Dorsoventral view of scolex (1, MHNG INVE 31550;2, MHNG INVE 31554), Egypt. (3) Detail of sucker showing the sphincter (MHNG INVE 63109), Egypt. (4–6) Sagittal sections of scolex (MHNG INVE32761), Egypt. Note the dense network of osmoregulatory canals in the apical region. (7) Scolex of juvenile specimen (MHNG INVE 33997), Egypt. (8) Matureproglottid, ventral view (MHNG INVE 32762), Egypt. (9) Gravid proglottid, testes omitted, dorsal view (MHNG INVE 63197), Sudan. (10) Pregravidproglottid, with cirrus everted, dorsal view (MHNG INVE 31554). (11) Detail of the posterior region of a pregravid proglottid, dorsal view (MHNG INVE31554), Egypt. Abbreviations: ad, additional opening; ao, apical organ; mg, Mehlis’ gland; ms, metascolex; oc, osmoregulatory canals; ov, ovary; sp, circularmusculature serving as sphincter; sr, seminal receptacle. Scale bars: 1, 11 5 200 mm; 2 5 1,000 mm; 3, 7 5 100 mm; 4–6, 9–10 5 500 mm; 8 5 300 mm.

1144 THE JOURNAL OF PARASITOLOGY, VOL. 97, NO. 6, DECEMBER 2011

Eggs spherical, with hyaline outer membrane 95–100 in

diameter (collapsed in permanent mounts) and spherical,

bilayered embryophore, with outer layer 23–27 in diameter,

denser than inner nuclei-containing layer. Tubercle-like projec-

tions (outgrowths) on 1 pole of embryophore (Fig. 16). Onco-

spheres spherical to oval, 13–15 long by 12–14 wide, with 3 pairs

of embryonic hooks 5–6 long.

Taxonomic summary

Type host: Malapterurus electricus (Gmelin, 1789) (Siluri-

formes: Malapteruridae).

Type locality: Nile River in Egypt (exact locality not specified).

Type specimens: MHNG INVE 36374.

Additional host: Malapterurus gossei Norris, 2002 (but see

Discussion).

Site of infection: Intestine.

Prevalence: In Luxor, Egypt, prevalence 5 100% (n 5 2), mean

intensity of infection 38 (range 11–64); in Khartoum, Sudan, 75%

(n 5 12), 3.7 (range 1–10); Omdurman, Sudan, 67% (n 5 6), 3.3

(1–8); Kostı, Sudan, 67% (n 5 3), 4.0 (4).

Distribution: Basins of the Nile (Egypt, Sudan), Congo

(Democratic Republic of the Congo), and Omo (Turkana Lake,

Kenya) rivers, Senegal (last 3 localities represent new zoogeo-

graphical records).

FIGURES 12–18. (12–16) Corallobothrium solidum Fritsch, 1886 from Malapterurus electricus. (12–14) Cross sections of pregravid proglottid at level ofanterior, middle, and posterior part, respectively (MHNG INVE 32762 and 32763), Egypt. (15) Terminal genitalia, dorsal view (MHNG INVE 63197),Sudan. (16) Eggs in distilled water (MHNG INVE 48053), Sudan. (17) Megathylacoides giganteum (Essex, 1928) from Ictalurus punctatus. Eggs in distilledwater, with collapsed outer hyaline envelope (MHNG INVE 75439). (18) Corallobothrium fimbriatum Essex, 1928 (5 Essexiella fimbriata), from I.punctatus. Eggs in distilled water, with collapsed outer hyaline envelope (MHNG INVE 75464) Abbreviations: cs, cirrus-sac; doc, dorsal osmoregulatorycanal; em, bilayered embryophore; ga, genital atrium; ilm, longitudinal internal musculature; oe, outer envelope; on, oncospheres; ov, ovary; te, testes; tp,tubercule-like projections; ut, uterus; va, vagina; vd, vas deferens; vf, vitelline follicles; voc, ventral osmoregulatory canal; vs, vaginal sphincter. Scale bars:12–14 5 500 mm; 15 5 100 mm; 16–18 5 20 mm.


