Macrourimegatrema gadoma n. sp. (Digenea: Opecoelidae) from the ...

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thread grenadier Gadomus arcuatus (Goode &. Bean) (Macrouridae) collected from the north- eastern Gulf of Mexico and off Venezuela. The new species differs ...
Syst Parasitol (2007) 67:93–99 DOI 10.1007/s11230-006-9074-2

ORIGINAL PAPER

Macrourimegatrema gadoma n. sp. (Digenea: Opecoelidae) from the doublethread grenadier Gadomus arcuatus (Goode & Bean) (Macrouridae) in the Gulf of Mexico and Caribbean Sea Charles K. Blend Æ Norman O. Dronen Æ Howard W. Armstrong

Received: 13 March 2006 / Accepted: 17 May 2006 / Published online: 2 December 2006  Springer Science+Business Media B.V. 2006

Abstract Macrourimegatrema gadoma n. sp. (Digenea: Opecoelidae: Plagioporinae) is described from the pyloric caeca and intestine of the doublethread grenadier Gadomus arcuatus (Goode & Bean) (Macrouridae) collected from the northeastern Gulf of Mexico and off Venezuela. The new species differs from Macrourimegatrema brayi Blend, Dronen & Armstrong, 2004, the type and only species in the genus, in the distribution of the vitelline follicles and gonads, a larger body size, and the presence of highly-folded caeca with numerous outpocketings or pouches. It is suggested that species of Macrourimegatrema Blend, Dronen & Armstrong, 2004 probably infect their piscine hosts through the ingestion of a benthopelagic crustacean.

Introduction Blend, Dronen, and Armstrong (2004) established Macrourimegatrema Blend, Dronen & Armstrong, C. K. Blend (&) Department of Biology, Gordon College, 255 Grapevine Road, Wenham, MA 01984, USA e-mail: [email protected] N. O. Dronen Æ H. W. Armstrong Laboratory of Parasitology, Department of Wildlife and Fisheries Sciences, College of Agriculture and Life Sciences, Texas A&M University, College Station, TX 77843-2258, USA

2004 and described M. brayi Blend, Dronen & Armstrong, 2004 collected from the pyloric caeca and intestine of the bullseye grenadier Bathygadus macrops Goode & Bean, B. favosus Goode & Bean, Vaillant’s grenadier B. melanobranchus Vaillant and the doublethread grenadier Gadomus arcuatus (Goode & Bean) inhabiting deeper waters within the Gulf of Mexico and Caribbean Sea. Macrourimegatrema was distinguished from other plagioporine genera by the combination of the following diagnostic features: an atypically large elongate body; a short, distinct forebody separated from a long hindbody by a distinct constriction at the level of the ventral sucker; a terminal, funnelshaped oral sucker; nearly equatorial gonads and an unusual tubular excretory vesicle winding between the two tandem testes. Blend et al. (2004, table 1) also provided a review of the endohelminths reported from species of Bathygadus Gu¨nther and Gadomus Regan, discussed the complexities of placing opecoelid genera into subfamilies within the Opecoelidae Ozaki, 1925, and suggested that M. brayi probably infected its fish hosts through the ingestion of a benthopelagic crustacean intermediate host. During an ongoing study of the helminth parasites of deep-sea macrourid fishes from the Gulf of Mexico and Caribbean Sea, specimens of an undescribed opecoelid digenean representing a new species of Macrourimegatrema were found; these are described herein.

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Table 1 Dimensions of Macrourimegatrema gadoma n. sp. and M. brayi Blend, Dronen & Armstrong, 2004 from Gadomus arcuatus (Goode & Bean) Parasite n

M. gadoma n. sp. 9

M. brayi1 4

Length Width at pharynx at VS at PT Forebody l2 Oral sucker (OS) l w2 Prepharynx l Pharynx l w Oesophagus l Ventral sucker (VS) l w VS to Vitell. VS to OV Cirrus-sac l w Ovary (OV) l w Seminal receptacle l w OV to AT Anterior testis (AT) l w AT to PT Posterior testis (PT) l w Post-test. region (PTR) l w Post-uterine region (PUR) l Post-caecal distance Egg l w Width at PT %3 Forebody %3 Sucker-ratio OS:pharynx width ratio Oesophagus %3 VS to OV %3 PTR %3 PUR %3

