The deep-sea fish digenean genus Tellervotrema Gibson & Bray, 1982 (Opecoelidae: Plagioporinae): Re-evaluation of the type species, T. armstrongi Gibson & Bray, 1982 and T. beringi (Mamaev, 1965) Author Blend, Charles K. Author Dronen, Norman O. Author Gardner, Scott L. Author Racz, Gabor R. Author Armstrong, Howard W. text Zootaxa 2012 3295 1 29 journal article 10.5281/zenodo.208704 3abcbac8-1a03-48b0-bc46-a27cb2097a13 1175-5326 208704 Tellervotrema beringi ( Mamaev, 1965 ) ( Figs. 4–7 ) Synonyms: Plagioporus beringi Mamaev, 1965 . Hosts: Albatrossia pectoralis (Gilbert) ; Gadiformes : Macrouridae : Macrourinae ; giant grenadier. Coryphaenoides sp.; Gadiformes : Macrouridae : Macrourinae . Localities: A. pectoralis : Northeastern Pacific Ocean, 44°25'N , 125°07'W , depth = 1,530 m , 14/August/1964 . Coryphaenoides sp.: Northeastern Pacific Ocean, 44°38'N , 125°25'W , depth = 2,800 m , 20/February/1964 ; 44°38'N , 125°50'W , depth = 2,800 m , 30/December/1963 . Site: Intestine. Deposited Specimens: Collector JEM, HWML neotype 49709 ( 1 adult [McCauley ID # OTB-42-F-1-11]), HWML paraneotypes 42665 ( 19 adult ), HWML vouchers 42665 ( 2 adult & 6 immature); Collector JEM, HWML paraneotypes 42743, 42855 ( 2 adult ). Prevalence: Coryphaenoides sp.: 2 of 2 host specimens (100% infected). Intensity: Coryphaenoides sp.: only 1 specimen found in each fish. Mean intensity: Coryphaenoides sp.: 2 worms in 2 specimens or 1 worm/infected fish. Relative density/abundance: Coryphaenoides sp.: 2 worms in 2 specimens or 1.0 worm/total fish examined. Records: 1. Mamaev (1965) ; 2. Yamaguti (1971) ; 3. Gibson & Bray (1982) ; 4. Bray (1995); 5. Blend (1996) ; 6. Present study. Descriptions: 1, 6. Redescription. [Based on 22 specimens . Measurements and proportions are given in Table 3 .] Body elongateoval, clavate or lanceolate, widest postequatorially; some individuals slightly hour-glass-shaped with narrowing of body around equatorial level. Forebody attenuated anteriorly, narrowing at bifurcal level. Hindbody rounded posteriorly and wider than forebody. Tegument smooth. Pre-oral lobe absent. Oral sucker subspherical, subterminal (terminal in a few specimens). Ventral sucker sessile, spherical to subspherical, wider than long in most specimens, larger than oral sucker, postbifurcal, preequatorial and located near junction of anterior and middle thirds of body. Prepharynx quite short. Pharynx muscular, elongate oval, majority wider than long. Oesophagus with tegumental lining, straight in most specimens (67%) while sinuous in others (33%). Intestinal bifurcation short distance anterior to ventral sucker. Caeca narrow yet distal ends can be inflated, unbranched, with thickened walls, running posteriorly along lateral sides of worm to end blindly near posterior extremity; ends of caeca arcuate in some individuals. FIGURES 4–7. Tellervotrema beringi (Mamaev, 1965) from the giant grenadier, Albatrossia pectoralis . 