FIGURES 19–27. Scanning electron micrographs. 19–22, 25–27. Corallobothrium solidum Fritsch, 1886 from Malapterurus electricus, Egypt (19–21)Dorsoventral, apical, and lateral view, respectively (MHNG INVE 32762). (22) Detail of suckers (MHNG INVE 32763). (23, 24) Apical view of scolexand detail of the apical region, respectively. (25) C. solidum from M. electricus, Egypt (MHNG INVE 32762). Longitudinal and transverse grooves on thestrobila. (26, 27) Papilliform filitriches on suckers and apex of the scolex, respectively (MHNG INVE 32763). 23, 24. Corallobothrium cf. solidum Fritsch,1886, from Malapterurus gossei, Democratic Republic of the Congo (MHNG INVE 63057). Scale bars: 19–21, 25 5 200 mm; 22 5 100 mm; 24 5 150 mm;26, 27 5 2 mm.


Remarks

The original description of C. solidum by Fritsch (1886) was

very brief; only 2 measurements (total length and maximum width

of the body), a sketch of the whole worm, and figures of sections

of an apparently contracted specimen were provided (Fritsch,

1886). Fuhrmann (1916), who studied Fritsch’s original material

(currently deposited in MHNG, but of very poor quality due to

strong contraction of the worms), provided additional data on the

scolex, proglottids, and genital organs, including the number of

testes (140–180). However, he erroneously reported as many as

50–60 lateral branches of the uterus (10–12 branches in 3–5

layers), which was not confirmed by a study of type material, and

mentioned the absence of a seminal receptacle in C. solidum,

which is in fact present (Fig. 11).

Janicki (1928) described a dense network of excretory canals on

the ventral side of the strobila (fig. 25 in his paper), but this

network and foramina secundaria were not observed in cross

sections of the new material. In contrast, we confirm the presence

of numerous longitudinal and transverse grooves on the body

surface (compare Fig. 25 in the present paper with figs. 22 and 24

in Janicki, 1928), and the shape of the bands of vitelline follicles,

which bent inward (medially) near the posterior margin of

proglottids (Figs. 8–10).

Some previously unreported morphological characteristics were

observed in the present study. The most important feature is the

presence of a well-developed, semi-circular (U-shaped) muscula-

ture on the anterior margin of suckers, which forms a large

sphincter interrupted anteriorly (Figs. 2, 3). Such a sphincter has

been found in some other proteocephalidean genera, including

species of the corallobothriine Megathylacoides Jones, Kerly, and

Sneed, 1956, from North American ictalurid catfish (Freze, 1965;

Rego, 1994), but also in Barsonella de Chambrier, Scholz,

Beletew, and Mariaux, 2009, from Clarias catfish in Africa (de

Chambrier et al., 2009). In contrast, sphincters are absent on the

suckers of both remaining species of Corallobothrium, C.

fimbriatum and C. parafimbriatum, both from channel catfish

(Ictaluridae) (Essex, 1928; Freze, 1965; Befus and Freeman, 1973;

present study).

FIGURE 28. Phylogram (maximum likelihood—ML) showing the relationships of 13 corallobothriine tapeworms inferred from partial sequences ofthe 28S rRNA gene. The same topology is obtained from a parsimony analysis. Parsimony bootstrap values are above the nodes and ML ones belowthe nodes.


Another character of C. solidum reported here for the first

time is a unique egg morphology. The embryophore of the eggs

possesses tubercle-like projections (outgrowths) (Fig. 16). These

projections have not been observed on the eggs of species of

Corallobothrium and Megathylacoides from ictalurids (Figs. 17,

18; see also Essex, 1928; Befus and Freeman, 1973) or those of

other proteocephalidean cestodes (Freze, 1965; Scholz, 1999).

Other characteristics of C. solidum, which were unreported

previously, are the presence of a well-developed seminal receptacle

(observed also in type material) and a vaginal sphincter (Figs. 11,

15). However, the former structure serving for storage of sperm is

probably present in all proteocephalidean cestodes, yet difficult

to observe in some species, and the presence of the sphincter

surrounding the distal end of the vaginal canal is also common

(Freze, 1965; de Chambrier and Vaucher, 1999).

Another feature typical of C. solidum is a concentration of

muscle fibers of the inner longitudinal musculature on the lateral

sides of the strobila (Figs. 12–14). Such a feature is uncommon in

proteocephalidean cestodes and has been reported for a few

species only, such as those of Amphoteromorphus Diesing, 1850

(see Carfora et al., 2003).

New, well-fixed material of C. solidum also enabled us to better

describe the shape of the scolex. SEM observations have shown

that it is in fact markedly different (asymmetrical in apical view,

i.e., wider laterally than dorsoventrally; Fig. 20) from that de-

scribed by previous authors, who apparently studied contracted

specimens (see fig. 2 in Fritsch, 1886, and fig. 22 in Janicki, 1928).