6,275–11,100 (9,290)2 300–650 (460) [n = 8]2 430–780 (575) 530–1,200 (850) 560–1,025 (765) 350–670 (460) [n = 8] 310–610 (410) [n = 8] 0–70 (32) [n = 8] 80–175 (112) [n = 7] 65–155 (110) [n = 7] 210–470 (290) [n = 8] 280–490 (380) 290–520 (400) 1,200–2,550 (1,840) 2,500–4,360 (3,550) 320–690 (545) [n = 8] 105–230 (190) 180–340 (260) 210–550 (335) 100–680 (235) [n = 8] 70–540 (95) [n = 7] 60–730 (320) 290–560 (445) 300–620 (440) 35–560 (210) 310–650 (525) 310–620 (440) 2,025–4,250 (2,940) 625–1,350 (935) 2,885–6,175 (4,600) 175–390 (275) 55.0–67.5 (61.5) [n = 37] 35.0–45.0 (39.2) [n = 36] 5.6–12.3 (9.1) 5.6–10.8 (8.4) 1:0.9–1.1 (1.0) [n = 8] 1:3.0–4.6 (3.9) [n = 7] 2.4–4.2 (3.2) [n = 8] 31.2–45.2 (38.5) 27.2–38.3 (31.5) 41.1–55.2 (49.0)

4,000–9,780 (6,100) 490–620 (525) 430–700 (565) 540–990 (720) 410–1,200 (660) 330–520 (400) 300–480 (370) 8–110 (60) 75–130 (110) 75–105 (90) 140–220 (185) 250–350 (310) 280–450 (350) 100–210 (155) 1,250–3,000 (1,830) 315–575 (400) 115–280 (170) 90–315 (185) 190–390 (270) 110–225 (170) 35–100 (75) 75–290 (140) 155–530 (295) 195–450 (305) 60–120 (95) 160–550 (340) 250–460 (320) 1,400–3,450 (2,240) 575–1,075 (735) 2,025–5,275 (3,295) 320–610 (435) 60.0–72.5 (65.0) 27.5–42.5 (35.0) 10.1–15.3 (12.4) 7.7–12.6 (10.7) 1:0.9–1.0 (1.0) 1:3.5–4.6 (4.1) 1.4–4.5 (3.1) 27.1–31.4 (30.1) 33.1–42.2 (36.4) 48.0–60.2 (53.2)

1

Measurements for M. brayi are from Blend et al. (2004, Table 2)

2

l, length; w, width; mean (parentheses); number [n] of measurements

3

Proportion of body length

Materials and methods Sixteen specimens of the doublethread grenadier Gadomus arcuatus were examined for parasites. Specimens of the new species described herein were collected aboard ship or procured from

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fishes housed in the Texas Cooperative Wildlife Collection, Texas A&M University (TCWC). Ten G. gadomus were examined by one of us (HWA); nine obtained during June, 1971 from two locations within the northeastern Gulf of Mexico off Florida (2738¢N, 8515¢W; depth

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637 m; and 2822¢N, 8631¢W; depth 710 m) and a tenth specimen obtained during November, 1970 from the Caribbean Sea off Colombia (1107¢N, 7530¢W; depth 1,092 m). Six additional G. gadomus housed in the TCWC obtained during July, 1970 from the Caribbean Sea off Venezuela (1253¢N, 6957.5¢W; depth 1,006–1,115 m) were examined by two of us (CB & ND). All fish were collected by trawl and either examined for parasites onboard ship, with live specimens being heat-fixed under slight coverslip pressure in hot AFA and preserved in 70% ethanol, or live fish were immediately fixed in 10% formalin onboard ship and transported back to the university before being transferred to and stored in 70% ethanol prior to dissection. Digenea were stained in Semichon’s carmine or alum cochineal, sometimes counterstained in fast green and mounted in Kleermount or Permount. Drawings were made with the aid of a drawing tube and a Nikon Superhigh-Performance 3 · Zoom Coolpix 990 digital camera and image software system. Measurements are in micrometres with the range followed by the mean in parentheses; the number [n] of measurements is also noted. Specimens fixed in situ generally did not appear to be significantly different than those fixed live. The identification of the fish for this study was based on Cohen, Inada, Iwamoto, and Scialabba (1990), and the fish classification and authorities follow FishBase (Froese & Pauly, 2006). The identification of the digeneans was based on Pritchard (1966), Yamaguti (1971) and Gibson and Bray (1982, 1984), and ecological terms follow Bush, Lafferty, Lotz, and Shostak (1997). Specimens of M. brayi from the following museums were examined for this study: the Natural History Museum, London, UK (BMNH 2004.3.18.5–95); the United States National Parasite Collection, Beltsville, Maryland, USA (USNPC 094587.00–094593.00); the Harold W. Manter Laboratory, University of Nebraska– Lincoln, Lincoln, Nebraska, USA (HWML 45684–45693); and the Coleccio´n Nacional de Helminthos, Instituto de Biologı´a, Universidad Nacional Auto´noma de Me´xico, Mexico City, Mexico (CNHE 4939–4940).

