RESEARCH EVOLVED

A NEW GENUS AND SPECIES OF MACRODEROIDIDAE, AND OTHER DIGENEANS FROM FISHES OF , AFRICA Author(s): Rodney A. Bray and Sherman S. Hendrix Source: Journal of Parasitology, 93(4):860-865. Published By: American Society of Parasitologists DOI: http://dx.doi.org/10.1645/GE-1084.1 URL: http://www.bioone.org/doi/full/10.1645/GE-1084.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms of use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. J. Parasitol., 93(4), 2007, pp. 860-865 © American Society of Parasitologists 2007

A NEW GENUS AND SPECIES OF MACRODEROIDIDAE, AND OTHER DIGENEANS FROM FISHES OF LAKE MALAWI, AFRICA

Rodney A. Bray and Sherman S. Hendrix* Department of Zoology, Natural History Museum, Cromwell Road, London SW7 5BD, United Kingdom. e-mail: [email protected]

a b s t r a c t : Malawitrema staufferi n. gen., n. sp., an unusual digenean, is described from Clarias mossambicus (type host) and meridionalis from Lake Malawi. It has a small, pyriform body, with a spinous tegument. The ceca are relative short, not reaching to the testes. The 2 testes are symmetrical in the middle hind body. The cirrus sac is long and narrow, reaching into hind body. The genital pore is median, immediately anterior to the ventral sucker. The ovary is pretesticular, and a canalicular seminal vesicle and Laurer’s canal are present. The uterus usually reaches distinctly posteriorly to testes. The eggs are small. The follicular vitellarium is in 2 small fields just anterior to testes. The ventrally subterminal excretory pore leads to a claviform vesicle. This species does not fit clearly into any known family of digeneans and is placed in the Macroderoididae as a temporary measure. Other digeneans reported from Lake Malawi include Haplorchoides cahirinus (Looss, 1896) in C. mossambicus and B. meridionalis; Astiotrema turneri Bray, van Oosterhout, Blais & Cable, 2006 in Protomelas annectens, P. cf. taeniolatus, Labeo- tropheus fuelleborni, Ctenopharynx (Otopharynx) pictus, and Pseudotropheus zebra; Glossidium pedatum Looss, 1899 in C. mossambicus and B. meridionalis; and an unidentifiable sanguinicolid from Bathyclarias nyasensis.