Juvenile specimens possess a large apical organ, spherical to

widely oval in shape (Fig. 7), 190–285 long by 150–300 wide, but

their metascolex is weakly developed (Fig. 7).

Neither of the 2 species from ictalurid catfish, that is C.

fimbriatum and C. parafimbriatum, possess the following charac-

teristics observed in C. solidum: a sphincter on the suckers,

tubercle-like projections on the embryophore of the eggs (see

Figs. 17, 18), longitudinal and transverse wrinkles on the strobilar

surface, and type 1 development of the uterus (Essex, 1928; Befus

and Freeman, 1973; present study).

These conspicuous morphological differences cast doubts upon

the current species composition of the genus Corallobothrium as a

natural, monophyletic assemblage. The genus is also heteroge-

neous when considering its spectrum of definitive hosts (ictalurids

vs. malapterurids) and its markedly disjunct geographical distri-

bution (North America vs. Africa).

Molecular analysis

The phylogenetic relationships of all 12 available sequences of

corallobothriine cestodes (11 published, 1 new; the sequence of

Megathylacus jandia Woodland, 1934 was not included because

this species was found to be unrelated with the remaining

corallobothriines—see de Chambrier, Zehnder et al., 2004) were

analyzed using both parsimony and maximum likelihood methods

applied to about 1 kb of the 59 end of the 28Sr RNA gene.

Paraproteocephalus parasiluri (Zmeev, 1936) was chosen as a

functional outgroup. The alignment obtained was 1,022 bp long,

including 49 gaps, and comprised 84 parsimony informative

positions. The shortest parsimony tree (uninformative positions

excluded) has a length of 123 (CI 5 0.64, RI 5 0.83). Treating the

gaps as a fifth character did not change the tree topology. The

best-fit model selected by AIC in jModeltest is TPM3uf+G with

the following parameters: Lset base 5 (0.1939, 0.2202, 0.3400,

0.2459); nst 5 6; rmat 5 (0.3707, 5.9067, 1.0000, 0.3707, 5.9067,

1.0000); rates 5 gamma; shape 5 0.1590; ncat 5 4; pinvar 5 0.

The best ML tree under these conditions has a 2ln likelihood of

2524.9436 and the same topology as the parsimony tree (Fig. 28).

Samples of C. solidum and C. cf. solidum from Congo are sister

taxa and basal. The other taxa group in 2 clades. The first is

composed of the Megathylacoides samples (M. giganteum and M.

lamothei) and shows a possibly paraphyletic M. giganteum (as in

Rosas-Valdez et al., 2004; with addition of 2 new sequences, the

same data were used in the present analysis). The second comprises

C. fimbriatum, C. parafimbriatum, and 2 species of Corallotaenia

Freze, 1965 [Corallotaenia intermedia (Fritts, 1959) Freze, 1965, and

Corallotaenia minuta (Fritts, 1959) Freze, 1965], with C. parafim-

briatum as sister taxon to both Corallotaenia species (Fig. 28).

Species composition of Corallobothrium

Based on the above mentioned morphological, bionomical

(spectrum of definitive hosts and geographical distribution), and

molecular data, species of Corallobothrium are newly placed in 2

genera. The former, Corallobothrium, now includes only a single

species, C. solidum, parasitic in African electric catfish (Malapter-

urus spp.), whereas a new genus is proposed to accommodate C.

fimbriatum from channel catfish (Ictaluridae) occurring originally

in North America.

Essexiella new genus

Diagnosis: Proteocephalidea, Proteocephalidae, Corallobothrii-

nae. Large tapeworms, with massive strobila and well-developed

inner longitudinal musculature. Testes, ovary, vitelline follicles,

and uterus medullary. Main osmoregulatory canals thin-walled,

dorsal canals situated more laterally than ventral ones. Scolex

large, with metascolex, edge curving forward and apex elongated

or evaginated. Suckers deeply embedded, oval, without sphincter.

Testes in 1 field, in 1 to 3 layers. Cirrus-sac elongate to oval.

Genital pores irregularly alternating, situated pre-equatorial.

Ovary bilobed, its width representing less than 50% of proglottis

width. Vagina posterior or anterior to cirrus-sac. Seminal

receptacle present. Vitelline follicles arranged in 2 lateral bands,

with posterior follicles turning medially, reaching ovarian lobes.

Uterine development of type 2 according to de Chambrier,

Zehnder et al. (2004). Eggs spherical, with smooth embryophore.