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Family Opecoelidae Ozaki, 1925 Subfamily Plagioporinae Manter, 1947 Genus Macrourimegatrema Blend, Dronen & Armstrong, 2004 Macrourimegatrema gadoma n. sp. Syns: Genus novum B, species nova no. 2 of Armstrong (1974); Opecoelidae gen. n. B, sp. n. No. 2 of Bray (1995, p. 182, 184) Type-host: Gadomus arcuatus (Goode & Bean); Gadiformes: Macrouridae: Bathygadinae; doublethread grenadier. Type-locality: Northeastern Gulf of Mexico, 2738¢N, 8515¢W, depth 637 m, 23/vi/1971. Additional localities: Northeastern Gulf of Mexico, 2822¢N, 8631¢W, depth 710 m, 26/vi/1971; Caribbean Sea off Venezuela, 1253¢N, 6957.5¢W; depth 1,006–1,115 m, 19/vii/1970. Records: 1. Armstrong (1974); 2. Bray (1995); 3. Present study. Descriptions: 1,3. Sites of infection: Pyloric caeca; intestine. Type-material: BMNH holotype 2006.4.28.1, BMNH paratypes 2006.4.28.2–7, BMNH voucher (immature) 2006.4.28.8; TCWC symbiotype 3352.12. Prevalence: 11 of 16 host specimens (68.8% infected). Intensity: 4–154 worms/host specimen. Etymology: The specific designation refers to the genus of the fish from which specimens were collected. It is used as a noun. Description (Figs. 1–4) [Based on 9 specimens. Measurements and proportions are given in Table 1.] Body large, elongate, narrow, flattened dorsoventrally. Forebody short, pyriform to slightly attenuate. Hindbody slightly to deeply crenulate, occasionally ruffled, elongate with nearly parallel sides; posterior extremity rounded to truncate, 5,665–10,455 (8,530) long, separated from forebody by slight constriction. Tegument smooth. Pre-oral lobe absent. Oral sucker trumpet or funnel-shaped, terminal to ventroterminal with deep central

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Syst Parasitol (2007) 67:93–99 Figs. 1–4 Macrourimegatrema gadoma n. sp. from Gadomus arcuatus. 1. Composite drawing of adult, ventral view. 2. Composite drawing of male terminal genitalia, dorsal view. 3. Composite drawing of oo¨type region, dorsal view. 4. Drawing of paratype specimen with paired sac-like inflations and associated excretory ducts at the level of the pharynx, ventral view. Abbreviations: A, ventral sucker; C, caecum; E, egg; ED, excretory ducts; G, genital pore; J, ejaculatory duct; L, Laurer’s canal; M, Mehlis’ gland; MT, metraterm; O, ovary; R, seminal receptacle; S, seminal vesicle; T, testis; U, uterus; V, vitelline reservoir; VD, vitelline ducts and VF, vitelline follicles. Scale-bars: 1, 1,585 lm; 2, 150 lm; 3, 140 lm; 4, 420 lm

cavity extending into posterior portion of oral sucker forming hour-glass-shape. Ventral sucker slightly protuberant, bordered by puckered margin, subspherical, wider than long, close to anterior extremity in first third of body. Prepharynx very short or apparently absent. Pharynx muscular, oval, longer than wide. Oesophagus long, slightly sinuous in some individuals. Intestinal bifurcation overlapped by anterior margin of ventral sucker or immediately anterior to it. Caeca narrow, thick-walled with sides highly folded forming numerous outpockets or pouches, terminating blindly close to posterior extremity. Testes 2, smooth to slightly indented, oval to subspherical, tandem, median, almost contiguous to some distance apart, postequatorial, located near junction of middle and posterior thirds of body, intercaecal; distance between anterior margin of anterior testis and posterior extremity 37.7–50.2% (43.8%) of body length. Post-testicular region occupies posterior third of body. Cirrussac thin-walled, club-shaped to elongate, 3.4–7.7% (6.0%) [n = 8] of body length, extends posterior to ventral sucker by 45–250 (184). Seminal vesicle internal, winding, tubular, very convoluted and wider in basal portion. Ejaculatory duct long. Prostatic gland-cells well developed, surrounding ejaculatory duct and seminal vesicle with larger numbers of cells in posterior portion of cirrus-sac. Pars prostatica apparently absent or indistinct. Genital pore submedian, slightly sinistral, bifurcal or just prebifurcal, overlapped by anterior margin of ventral sucker or just anterior to it by 32–50 (41) [n = 2], surrounded by dark-staining cells. Ovary smooth to slightly indented, oval to transversely elongate, median, pretesticular, in