Little is known of the digenean fauna of Lake Malawi (for­ Taxonomic summary merly Lake Nyasa). Prudhoe (1957) reported the metacercaria Type species: Malawitrema staufferi n. sp. of Clinostomoides brieni Dollfus, 1950 in Clarias sp., Taylor Etymology: The genus is named after the lake in which it is found. et al. (1998) mentioned unnamed digeneans in haplochromine , and Bray et al. (2006) recently described a new Astio- Remarks trema species from mbuna cichlids. The present article adds to This species on which this genus is based is not identifiable as any that small data set by reporting 5 species of adult digeneans, of those in Khalil and Polling (1997). In fact, it is difficult to place this including a puzzling new form from siluriforms. form into a currently recognized family; placing the new species in the Macroderoididae is considered a temporary measure until further evi­ dence is available. Using the fish parasite keys in Yamaguti (1971) MATERIALS AND METHODS positions it in either Fellodistomidae Nicoll, 1909 or the Lecithoden- driidae Odhner, 1910. The Fellodistomidae is a predominantly marine Fishes were captured by hook and line, transported alive to the work family, and is characterized by an unarmed tegument, a uterine seminal area, and necropsied within 4 hr of capture. Individual sections of the receptacle, and a Y- or V-shaped excretory vesicle. Clearly, M. staufferi digestive system were examined separately, and all worms were killed does not belong in this family. As far as the Lecithodendriidae is con­ in hot water and fixed in alcohol-formalin-acetic acid (AFA). Whole cerned, a few species of the predominantly amphibian, Ganeo Klein, mounts were stained with Mayer’s paracarmine, cleared in beechwood 1905 and Pleurogenoides Travassos, 1921, are reported in freshwater creosote, and mounted in Canada balsam. Measurements were made fishes in India and Bangladesh, but the present specimen does not look through a drawing tube on an Olympus BH-2 microscope, with the use anything like species in either of these genera with their Y-shaped ex­ of a Digicad plus digitizing tablet and Carl Zeiss KS100 software adapt­ cretory vesicles and lateral genital pores. Nevertheless, according to ed by Imaging Associates, and are quoted in micrometers. The material Yamaguti (1971), a few lecithodendriids are reported as having cylin­ is lodged in the BMNH collection of the Natural History Museum, drical or saccular excretory vesicles, and not all species have lateral London, United Kingdom. genital pores. With the use of the keys and diagnoses in the series by Gibson et al. DESCRIPTION (2002), Jones et al. (2005), and in Schell (1985), it appears that the short ceca suggest affinities with the Brachycoeliidae. Although some brachy- Malawitrema n. gen. coeliids are said to have a Y-shaped excretory system, Brachycoelium Du- jardin, 1845 and Cymatocarpus Looss, 1899 have either an I-shaped ex­ Diagnosis cretory vesicle, or a Y-shaped vesicle with a long stem and ‘‘short incon­ Macroderoididae McMullen, 1937. Body small, pyriform. Eye spot spicuous branches’’ (Prudhoe and Bray, 1982; T. Pojmaiiska, pers. comm.). pigment granules in forebody. Tegument spinous. Oral sucker subglobu- The Brachycoeliidae is reported as occurring only in amphibians, reptiles, lar, subterminal. Ventral sucker rounded, slightly pre-equatorial. Pre­ and, rarely, mammals, so the finding of a brachycoeliid in a fish would be pharynx short. Pharynx small, subglobular. Esophagus distinct. Intesti­ highly unusual. Malawitrema differs from well-established members of the nal bifurcation in posterior forebody. Caeca blind, narrow, reaching to Brachycoeliidae (see Schell, 1985) by the caeca reaching almost to the level of vitelline fields. Testes 2, rounded to oval, margins smooth, testes, the restricted vitelline distribution in the hind body, and the relatively symmetrical in middle hind body, separated, not contiguous. Cirrus sac short, claviform excretory vesicle. long, narrow, reaching into hind body. Internal seminal vesicle long. When Bray et al. (2006) described a new species of Astiotrema Pars prostatica long, wide. Ejaculatory duct short. Genital atrium dis­ Looss, 1900 from freshwater fishes in Lake Malawi, they considered tinct. Genital pore median, immediately anterior to ventral sucker. Ova­ that there were 4 nominal plagiorchiid-like genera in freshwater fishes ry oval, pretesticular, overlapping ventral sucker, separated from testes in Africa, i.e., Astiotrem a, Glossidium Looss, 1899, Alloglossidium Sim- by uterus. Canalicular seminal vesicle and Laurer’s canal present. Uterus er, 1929, and Afromacroderoides Khali, 1972. Malawitrema is not sim­ intercecal usually reaches distinctly posteriorly to testes. Eggs small. ilar to any of them; they all have longer caeca, more extensive vitelline Vitellarium follicular; in 2 small fields laterally, mainly just anterior to fields and tandem to oblique testes. McMullen (1937) erected the family testes. Excretory pore ventrally subterminal. Vesicle claviform, reaching Macroderoididae McMullen, 1937, for the plagiorchioids from fishes just anteriorly to testes. and differentiated it from the Plagiorchiidae by its I-shaped (as opposed to Y-shaped) excretory vesicle. Macroderoidids were, at this time, thought to be only in the digestive tract of fishes. This is still the case Received 4 October 2006; revised 24 January 2007; accepted 25 Jan­ for the type genus, Macroderoides Pearse, 1924, but not for all the other uary 2007. genera subsequently placed in the family, such as Alloglossidium , which * To whom correspondence should be addressed. Department of Biol­ is also found in leeches and crustaceans (Brooks, 2003). Nevertheless, ogy, Gettysburg College, Gettysburg, Pennsylvania 17325. several plagiorchiid-like genera from fishes have been considered mem­