Parasites of channel catfish (Ictaluridae), originally in North

America. Type and only species: Essexiella fimbriata (Essex, 1928)

new. comb.

Etymology: The generic name commemorates the contribution

of Hiram E. Essex to the systematics of fish cestodes, especially

his monograph on Corallobothrium from North America (Essex,

1928); the name should be treated as a feminine.

Differential diagnosis

The new genus is placed in the Corallobothriinae sensu Rego

(1994) because genital organs (testes, ovary, vitelline follicles, and

uterus) are situated in the medulla and a metascolex is present

(Freze, 1965; Rego, 1994). Essexiella differs from the remaining 5

genera of the Corallobothriinae, i.e., Corallobothrium, Corallo-

taenia, Megathylacoides, Megathylacus Woodland, 1934, and

Paraproteocephalus Chen, 1962, as follows:


(1) Corallobothrium possesses a U-shaped sphincter on the

external (outer) margin of suckers, tubercle-like projections

on the embryophore, and a network of osmoregulatory

canals in the scolex (all structures absent in Essexiella); it

also differs by the type of uterine development (type 1) and

testes arranged in 2 separate fields confluent anteriorly (in 1

field in Essexiella).(2) Corallotaenia can be distinguished from Essexiella by the

small size of its body, which consists of only a few pro-

glottids, with mature ones being longer than wide (much

wider than long in Essexiella), and a weakly developed

metascolex formed by a few lobes in the posterior part of

otherwise globular scolex (see Rosas-Valdez et al., 2004)

(Jones et al., 1956; Freze, 1965).(3) Megathylacoides differs by the presence of a sphincter in

suckers (absent in Essexiella) and by a different shape of the

scolex, with a less developed metascolex (see Scholz et al.,

2003; Rosas-Valdez et al., 2004).(4) Megathylacus possesses sphincters in the suckers (absent in

Essexiella), the scolex is of a markedly different shape (see

Freze, 1965; Rego, 1994), and the species possesses a type 1

development of the uterus (de Chambrier, Zehnder et al.,

2004).(5) Paraproteocephalus is conspicuously different from Essex-

iella in its unique morphology of the uterus, which forms

external branches (diverticula) in the vertical direction (see

Yamaguti, 1934; Freze, 1965; Rego, 1994) (the uterus of

Essexiella has lateral diverticula as in all other proteoce-

phalideans); it also differs in the shape of the scolex, which

is discoidal and possesses anteriorly situated suckers and an

apical sucker (Rego, 1994).

Phylogenetic relationships

Molecular data demonstrated that C. solidum and the 2

remaining species previously placed in Corallobothrium, i.e., C.

fimbriatum and C. parafimbriatum, are unrelated and should not

be placed in the same genus (Fig. 28). However, this analysis has

also indicated that the species composition of North American

corallobothriine genera may not reflect their phylogenetic

relationships, because C. parafimbriatum did not form a

monophyletic clade with C. fimbriatum, but represented a sister

taxon to both species of Corallotaenia (C. intermedia and C.

minuta, the latter being synonymized by Freze [1965] with the

former) (Fig. 28).

In some morphological characteristics, such as small size of the

body and the shape of the scolex, C. parafimbriatum resembles

species of Corallotaenia (see Freze, 1965; Befus and Freeman,

1973). Based on this morphological resemblance between C.

parafimbriatum and Corallotaenia spp., and new molecular data,

the former species is tentatively placed in Corallotaenia as

Corallotaenia parafimbriata n. comb., but further studies should

confirm this generic placement.

Molecular data also indicate that M. giganteum, type species of

the genus, may represent a complex of cryptic species, some of

them being unrelated to each other (Rosas-Valdez et al., 2004). It

is evident that the whole group of proteocephalidean cestodes

parasitic in ictalurids, including Corallotaenia, Essexiella, and

Megathylacoides, is pending taxonomic revision, which should

include morphological and molecular data.

Corallobothrium Fritsch, 1886—emended diagnosis

Diagnosis: Proteocephalidea, Proteocephalidae, Corallobothrii-

nae. Testes, ovary, vitelline follicles, and uterus medullary. Large

tapeworms, with massive strobila and well-developed inner

longitudinal musculature with muscle fibers concentrated on

lateral sides of strobila. Body surface with longitudinal and

transverse grooves. Main osmoregulatory canals thin-walled,

ventral canals overlapping testicular field. Scolex large, with

metascolex, wider laterally than dorsoventrally. Suckers deeply

embedded, oval, external (outer) margin of suckers with well-

developed semi-circular (U-shaped) musculature serving as

sphincter. Testes in 2 fields confluent anteriorly, in 1 complete

or 2 incomplete layers. Cirrus-sac oval. Genital pores irregularly

alternating, pre-equatorial. Genital atrium deep. Ovary bilobed,

its width occupies more than 50% of proglottis width. Vagina

usually posterior to cirrus-sac. Seminal receptacle present.