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middle third of body and far removed from ventral sucker and cirrus-sac; pre-ovarian space 3,390–5,420 (4,700) long. Seminal receptacle large, canalicular, bilobed, clavate to circular, submedian and dextral to midline of body, immediately pre-ovarian and either anterodorsal to or dorsally overlapping anterior margin of ovary. Laurer’s canal very convoluted, on opposite side of mid-line from majority of seminal receptacle; dorsal opening overlaps left caecum; numerous red-staining cells surround canal and its pore. Vitelline reservoir large, median to slightly sinistral, dorsal to and contiguous with anterior margin of ovary, 112–175 (150) [n = 5] · 55–155 (87) [n = 5]. Oo¨type immediately pre-ovarian and barely dextral to mid-line, slightly sinistral to seminal receptacle and level with anterior portion of vitelline reservoir. Uterus coiled, pre-ovarian, extends in narrow intercaecal band from ovary to ventral sucker, with distal portion passing ventral to cirrus-sac; space occupied by uterus 2,725– 4,800 (3,915) [n = 8] · 170–360 (275) [n = 8]; length of uterine field 34.7–49.5% (42.4%) [n = 8] of body length. Metraterm present, muscular. Vitellarium follicular, circumcaecal, removed from ventral sucker, beginning anteriorly at junction of first and second thirds of body, extending to posterior extremity, interrupted opposite gonads but occasionally only on 1 side of ovary or testis, confluent in pre-ovarian space, between anterior testis and ovary, and in intertesticular and post-testicular regions; vitelline follicles 25–80 (55) [n = 45] · 10–50 (25) [n = 45]. Eggs smooth, oval, yellow, nonfilamented, operculate. Excretory vesicle tubular, winding between testes, sinistral to posterior testis and dextral to anterior testis, terminating at or near level of ovary in 2 tiny arms; excretory ducts arising from anterior margin of vesicle, extend forward to or near level of pharynx where they expand terminally to form simple, sac-like inflations. Excretory pore subterminal.

Differential diagnosis The new species belongs to Macrourimegatrema within the Plagioporinae Manter, 1947 as defined

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by Blend et al. (2004) and Cribb (2005). Macrourimegatrema gadoma n. sp. can be distinguished from M. brayi, the type and only other species in the genus, by having: vitelline fields that are distinctly different in extent and distribution [they are posteriorly removed from the ventral sucker, beginning at the junction of the first and second thirds of the body, interrupted opposite the gonads and confluent in the pre-ovarian space vs extending posteriorly from, or very close to, the level of the posterior margin of the ventral sucker, not interrupted opposite the gonads and only slightly confluent in the immediate pre-ovarian space]; a body that is larger [6,275–11,100 vs 3,900–9,780 lm long]; gonads that are distributed over a slightly greater proportion of the body [present in the middle third of body, with the posterior testis extending into posterior third of body vs just postequatorial and entirely in the middle third of the body]; and caeca that are highly folded with sides forming numerous outpocketings or diverticula (Fig. 3).

Discussion In several specimens of M. gadoma n. sp., we observed excretory ducts that arose from the anterior margin of the excretory vesicle and that extended anteriorly to or near to the level of the pharynx, where they expanded terminally to form a pair of simple sac-like inflations (Fig. 4). We also observed this same feature in several specimens of M. brayi. While the current generic diagnosis of Macrourimegatrema is already unique (Blend et al., 2004) when compared to other opecoelid genera in the key to the Plagioporinae of Cribb (2005), we feel this feature may be of additional generic importance, since it was observed in both M. brayi and M. gadoma n. sp. It is also important to note that a few specimens identified as M. brayi (based on the extent and distribution of the vitellarium) were twice recovered from four specimens of Gadomus arcuatus (see Blend et al., 2004) in concurrent infections with M. gadoma n. sp. Because of the distinct differences, such as the extent and distribution of the vitelline fields, body size (Table 1) and position of the gonads relative to the entire worm as well as