860 BRAY AND HENDRIX— M. STAUFFERI, N. GEN., N. SP., FROM LAKE MALAWI 861

bers of the Macroderoididae, including the marine form Cirkennedya Gibson & Bray, 1979. The constituent genera of the Macroderoididae, and thus of other plagiorchioid families, are the subject of dispute, par­ ticularly as the shape of the excretory vesicle is often difficult to dis­ tinguish or is poorly described. Molecular studies are now being utilized to elucidate the relationships of the plagiorchioid genera and families. These results indicate that Macroderoides is a plagiorchioid genus, but not especially close to the Plagiorchiidae (Tkach, Snyder, and Swider- ski, 2001; V. Tkach, pers. comm.). Alloglossidium does not cluster with Macroderoides and, therefore, although a plagiorchioid is not a ma- croderoidid (V. Tkach, pers. comm.). Prudhoe and Bray (1982) consid­ ered Astiotrem a “a composite group of genera.’’ This idea has been supported by molecular results (Tkach, Pawlowski et al., 2001; V. Tkach, pers. comm.), which have shown that there are at least 3 groups of species, and that Astiotrema (sensu stricto) is not a plagiorchioid. Because of the unsatisfactory state of understanding of the status of plagiorchioid-like digeneans from freshwater fishes, Malawitrema is compared with some putative members of Macroderoididae McMullen, 1937, including Gauhatiana Gupta, 1955 (see Yamaguti, 1958), which is reported mainly from siluriform in India, China, Thailand, and the Philippines (Gupta, 1955; Wang, 1981; Wang et al., 1983; Lo­ pez, 1988; Wongsawad et al., 2004; Lerssutthichawal and Supamattaya, 2005). The type species, G. batrachii Gupta, 1955, has been reported once in Egypt (El-Gwady et al., 1995). It was considered a synonym of Astiotrema reniferum (Looss, 1898) by Yeh and Fotedar (1958). This synonymy was accepted by Kumari et al. (1973), but not by Agrawal (1966), who distinguished the genus by minor details of vitelline dis­ F ig u r e s 1—4. Malawitrema staufferi n. gen., n. sp. (1) Ventral view of tribution. Whichever of these courses is considered best, Malawitrema holotype from Clarias mossambicus, uterus in bold outline only. (2) Ventral is readily distinguished from Gauhatiana (and indeed Astiotrema) by view of worm from Bagrus meridionalis, uterus in bold outline only. (3) the short caeca, the restricted vitelline distribution in the hind body, the Terminal genitalia, specimen from C. mossambicus. (4) Region around fe­ symmetrical testes, and the claviform excretory vesicle. male proximal system, uterus in outline only, eggs obscure detail, specimen One species of Alloglossidium Simer, 1929 is described from Africa, from C. mossambicus. Abbreviations: c, caecum; cs, cirrus sac; Lc, Laurer’s namely A. fatem i Abdel-Maksoud, 1998, from the Clarias lazera canal; ov, ovary; sr, seminal receptacle; t, testis; ut, outline of uterus. Scale in Egypt (Abdel-Maksoud, 1998). As all other members of the genus bars = 1, 200 ^m; 2, 500 ^m; 3, 4, 100 ^m. are reported in freshwater fishes, leeches, and crustaceans in North and Central America, Bray et al. (2006) cast doubt on the generic status of this form. It differs greatly from Malawitrema in its long caeca, more extensive vitellarium with confluent fields at the posterior extremity, at level of esophagus. Tegument spinous, largest spines anterior, de­ and virtually tandem testes. creasing in size and density posterior, detected to about level of testes. Macroderoides is reported only from freshwater fishes, and mainly Oral sucker subglobular, subterminal. Ventral sucker rounded slightly in North America. Some worms are similar in shape to Malawitrema, pre-equatorial. Prepharynx short, within posterior concavity of oral whereas others are rather more elongate, e.g., the type species M. spi- sucker. Pharynx small, subglobular. Esophagus distinct, with recurved niferus Pearse, 1924, M. parvus (Hunter, 1932), and M. trilobatus Tay­ part anterior. Intestinal bifurcation in posterior forebody. Caeca blind, lor, 1978 (Pearse, 1924; Hunter, 1932; Taylor, 1978). Two species are narrow, reach to level of vitelline fields, not quite reaching to testes. more similar to Malawitrema in shape, although somewhat larger; these Testes 2, rounded to oval, margins smooth, symmetrical in middle are M. flavus Van Cleave & Mueller, 1932 and M. typicus (Winfield, hind body, separated, not contiguous. Cirrus sac long, narrow, reaching 1929) (Van Cleave and Mueller, 1932; Winfield, 1929). They differ in into hind body (Fig. 3). Internal seminal vesicle long, with evidence of the length of the caeca, which in both cases reach almost to the posterior folds. Pars prostatica long, wide, with sparse gland cells. Ejaculatory extremity, certainly well past the testes. The vitellarium is somewhat duct short, not seen to form cirrus. Genital atrium distinct. Genital pore more extensive, reaching to the posterior extent of the testes. The testes median, immediately anterior to ventral sucker. in both species are oblique. Ovary oval, pretesticular, overlapping ventral sucker, separated from One nominal species of Macroderoides is reported outside America, testes by uterus. Canalicular seminal receptacle oval, posterior to uterus. namely M. asiaticus Belouss in Skrjabin and Antipin, 1958, from the Laurer’s canal opens dorsally between seminal receptacle and ovary bagrid siluriforms, the yellow catfish Pseudobagrus fulvidraco (Rich­ (Fig. 4). Mehlis’ gland posterior to ovary. Uterus intercecal, usually ardson, 1846), Primorskii Krai, far eastern Russia, and the Ussuri catfish reaches distinctly posteriorly to testes, lies ventrally to ovary and me­ Liocassis ussuriensis (Dybowski, 1872), in the River Amur basin dian parts of testes. Eggs small, tanned, operculate. Metraterm narrow; (Skrjabin and Antipin, 1958; Akhmerov, 1961). This species looks rath­ reaches to about posterior margin of ventral sucker; walls slightly thick­ er like an Astiotrem a, with its long caeca, tandem testes, and relatively ened. Vitellarium follicular; in 2 small fields laterally, anterior extent extensive vitelline fields distinguishing it from Malawitrema. just posterior to ventral sucker, posterior extent to, or just overlapping, This unusual parasite is placed into the Macroderoididae until further testes. studies are undertaken. Regrettably, these worms were fixed in formalin Excretory pore ventrally subterminal. Vesicle claviform, reaching just and are not amenable to molecular study. anteriorly to testes.

Taxonomic summary DESCRIPTION Type host: Clarias mossambicus Peters, 1852, immature male, Clar- Malawitrema staufferi n. sp. iidae, Siluriformes, SL = 430 mm (syn. of North African catfish Clarias (Figs. 1-4) gariepinus [Burchell, 1822] according to Froese and Pauly, 2006). Other host: Bagrus meridionalis Gunther, 1894 juvenile, , Diagnosis (Based on 11 specimens from C. mossambicus and Siluriformes, kampango, SL = 445 mm. 3 from B. meridionalis) Type locality: Deep water of the southeast arm of Lake Malawi Measurements in Table I. Body small, pyriform, narrow, widest in (14°06'S, 35°03'E) anterior hind body or, in younger specimens, constricted in anterior hind Site of infection: Clarias mossambicus, in pyloric half of intestine; body (Figs. 1 and 2). Eyespot pigment granules scattered in forebody B. meridionalis, distal half of intestine. 862 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 4, AUGUST 2007

T a b l e I. M easurements of Malawitrema staufferi n. gen., n. sp.