Vitelline follicles arranged in 2 lateral bands, with posterior

follicles turning medially, reaching ovarian lobes. Uterine

development of type 1 according to de Chambrier, Zehnder et al.

(2004). Eggs with tubercle-like projections on embryophore.

Parasites of electric catfishes (Malapteruridae) in Africa. Type

and only species: C. solidum Fritsch, 1886.

DISCUSSION

As many as 11 species of proteocephalidean cestodes possessing

a metascolex have been placed in Corallobothrium Fritsch, 1886

(see Freze [1965] for overview of the taxonomic history of the

genus). However, only 3 species, namely C. solidum, C. fimbriatum,

and C. parafimbriatum, were retained in the genus more recently

(Schmidt, 1986). Based on the present study, the genus should be

considered to be monotypic, with its single species specific to

electric catfishes in Africa, whereas the 2 species from ictalurids are

accommodated in newly proposed genera, Essexialla and Corallo-

taenia, respectively. These 2 latter species were originally described

from North America (Essex, 1928; Befus and Freeman, 1973), but

they may occur outside of North America as a result of the import

of channel catfishes to other continents, especially to Europe

(Scholz and Cappellaro, 1993; C. Vaucher, unpubl. data; MHNG

INVE 32944).

A study of the type material and newly collected specimens of

C. solidum has revealed some morphological characteristics of

taxonomic importance, which were previously unreported. The

most important novelty is the presence of muscular sphincters in

suckers and tubercle-like projections on the outer layer of the

embryophore of the eggs. The presence/absence of a sphincter in

suckers is considered to be a taxonomically important character

that is suitable for differentiation of genera of proteocephalidean

cestodes (Jones et al., 1956; Freze, 1965; Rego, 1994; de

Chambrier and Rego, 1995; de Chambrier and Vaucher, 1999,

de Chambrier et al., 2009). Egg morphology is also considered to

represent a taxonomic character suitable for differentiation of

species (Gil de Pertierra and de Chambrier, 2000; Carfora et al.,

2003; de Chambrier et al., 2007, 2009, 2010; Scholz et al., 2009).

Presence of a dense network of osmoregulatory canals within

the scolex is an unusual observation for the Proteocephalidea,

although it was already reported for Proteocephalus torulosus

(Batsch, 1786), a parasite of cyprinids in the Holarctic, by Wagner

(1917), for M. lamothei (Garcia-Prieto, 1990), a parasite of

(1)


Ictalurus furcatus (Siluriformes: Ictaluridae) in Mexico, by Scholz

et al. (2003), and for Brooksiella praeputialis (Rego, Santos, and

Silva, 1974), a parasite of Cetopsis coecutiens (Siluriformes:

Cetopsidae) in the Neotropical Region, by de Chambrier, Rego,

and Mariaux (2004). This structure seems to be invariable and

may represent a good discriminative character at the species level.

Corallobothrium solidum type and only species of the newly

erected Essexiella closely resemble each other in the overall shape

of the scolex with a well-developed metascolex, but molecular data

show that they are not closely related. A well-developed metascolex

of these tapeworms thus represents a homoplastic character, which

is a result of their convergent evolution. Similarly, previous

phylogenetic studies (de Chambrier, Zehnder et al., 2004; Hypsa

et al., 2005) also showed that proteocephalidean genera possessing

a metascolex did not form a monophyletic assemblage. Therefore,

the presence/absence of a metascolex should not be used as a

taxonomic character at the subfamilial or familial level. Rego

(1995) proposed a new classification of the Proteocephalidea,

which markedly differed from his classification 1 yr earlier (Rego,

1994). He newly placed as many as 16 proteocephalidean genera

within the subfamily Corallobothriinae solely on the basis of the

presence of a metascolex. Results of the present and previous

studies thus do not support Rego’s (1995) classification.