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the small number of M. brayi found in G. arcuatus (intensity 1–2 worms) by Blend et al. (2004), we believe the two to be different species. M. brayi appears to be a common parasite of species of Bathygadus and to occur only occasionally in species of Gadomus; this species also exhibits a broader host range occurring in at least four macrourid species. M. gadoma was not found in species of Bathygadus, and it is only known to occur in one macrourid species, G. arcuatus. Of the 11 fish infected with M. gadoma, high intensities were observed with 4–154 worms per fish. The development of the worms recovered also varied; most of the specimens were immature individuals, but others were observed to be decomposing adults. Members of the macrourid subfamily Bathygadinae are not known to feed on fish; they have been found to feed on copepods, euphausiids and natantian decapod crustaceans, suggesting a preference for free-swimming, off-bottom prey (Cohen et al., 1990). Opecoelids are known to utilise either a crustacean or a fish as the second intermediate host (Bray, Littlewood, Herniou, Williams, & Henderson, 1999). The finding of a second species of Macrourimegatrema from a bathygadine host adds further evidence to the conclusion of Blend et al. (2004) that members of this genus within the deep sea probably infect their host via the ingestion of a benthopelagic crustacean. Acknowledgements The authors gratefully thank Dr John D. McEachran, Dr Kathryn Vaughan and Heather Prestridge, Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, Texas for assistance in identifying host fish and for providing us access to fish in their collections. We also thank Mrs. Eileen Harris, the Natural History Museum, London, UK for her assistance in depositing the type-material. We are grateful to the Tisch Library at Tufts University, Medford, Massachusetts for access to and use of their on-line literature database.

References Armstrong, H. W. (1974). A study of the helminth parasites of the family Macrouridae from the Gulf of Mexico and Caribbean Sea: Their systematics, ecology and zoogeographical implications. PhD Thesis, Texas A&M University, 329 pp.

Syst Parasitol (2007) 67:93–99 Blend, C. K., Dronen, N. O., & Armstrong, H. W. (2004). Macrourimegatrema brayi n. gen., n. sp. (Digenea: Opecoelidae) from four species of deep-sea macrourid fishes from the Gulf of Mexico and Caribbean Sea, with a list of endohelminths reported from species of Bathygadus and Gadomus (Macrouridae). Zootaxa, 566, 1–18. Bray, R. A. (1995). Annotated checklist of digenean parasites of Macrouridae (Teleostei, Gadiformes). Acta Parasitologica, 40, 168–192. Bray, R. A., Littlewood, D. T. J., Herniou, E. A., Williams, B., & Henderson, R. E. (1999). Digenean parasites of deep-sea teleosts: A review and case studies of intrageneric phylogenies. Parasitology, 119, S125–144. Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. Cohen, D. M., Inada, T., Iwamoto, T., & Scialabba, N. (1990). Gadiform fishes of the world (Order Gadiformes). An annotated and illustrated catalogue of cods, hakes, grenadiers and other gadiform fishes known to date. FAO Fisheries Synopsis, No. 125, 10. Rome: FAO, 442 pp.

99 Cribb, T. H. (2005). Family Opecoelidae Ozaki, 1925. In A. Jones, R. A. Bray, & D. I. Gibson (Eds.), Keys to the Trematoda. Volume 2 (pp. 443–531). Wallingford: CABI Publishing and the Natural History Museum. Froese, R., & Pauly, D. (2006). FishBase. World Wide Web electronic publication (http://www.fishbase.org). Gibson, D. I., & Bray, R. A. (1982). A study and reorganization of Plagioporus Stafford, 1904 (Digenea: Opecoelidae) and related genera, with special reference to forms from European Atlantic waters. Journal of Natural History, 16, 529–559. Gibson, D. I., & Bray, R. A. (1984). On Anomalotrema Zhukov, 1957, Pellamyzon Montgomery, 1957, and Opecoelina Manter, 1934 (Digenea: Opecoelidae), with a description of Anomalotrema koiae sp. nov. from North Atlantic waters. Journal of Natural History, 18, 949–964. Pritchard, M. H. (1966). A revision of the genus Podocotyle (Trematoda: Opecoelidae). Zoologische Jah¨ kologie und rbu¨cher (Abteilung fu¨r Systematik, O Geographie der Tiere), 93, 158–172. Yamaguti, S. (1971). Synopsis of digenetic trematodes of vertebrates. Volume I. Tokyo: Keigaku Publishing Co., 1,074 pp.

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