Host Clarias mossambicus (n = 11) Bagrus meridionalis (n = 3)

Length 664-799 (734) 581-965 (733) Width 194-273 (235) 224-352 (268) Forebody (%) 246-324 (280) 224-370 (284) Oral sucker 96-118 X 113-132 (107 X 123) 107-146 X 110-152 (121 X 125) Prepharynx 0 0 Pharynx 31-39 X 39-52 (35 X 46) 3 3 -4 4 X 38-54 (38 X 46) Esophagus 96-133 (118) 88-162 (119) Intestinal bifurcation to ventral sucker 23-52 (35) 19-39 (28) Previtelline distance 364-465 (402) 331-527 (412) Long vitelline field 85-150 (114) 107-175 (137) Short vitelline field 83-133 (104) 84-144 (112) Ventral sucker 93-109 X 99-129 (101 X 113) 89-133 X 97-144 (104 X 114) Cirrus sac 141-207 X 25-31 (173 X 29) 154-237 X 28-50 (187 X 38) Ventral sucker to ovary distance 0 0 Ovary 63-80 X 43-73 (72 X 61) 67-81 X 63-77 (74 X 69) Ovary to anterior testis distance 53-108 (76) 40-152 (84) Testes 76-110 X 57-95 (93 X 75) 87-112 X 72-114 (93 X 86) Intertesticular distance 0-9 9 (42) 6-55 (28) Posttesticular distance 117-179 (140) 76-180 (121) Postvitelline distance 170-245 (201) 152-262 (191) Postuterine distance 78-129 (103) 21-95 (67) Postcecal distance 247-324 (283) 214-228 (221) Eggs 27-38 X 11-15 (34 X 14) 30-35 X 15-18 (32 X 16) Width (%)* 26.5-38.9 (32.1) 35.2-38.5 (36.7) Forebody (%)* 35.3-41.1 (38.2) 38.4-39.7 (38.9) Intestinal bifurcation to ventral sucker as percent of forebody length 8.21-16.0 (12.4) 7.39-10.9 (9.64) Sucker-length ratio 1:0.90-0.99 (0.95) 1:0.83-0.91 (0.86) Sucker-width ratio 1:0.85-0.99 (0.92) 1:0.88-0.95 (0.90) Oral sucker:pharynx ratio 1:0.34-0.40 (0.37) 1:0.34-0.40 (0.37) Oral sucker length (%)* 13.1-17.1 (14.5) 15.2-18.4 (16.7) Pharynx length (%)* 3.96-5.49 (4.72) 4.54-5.76 (5.30) Ventral sucker length (%)* 12.9-15.4 (13.7) 13.8-15.3 (14.4) Esophagus (%)* 13.8-18.2 (16.1) 15.1-16.8 (16.1) Previtelline distance (%)* 47.7-58.7 (54.8) 54.6-58.0 (56.5) Long vitelline field (%)* 11.3-19.6 (15.6) 18.1-19.9 (18.8) Cirrus sac length (%)* 20.1-25.9 (23.6) 24.6-26.5 (25.7) Ovary length (%)* 8.23-12.1 (9.88) 8.34-11.5 (10.4) Ventral sucker to ovary distance (%) 0 0 Ovary to anterior testis distance (%)* 7.58-14.7 (10.4) 6.90-15.7 (10.6) Testis length (%)* 10.1-14.4 (12.6) 9.24-16.5 (13.2) Intertesticular distance (%)* 0-13.8 (5.85) 0.95-5.67 (3.60) Posttesticular distance (%)* 15.3-23.5 (19.0) 13.1-18.7 (16.0) Postvitelline distance (%)* 22.3-32.1 (27.4) 24.5-27.2 (26.0) Postuterine distance (%)* 9.81-18.0 (14.2) 3.59-14.5 (8.97) Postcecal distance (%)* 19.2-40.0 (34.7) 34.1-37.9 (36.0)

* Percent of body length.

Prevalence: Clarias mossambicus, 1 of 1; B. meridionalis, 1 of 1. iepinus [Burchell, 1822] according to Froese and Pauly, 2006); Bagrus Type and voucher specimens: Clarias mossambicus Holotype BMNH meridionalis Gunther, 1894 juvenile, Bagridae, Siluriformes,kampango, 2006.11.8.94, paratypes 2006.11.8.95—118; B. meridionalis, paratypes SL = 445 mm. BMNH 2006.11.8.91-93. Locality: Deep water of the southeast arm of Lake Malawi. Etymology: The specific name honors Dr. Jay R. Stauffer, Jr. of Penn­ Site of infection: Clarias mossambicus, in pyloric half of intestine; sylvania State University for his kindness in granting S.S.H. the op­ B. meridionalis, distal half of intestine. portunity to collect the fish hosts at his research base in Malawi. Prevalence: Clarias mossambicus, 1 of 1; B. meridionalis, 1 of 1. Voucher specimens: Clarias mossambicus BMNH 2006.11.8.145­ OTHER TREMATODA COLLECTED 146; B. meridionalis, BMNH 2006.11.8.129-144.