Current studies on proteocephalidean cestodes (e.g., de

Chambrier et al., 2007, 2009) have also demonstrated that

complicated 3-dimensional structures such as the metascolex of

corallobothriine and other proteocephalidean cestodes may be

difficult to correctly describe without use of scanning electron

microscopy. In addition, fixation may considerably influence the

appearance of these complicated structures, which can then lead

to incorrect taxonomic conclusions. Besides SEM observations,

longitudinal sections (frontal or sagittal) of the scolex appear

to be of great value for correct description of the internal

morphology of the scolex. This also concerns the structure of the

suckers and the apical part of the scolex, which may contain gland

cells, apical structures and/or a dense network of excretory canals

as observed in C. solidum.

In juvenile C. solidum tapeworms, the metascolex of which was

not yet fully developed, a large apical organ with granular content

was observed (Fig. 7). However, this organ, or its traces, were not

observed in any of the numerous adult tapeworms studied (Figs. 1,

2, 4–6), which indicates that this organ disappears completely

during the maturation of the worms within the definitive host. This

organ may serve as an additional attachment organ important for

firm fixation of juvenile, recently recruited tapeworms in the

intestinal lumen of the fish host, but no data are available on the

life-cycle and ontogenetic development of C. solidum to confirm

this assumption, which is based on existing information about life-

cycles of other proteocephalideans (for review, see Freze, 1965;

Scholz, 1999; Scholz and de Chambrier, 2003).

Congeneric tapeworms with a well-developed metascolex and

robust strobila were found in another electric catfish, M. gossei

Norris, from the lower Congo River in the Democratic Republic

of the Congo. They slightly differ from C. solidum in the shape of

the scolex (Figs. 23, 24) and sequences of the 28S rRNA gene

(Fig. 28). They may represent a new, yet undescribed species of

the genus, but the material available is not sufficient for a reliable

taxonomic description of the new taxon. Accordingly, Corallobo-

thrium is tentatively considered to be a monotypic genus, specific

to electric catfish (Malapterurus spp.) in Africa.

ACKNOWLEDGMENTS

The authors express their deep gratitude to Dr. Kirsten Jensen and 2anonymous reviewers for valuable suggestions and helpful comments; toDrs. Juan M. Caspeda-Mandujano (Cuernavaca, Mexico), Kirsten Jensen(Kansas, USA), Miloslav Jirku (IPCAS), Tom Mattis (Tennessee, USA),and Vasyl Tkach (North Dakota, USA) for providing specimens; to Dr.Zuheir N. Mahmoud, Ali Adam, and Sayed Yousif Osman Elsheikh(University of Khartoum), Khalid Bashir Abaker and Ammar Osmar(White Nile Fisheries Research Station in Kostı) for invaluable helpduring sampling trips to the Sudan; to Andre Piuz for providing SEMphotomicrographs; and to Janik Pralong, Florence Marteau, and GillesRoth (all MHNG) for their help with drawings and laboratory assistance.The support of the Embassy of Switzerland in Khartoum (AndreaReichlin) is also acknowledged. A. de C. is deeply indebted to the‘‘Donation Georges et Antoine Claraz’’ for financial support, as are R. K.and T. S. to the Grant Agency of the Czech Republic (project Nos. 524/04/0342 and 524/08/0885), Grant Agency of the Academy of Sciences ofthe Czech Republic (project No. KJB600960902), and the Institute ofParasitology (project Nos. Z60220518 and LC 522). The financial supportof the National Science Foundation, USA (PBI award Nos. 0818696 and0818823) is also greatly appreciated.

LITERATURE CITED

BEFUS, A. D. AND R. S. FREEMAN. 1973. Corallobothrium parafimbriatumsp. n. and Corallotaenia minutia (Fritts, 1959) comb. n. (Cestoda:Proteocephaloidea) from Algonquin Park, Ontario. Canadian Jour-nal of Zoology 51: 243–248.

BRUNANSKA, M., T. SCHOLZ, AND M. H. IBRAHEEM. 2004. Ultrastructuralcharacteristics of the spermatozoon of the cestode Corallobothriumsolidum Fritsch, 1886 (Proteocephalidae: Corallobothriinae), aparasite of Malapterurus electricus (Siluriformes: Malapteruridae)from the Nile, Egypt. Parasitology Research 94: 421–426.

———, ———, AND ———. 2005. Spermiogenesis in the cestodeCorallobothrium solidum Fritsch, 1886 (Proteocephalidea: Corallobo-thriinae). Acta Zoologica (Stockholm) 86: 55–61.

CARFORA, M., A. DE CHAMBRIER, AND C. VAUCHER. 2003. Le genreAmphoteromorphus (Cestoda: Proteocephalidea), parasite de poissons-chats d’Amerique tropicale: Etude morphologique et approche biosys-tematique par electrophorese des proteines. Revue Suisse de Zoologie110: 381–409.