Heterophyidae Leiper, 1909 Remarks Haplorchoides cahirinus (Looss, 1896) Chen, 1949 This species is reported in Bagrus spp. in Egypt and Uganda (Khalil Hosts: Clarias mossambicus Peters, 1852, immature male, Clariidae, and Polling, 1997; Arafa et al., 2002; Hamada and Abdrabouh, 2005). Siluriformes, SL = 430 mm (syn. of North African catfish Clarias gar- We detected no morphological distinctions to published descriptions BRAY AND HENDRIX— M. STAUFFERI, N. GEN., N. SP., FROM LAKE MALAWI 863

TABLE II. Measurements of Astiotrema turneri and Glossidium pedatum .

Species Astiotrema Astiotrema Astiotrema Astiotrema Glossidium Glossidium turneri turneri turneri turneri pedatum pedatum Host

Protomelas Protomelas Labeotropheus Ctenopharynx Clarias Bagrus annectens ?taeniolatus fuelleborni (Otopharynx) mossambicus meridionalis (n = 1) (n = 1) (n = 1) pictus (n = 2) (n = 1) (n = 1)

Length 1,329 1,537 1,850 1,490-1,897 1,214 1,757 Width 580 768 584 574-646 376 438 Forebody (%) 305 412 536 371-575 399 484 Oral sucker 130 X 169 137 X 187 179-192 145-176 X 181-205 143 X 174 170 X 174 Prepharynx 5 7 0 2-22 22 5 Pharynx 61 X 71 88 X 68 93 X 71 78-97 X 83-107 74 X 86 79 X 91 Esophagus 224 193 244 289-374 29 26 Intestinal bifurcation to ventral 34 74 84 33-87 169 206 sucker Previtelline distance 241 358 364 360-566 535 589 Long vitelline field 682 803 1,036 773-838 549 700 Short vitelline field 685 682 779 556-712 388 635 Ventral sucker 150 X 175 187 X 203 183 X 188 187-196 X 199-242 164 X 180 200 X 200 Cirrus sac 265 X 49 ? 228 X 50 255-292 X 48-54 366 X 45 385 X 93 Ventral sucker to ovary distance 0 0 0 0-7 12 19 Ovary 172 X 187 104-191 197 X 176 132-165 X 160-165 114 X 111 135 X 211 Ovary to anterior testis distance 132 112 0 12-59 81 42 Anterior testis 128 X 167 114 X 187 140 X 170 149-172 X 169-187 137 X 163 143 X 186 Intertesticular distance 69 177 136 54-68 27 111 Posterior testis 124 X 192 85 X 214 124 X 194 98-115 X 140-144 126 X 209 149 X 220 Posttesticular distance 462 532 634 461-646 187 508 Postvitelline distance 349 435 466 387-389 168 477 Postuterine distance 73 33 12 226-411 12 19 Postcecal distance 188-189 245 ? 226-368 89-106 ? Eggs 34 X 17 41 X 14 37 X 11 39-40 X 11-13 36 X 18 39 X 18 Width (%)* 43.7 49.9 31.5 34.0-38.5 31.0 24.9 Forebody (%)* 22.9 26.8 29.0 24.9-30.3 32.9 27.5 Intestinal bifurcation to ventral 11.0 17.9 15.6 8.76-15.2 42.3 42.6 sucker as % of forebody length Sucker-length ratio 1:1.54 1:1.37 1:1.02 1:1.11-1.29 1:1.15 1:1.18 Sucker-width ratio 1:1.04 1:1.08 1:0.98 1:1.00-1.18 1:1.03 1:1.15 Oral sucker-pharynx ratio 1:0.42 1:0.36 1:0.37 1:0.42-0.52 1:0.49 1:0.52 Oral sucker length (%)* 9.77 8.89 9.70 9.29-9.74 11.8 9.65 Pharynx length (%)* 4.59 5.70 5.02 5.11-5.26 6.07 4.50 Ventral sucker length (%)* 11.3 12.2 9.90 10.3-12.5 13.5 11.4 Esophagus (%)* 16.8 12.6 13.2 19.4-19.7 2.36 1.46 Previtelline distance (%)* 18.2 23.3 19.7 24.2-29.8 44.1 33.5 Long vitelline field (%)* 51.4 52.2 56.0 44.2-51.9 45.3 39.8 Cirrus sac length (%) 19.9 ? 12.3 15.4-17.1 30.1 21.9 Ovary length (%)* 13.0 13.3 10.7 8.70-8.84 9.37 7.66 Ventral sucker to ovary distance (%) 0 0 0 0-0.38 0.99 1.11 Ovary to anterior testis distance (%)* 10.0 7.27 0 0.62-3.93 6.69 2.42 Anterior testis length (%)* 9.63 7.40 7.55 9.08-10.0 11.3 8.11 Intertesticular distance (%)* 5.17 11.5 7.34 2.86-4.58 2.22 6.31 Posterior testis length (%)* 9.31 5.55 6.72 6.05-6.58 10.34 8.49 Posttesticular distance (%)* 34.7 34.6 34.3 30.9-34.1 15.4 28.9 Postvitelline distance (%)* 26.3 28.3 25.2 20.5-26.0 13.8 27.2 Postuterine distance (%)* 5.47 2.12 0.64 0.39-2.09 0.97 1.10 Postcecal distance (%)f 40.9 23.1 ? 42.0-84.5 52.0 ? Postcecal distance (%)* 14.2 7.98 ? 14.3-26.2 7.99 ?

* Percent of body length. f Percent of posttesticular distance. 864 THE JOURNAL OF PARASITOLOGY, VOL. 93, NO. 4, AUGUST 2007

(Looss, 1899; Khalil and Thurston, 1973). Many specimens were found Remarks in B. meridionalis and only 2 in C. mossambicus. This appears to be A single, nonovigerous worm was found in the proximal half of the the first report of this species from Clarias. intestine. It has a large, deeply divided testis, which reaches almost to the nerve ring and envelopes the X-shaped part of the intestine. This Plagiorchiidae Luhe, 1901 feature distinguishes this specimen from members of the freshwater sanguinicolid genus Sanguinicola Plehn, 1905 (see Smith, 2002), in­ Astiotrema turneri Bray, van Oosterhout, Blais & Cable, 2006 cluding the only species known from Clarias in Africa, i.e., S. clarias Hosts: Protomelas annectens (Regan, 1922) male?, Cichlidae, Per- Imam, Marzouk, Hassan & Itman, 1984, from C. lazera in the Nile at ciformes, SL = 75 mm, kambuzi; Protomelas cf. taeniolatus (Trewavas, Cairo and Giza, Egypt (Imam et al., 1984). 1935) female, Cichlidae, Perciformes, SL = 78 mm, spindle hap; La- beotropheus fuelleborni Ahl, 1926, male, Cichlidae, Perciformes, blue ACKNOWLEDGMENTS mbuna; Ctenopharynx (Otopharynx) pictus (Trewavas, 1935), Cichlidae, Perciformes, SL = 105 mm; Pseudotropheus zebra (Boulenger, 1899) We would like to acknowledge financial support by Gettysburg Col­ male, Cichlidae, Perciformes, SL = 84 mm, zebra mbuna. All lege for making the collection of hosts possible. A special thanks to hosts were collected alive with the use of SCUBA and maintained alive Jay R. Stauffer, Jr. and Matthew E. Arnegard for their help in host until examined. collection and to the government of Malawi for issuing the collecting Localities: All Lake Malawi, July 1996, P. annectens, Songwe Hill, permit to Jay R. Stauffer. We also thank Teresa Pojmailska, W. Stefanski between Harbor Island and Kanchedza Island, SE Arm; P . cf. taeniola- Institute of Parasitology, Warsaw, Poland, for permission to cite as-yet- tus, Kanchedza Island; L. fuelleborni, Harbor Island; C. pictus, Kan- unpublished work. Vasyl Tkach, University of North Dakota, Grand chedza Island; P. zebra, Harbor Island. Forks, North Dakota, kindly commented on a draft of the article and Sites of infection: Protomelas annectens, midintestine; P . cf. taeni- gave permission to mention an unpublished finding. olatus, midintestine; L. fuelleborni, intestine 1/3 distance from stomach; C. pictus, intestine; P. zebra, intestine. LITERATURE CITED Prevalence: Protomelas annectens, 33%, 1 of 3; P. cf. taeniolatus, ABDEL-MAKSOUD, N. M. 1998. Revision o f Alloglossidium Simer 1929 25%, 1 of 4; L. fuelleborni, 33%, 1 of 3; C. pictus, 1of 1; P. zebra, (Trematoda: Macroderoididae) and description of A. fatem i sp. n. 20%, 1 of 5. from a freshwater catfish. Journal of the Egyptian German Society Voucher specimens: Protomelas annectens, BMNH 2006.11.8.126; of Zoology. Invertebrate Zoology & Parasitology 25(D): 115-124. P. cf. taeniolatus, BMNH 2006.11.8.125; L. fuelleborni, BMNH A g r a w a l , V. 1966. Four trematode parasites (Plagiorchiidae Luhe, 1901 2006.11.8.127; C. pictus, BMNH 2006.11.8.123-124; P. zebra, BMNH emend. Ward, 1917) from reptiles of Lucknow. Revista de Biologia 2006.11.8.128. Tropical 14: 133-151. AKHMEROV, A. H. 1961. On the trematode fauna of fishes in the basin Remarks of the River Amur. Trudy Gelmintologicheskoi Laboratorii 11: 22­ This species was recently described by Bray et al. (2006) from the 31. cichlids Pseudotropheus zebra (type host), P. emmiltos (Stauffer et al. A r a f a , S. Z, E. S. R e d a , a n d M. M. El-Naggar. 