DE CHAMBRIER, A., M. AMMANN, AND T. SCHOLZ. 2010. First Ophiotaenia(Cestoda: Proteocephalidea) from Madagascar: O. georgievi sp. n., aparasite of the endemic snake Leioheterodon geayi (Colubridae). FoliaParasitologica 57: 197–205.

———, AND A. A. REGO. 1995. Mariauxiella pimelodi n. g., n. sp.(Cestoda: Monticelliidae): A parasite of pimelodid siluroid fishesfrom South America. Systematic Parasitology 30: 57–65.

———, ———, AND J. MARIAUX. 2004. Redescription of Brooksiellapraeputialis and Goezeella siluri (Eucestoda: Proteocephalidea),parasites of Cetopsis coecutiens (Siluriformes) from the Amazonand proposition of Goezeella danbrooksi sp. n. Revue Suisse deZoologie 111: 111–120.

———, T. SCHOLZ, M. BELETEW M., AND Z. N. MAHMOUD. 2007.Redescription of Proteocephalus sulcatus (Klaptocz, 1906) (Cestoda:Proteocephalidea), a poorly known parasite of Clarotes laticeps(Pisces: Siluriformes) in Africa. Revue Suisse de Zoologie 114:693–702.

———, ———, ———, AND J. MARIAUX. 2009. A new genus and speciesof proteocephalidean (Cestoda) from Clarias catfishes (Siluriformes:Clariidae) in Africa. Journal of Parasitology 95: 160–168.

———, ———, AND M. H. IBRAHEEM. 2004. Redescription of Electro-taenia malopteruri (Fritsch, 1886) (Cestoda: Proteocephalidae), aparasite of Malapterurus electricus (Siluriformes: Malapteruridae)from Egypt. Systematic Parasitology 57: 97–109.

———, AND C. VAUCHER. 1999. Proteocephalidae et Monticelliidae(Eucestoda: Proteocephalidea) parasites de poissons d’eau douce duParaguay avec descriptions d’un genre nouveau et de dix especesnouvelles. Revue Suisse de Zoologie 106: 165–240.

———, M. P. ZEHNDER, C. VAUCHER, AND J. MARIAUX. 2004. Theevolution of the Proteocephalidea (Platyhelminthes, Eucestoda)based on an enlarged molecular phylogeny, with comments on theiruterine development. Systematic Parasitology 57: 159–171.


ESSEX, H. E. 1928. The structure and development of Corallobothrium withdescriptions of two new fish tapeworms. Illinois Biological Mono-graphs 11, No. 3, 64 pp. + 5 Plates.

FREZE, V. I. 1965. Proteocephalata in fish, amphibians and reptiles. InEssentials of cestodology. Vol. V., K. I. Skryabin (ed.). Nauka,Moscow, 538 p.

FRITSCH, G. 1886. Die Parasiten des Zitterwelses. Sitzungsberichte derAkademie der Wissenschaften zu Berlin 6: 99–108.

FUHRMANN, O. 1916. Eigentumliche Fischcestoden. Zoologischer Anzeiger18: 385–398.

GIL DE PERTIERRA, A. A., AND A. DE CHAMBRIER. 2000. Rudolphiella szidatin. sp. (Proteocephalidea: Monticelliidae, Rudolphiellinae) parasite ofLuciopimelodus pati (Valenciennes, 1840) (Pisces: Pimelodidae) fromArgentina and new information on Rudolphiella lobosa (Riggenbach,1895). Revue Suisse de Zoologie 107: 81–95.

GUINDON, S., AND O. GASCUEL. 2003. A simple, fast, and accuratealgorithm to estimate large phylogenies by maximum likelihood.Systematic Biology 52: 696–704.

HYPSA, V., A. SkERIKOVA, AND T. SCHOLZ. 2005. Multigene analysis andsecondary structure characters in a reconstruction of phylogeny,evolution and host-parasite relationship of the order Proteocephali-dea (Eucestoda). Parasitology 130: 359–371.

IBRAHEEM, M. H. 1998. The mode of attachment of two cestode speciesinfesting the Nile electric catfish Malapterurus electricus (Froskal),with species reference to the functional morphology of the scolexand histopathology. Arab Gulf Journal of Scientific Research 16:159–172.