2002. Cholinergic 1997), Labeotropheus trewavasae (Fryer 1956), and Melanochromis components of the nervous system of the digenean parasites, Hap- vermivorus Trewavas, 1935, in Lake Malawi. As most of the hosts re­ lorchoides cahirinus and Acanthostomum absconditum from the ported here are new, we have included measurements of the specimens catfish Bagrus bayad in Egypt. Acta Parasitologica 47: 272-279. in Table II. There appear to be no morphological reasons for considering B r a y , R. A., C. V. O osterhout, J. Blais, and J. C a b l e . 2006. Astio- any of these specimens distinct. As noted above, the genus Astiotrema trema turneri n. sp. (Digenea: Plagiorchiidae) from cichlid fishes (sensu stricto) is not a plagiorchioid, but is retained in the Plagiorchiidae (Cichlidae: Perciformes) of Lake Malawi. Zootaxa 1319: 43-58. here pending publication of further evidence on its status. B r o o k s , D. R. 2003. Lessons from a quiet classic. Journal of Parasi­ tology 89: 878-888. E l - G w a d y , H. M., M. G. H a s s a n , A. A. Abdel-Aal, and A. S. D ia b . Glossidium pedatum Looss, 1899 1995. Internal helminths of some Egyptian fresh water fishes. In Hosts: Clarias mossambicus Peters, 1852, immature male, Clariidae, Program and book of abstracts. IVth International Symposium of Siluriformes, SL = 430 mm (syn. of North African catfish Clarias gar- Fish Parasitology. Munich, Germany, 101 p. iepinus [Burchell, 1822] according to Froese and Pauly, 2006); Bagrus F r o e s e , R., a n d D. P a u l y . 2006. FishBase. http://www.fishbase.org. meridionalis Gunther, 1894 juvenile, Bagridae, Siluriformes, kampango, G ib s o n , D. I., A. Jones, and R. A. B r a y . 2002. Keys to the Trematoda. SL = 445 mm. Volume 1. CABI Publishing and the Natural History Museum, Wal­ Locality: Deep water of the southeast arm of Lake Malawi. lingford, U.K., 521 p. Sites of infection: Clarias mossambicus, in pyloric half of intestine; G u p t a , S. P. 1955. Trematode parasites of fresh-water fishes. Indian B. meridionalis, distal half of intestine. Journal of Helminthology 5(1953): 1-80. Prevalence: Clarias mossambicus, 1 of 1; B. meridionalis, 1 of 1. H a m a d a , S. F., a n d A. E. S. Abdrabouth. 2005. Anatomical and mor­ Voucher specimens: Clarias mossambicus BMNH 2006.11.8.122; B. phological studies on the intestinal digenean parasite Haplorchoi- meridionalis, BMNH 2006.11.8.119-121. des cahirinus from Bagrus bajad in Egypt. Egyptian Journal of Zoology 44: 81-97. H u n t e r , G. W., III. 1932. A new trematode (Plesiocreadium parvum, Remarks sp. nov.) from fresh water fish. Transactions of the American Mi­ This species was discussed by Bray et al. (2006), who pointed out croscopical Society 51: 16-21. that it was originally described in Bagrus spp. and has been reported Im a m , E. A., M. S. M. M a r z o u k , A. A. Hassan, and R. H. I t m a n . in C. mossambicus, or its putative synonyms, from as widely apart as 1984. Studies of Sanguinicola sp. (Trematoda) of Nile fishes. Vet­ Ethiopia, Egypt, and South Africa. Measurements are included in Table erinary Medical Journal, Egypt 32: 1-13. II. J o n e s , A., R. A. B r a y , a n d D. I. G ib s o n . 2005. Keys to the Trematoda. Volume 2. CABI Publishing and the Natural History Museum, Wal­ Sanguinicolidaevon Graff, 1907 lingford, u.K., 745 p. K h a l i l , L. F., a n d L. P o l l i n g . 1997. Check list of the helminth parasites Host: Bathyclarias nyasensis (Worthington, 1933), Clariidae, Siluri- of African freshwater fishes. University of the North, Pietersburg, formes, sapuwa. South Africa, 185 p. Locality: Deep water of the southeast arm of Lake Malawi. ------, a n d J. P. T h u r s t o n . 1973. Studies on the parasites of fresh­ Site of infection: Proximal half of intestine. water fishes of Uganda, including the descriptions of two new spe­ Prevalence: One of 1. cies of digeneans. Revue de Zoologie et Botanique Africaines 87: Voucher specimen: BMNH 2006.11.8.147. 209-248. BRAY AND HENDRIX— M. STAUFFERI, N. GEN., N. SP., FROM LAKE MALAWI 865

K u m a r i , N. V., C. B. Srivastava, and B. S. C h a u h a n . 1973. Rede­ T a y l o r , M. I., G. F. T u r n e r , R. L. Robinson, and J. R. Stauffer, Jr. scription of Astiotrema reniferum (Looss, 1898) Looss, 1900 with 1998. Sexual selection, parasites and bower height skew in a bow­ comments on the status of the genus Pseudoparamacroderoides er-building cichlid fish. Behaviour 56: 379-384. Gupta & Agarwal, 1968 (Trematoda: Plagiorchiidae). Records of T a y l o r , P. W. 1978. Macroderoides trilobatus sp. n. (Digenea: Ma- the Zoological Survey of India 67: 315-323. croderoididae) from the bowfin, Am ia calva, and emendation of the Lerssutthichaw al, T., a n d K. Supam attaya. 2005. Diversity and dis­ genus. Journal of Parasitology 64: 393-394. tribution of parasites from potentially cultured freshwater fish in T k a c h , V. V., J. Pawlowski, J. M ariaux, and Z. Swiderski. 2001. Nakhon Si Thammarat. Songklanakarin Journal of Science and Molecular phylogeny of the suborder Plagiorchiata and its position Technology 27(Suppl. 1): 333-345. in the system of Digenea. In Interrelationships of the Platyhelmin- L o o s s , A. 1899. Weitere Beitrage zur Kenntnis der Trematoden-fauna thes, D. T. J. Littlewood, and R. A. Bray (eds.). Taylor & Francis, Aegyptens, zugleich Versuch einer natiirlichen Gliederung des Ge­ London, U.K., p. 186-193. nus D istomum Retzius. Zoologische Jahrbucher 12: 521-784. ------, S. D. Snyder, and Z. Swiderski. 2001. On the phylogenetic L o p e z , N. C. 1988. Helminth and arthropod parasites of some freshwater relationships of some members of Macroderoididae and Ocheto- fishes from Laguna Lake and vicinities. In Fish health problems in somatidae (Digenea, Plagiorchioidea). Acta Parasitologica 46: 267­ Laguna de Bay and environs, M. R. delos Reyes, and E. H. Belen 275. (eds.). Phillippine Council for Agriculture, Forestry and Natural Van Cleave, H. J., a n d J. F. M u e l l e r . 1932. Parasites of the Oneida Resources Research and Development, Book Series No. 49, Los Lake fishes. Part 1. Descriptions of new genera and new species. Banos, Philippines, p. 7-14. Roosevelt Wildlife Annals 3: 9-71. W a n g , P.-Q. 1981. Notes on some trematodes from freshwater fishes in M c M u l l e n , D. B. 1937. A discussion of the of the family Plagiorchiidae Luhe, 1901, and related trematodes. Journal of Par­ Fujian Province. Journal of Fujian Teacher’s University. Natural Science Edition 11: 81-90. asitology 23: 244-258. ------, Y.-R. Z h a o , Q.-G. C h e n , a n d J.-Y. T a o . 1983. Notes on some P e a r s e , A. S. 1924. Observations on parasitic worms from Wisconsin species of parasitic helminths from freshwater fishes and five new fishes. Transactions of the Wisconsin Academy of Sciences, Arts species in Hongze Lake. Journal of Fujian Teacher’s University. and Letters 21: 147-160. Natural Science Edition 1983: 125-134. P r u d h o e , S. 1957. Trematoda. Exploration du Parc National de W i n f i e l d , G. F. 1929. Plesiocreadium typicum, a new trematode from l’Upemba 48: 1-28. Am ia calva. Journal of Parasitology 16: 81-87. ------, a n d R. A. B r a y . 1982. Platyhelminth parasites of the Am­ WONGSAWAD, C., J. ROJTINNAKOM, P. WoNGSAWAD, A. ROJANAPAIBUL, phibia. British Museum (Natural History) and Oxford University T. M a r a y o n g , S. Suwattanacoupt, P. Sirikanchana, O. S e y , a n d Press, London, U.K., 217 p. B. V. J a d h a v . 2004. Helminths of vertebrates in Mae Da Stream, S c h e l l , S. C. 1985. Handbook of trematodes of North America north Chiang Mai, Thailand. Southeast Asian Journal of Tropical Medi­ of Mexico. University of Idaho Press, Moscow, Idaho, 263 p. cine and Public Health 35(Suppl. 1): 140-146. S k r j a b i n , K. I., a n d D. N. A n t i p i n . 1958. Superfamily Plagiorchioidea Y a m a g u t i , S. 1958. Systema helminthum. Vol. I. The digenetic trem­ Dollfus, 1930. Part 2. Family Plagiorchidae [sic] Liuhe, 1901. Tre- atodes of vertebrates. Interscience Publishers, New York, New matody Zhivotnykh I Cheloveka. Osnovy Trematodologii 14: 73­ York, 1575 p. 631. ------. 1971. Synopsis of digenetic trematodes of vertebrates, Volume S m ith , J. W. 2002. Family Sanguinicolidae Graff, 1907. In Keys to the I. Keigaku Publishing Co., Tokyo, Japan, 1074 p. trematode parasites of vertebrates, Volume 1, D. I. Gibson, A. Y e h , L.-S., a n d D. N. F o t e d a r . 1958. A review of the trematode genus Jones, and R. A. Bray (eds.). CAB International, Wallingford, U.K., Astiotrem a in the family Plagiorchiidae. Journal of Helminthology p. 433-452. 32: 17-32.