JANICKI, C. 1928. Cestoden s. str. aus Fischen und Amphibien. In Resultsof the Swedish zoological expedition to Egypt and the White Nile,1901, part 5, L. A. Jagerskiold (ed.). The Library of the RoyalUniversity of Uppsala, Uppsala, Sweden, p 1–58.

JONES, A. W., C. KERLEY, AND K. E. SNEED. 1956. New species and a newsubgenus of Corallobothrium (Cestoda, Proteocephala) from catfishesof the Mississippi basin. Journal of the Tennessee Academy of Science31: 179–185.

KHALIL, L. F. 1963. On some proteocephalid cestodes from freshwaterfishes in the Sudan. Journal of Helminthology 37: 307–318.

———. 1971. Check list of the helminth parasites of African freshwaterfishes. Commonwealth Agricultural Bureau, Farnham Royal, U.K.,80 p.

———, AND L. POLLING. 1997. Check list of the helminth parasites ofAfrican freshwater fishes. University of the North, Pietersburg,Republic of South Africa, 185 p.

OROS, M., T. SCHOLZ, V. HANZELOVA, AND J. S. MACKIEWICZ. 2010. Scolexmorphology of monozoic cestodes (Caryophyllidea) from thePalaearctic Region: A useful tool for species identification. FoliaParasitologica 57: 37–46.

POSADA, D. 2008. jModelTest: Phylogenetic model averaging. MolecularBiology and Evolution 25: 1253–1256.

REGO, A. A. 1994. Order Proteocephalidea Mola, 1928. In Keys to thecestode parasites of vertebrates, L. F. Khalil, A. Jones, and R. A.Bray (eds.). Wallingford: CAB International, p. 257–293.

———. 1995. A new classification of the cestode order ProteocephalideaMola. Revista Brasileira de Zoologia 12: 791–814.

ROSAS-VALDEZ, R., A. CHOUDHURY, AND G. PEREZ-PONCE DE LEON. 2004.Phylogenetic analysis on genera of Corallobothriinae (Cestoda:Proteocephalidea) from North American ictalurid fishes, using partialsequences of the 28S ribosomal gene. Journal of Parasitology 90:1123–1127.

SCHMIDT, G. D. 1986. CRC handbook of tapeworm identification. CRCPress, Boca Raton, Florida, 675 p.

SCHOLZ T. 1999. Life cycles of species of Proteocephalus Weinland, 1858(Cestoda: Proteocephalidae), parasites of freshwater fishes in thePalearctic region: A review. Journal of Helminthology 72: 1–19.

———, AND H. CAPPELLARO. 1993. Corallobothrium parafimbriatum Befuset Freeman, 1973 (Cestoda, Proteocephalidae), a parasite of NorthAmerican catfishes (Ictalurus spp.) newly introduced into Europe.Folia Parasitologica 40: 105–108.

———, A. DE CHAMBRIER. 2003. Taxonomy and biology of proteocepha-lidean cestodes: Current state and perspectives. Helminthologia 40:65–77.

———, ———, M. BELETEW, AND Z. N. MAHMOUD. 2009. Redescriptionof Proteocephalus glanduligerus (Janicki, 1928) Fuhrmann, 1933(Cestoda: Proteocephalidea), a parasite of Clarias catfishes in Africawith a unique glandular apical organ. Journal of Parasitology 95:443–449.

———, V. R. ROSAS, G. PEREZ-PONCE DE LEON, A. CHOUDHURY, AND A. DE

CHAMBRIER. 2003. Taxonomic status of Choanoscolex lamotheiGarcıa-Prieto, 1990 (Cestoda: Proteocephalidea) and its phylogeneticrelationships to corallobothriine tapeworms from ictalurid catfishesin North America using rDNA sequences. Journal of Parasitology 89:1212–1219.

SWOFFORD, D. L. 2002. PAUP*. Phylogenetic analyses using parsimony(*and other methods). Version 4. Sinauer Associates, Sunderland,Massachusetts.

WAGNER, O. 1917. Uber den Entwicklungsgang und Bau einer Fischtaenie(Ichthyotaenia torulosus Batsch). Jena Zeitschrift fur Naturwis-senschaft 55: 1–66.

YAMAGUTI, S. 1934. Studies on the helminth fauna of Japan. Part 4.Cestodes of fishes. Japanese Journal of Zoology 6: 1–112.

ZEHNDER, M., AND J. MARIAUX. 1999. Molecular systematic analysis of theorder Proteocephalidea (Eucestoda) based on mitochondrial andnuclear rDNA sequences. International Journal for Parasitology 29:1841–1852.


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