4. Whole specimen, ventral view. 5. Composite drawing of male terminal genitalia, ventral view. 6. Cirrus-sac showing straight distal portion running anterior to ventral sucker, dorsal view. 7. Cirrus-sac showing markedly curved distal portion running anterior to ventral sucker, ventral view. Abbreviations: C, cecum; E, egg; EJ, ejaculatory duct; EP, excretory pore; GP, genital pore; M, metraterm; OS, oral sucker; OV, ovary; P, pharynx; PP, pars prostatica; SV, seminal vesicle; T, testes; U, uterus; V, vitelline follicles; VS, ventral sucker. Scale-bars: 4, 550 µm; 5, 230 µm; 6, 200 µm; 7, 460 µm. Testes 2, tandem, irregularly indented to deeply lobed, transversely elongate, median, intercaecal, postequatorial, contiguous (91%), rarely separated (9%). Post-testicular region fairly sizeable, occupying posterior third of body. Cirrus-sac thin-walled, distinctly elongate in anterior portion, clavate to pyriform in shape, extending from point midway between left lateral body edge and midline in a long and either nearly straight or markedly curved posterodextral line beyond anterior margin of ventral sucker to overlap 1/5 to 3/4 length of ventral sucker, terminating well posterior to level of intestinal bifurcation near midline. Seminal vesicle bipartite; posterior portion saccular; anterior portion tubular, narrow, looping back and ventrally overlapping posterior portion before passing anterosinistrally in long straight line from near midline of worm to enter distal portion of cirrus-sac, which itself either continues anterosinistrally or turns sharply anteriorly over left cecum at level of intestinal bifurcation to proceed anteriorly to terminate in small, subcircular genital atrium. Prostate gland-cells well developed, numerous in cirrus-sac. Pars prostatica conspicuous and just anterior to or dorsally overlapping anterior margin of ventral sucker; narrow ejaculatory duct and cirrus present. Genital pore submedian, sinistral, midway between body margin and midline but can be either nearer to lateral margin or nearer to midline in some individuals, at level of intestinal bifurcation but can reach level of posterior oesophagus, preacetabular and closer to ventral sucker than oral sucker. TABLE 3. Dimensions of Tellervotrema beringi (Mamaev, 1965) from Coryphaenoides sp. and from Albatrossia pectoralis collected off the coast of Oregon. Parasite T. beringi T. beringi n 2 20 Host Coryphaenoides sp. Albatrossia pectoralis Source of data HWML 42743 & 42855 1 HWML 49709 & 42665 1 Collector & fixation McCauley, host AFA injection McCauley, host AFA injection Length 2,540–2,960 (2,750) 1,680–3,440 (2,524) [n = 18]2 Width at pharynx 356–405 (381) 316–599 (476) [n = 19] at VS 567–802 (685) 591–1,004 (751) at PT 543–786 (665) 664–1,269 (931) [n = 19] Forebody l2 851–891 (871) 608–1,288 (862) [n = 19] Hindbody l 1,689–2,069 (1,879) 1,072–2,369 (1,637) [n = 19] Oral sucker (OS) l 216–272 (244) 148–308 (246) [n = 19] w2 244–260 (252) 164–332 (247) [n = 19] Prepharynx l 16–36 (26) 0–80 (27) [n = 19] Pharynx l 124–148 (136) 76–168 (117) [n = 19] w 96–108 (102) 124–192 (153) [n = 19] Oesophagus l 220–316 (268) 162–592 (328) [n = 17] Ventral Sucker (VS) l 276–332 (304) 260–462 (350) [n = 19] w 276–389 (333) 284–567 (375) [n = 19] Cirrus-sac (CS) l 336–412 (374) 264–632 (443) [n = 19] w 136 (136) 100–256 (161) [n = 19] CS overlap VS 52–122 (87) 112–360 (211) [n = 17] Ejaculatory ductw 26 [n = 1] 6–24 (14) [n = 17] in distal CS Genital pore to lateral margin 124–184 (154) 68–288 (175) [n = 17] Pre-ovarian region l 1,360–1,460 (1,410) 1,045–2,000 (1,478) [n = 19] Ovary (OV) l 180–192 (186) 60–204 (124) w 232–332 (282) 164–344 (256) continued next page Parasite T. beringi T. beringi TABLE 3. (continued) VS to OV 236–243 (240) 128–559 (297) [n = 19] Vitelline follicles l 56–100 (70) [n = 10] 42–98 (66) [n = 92] w 28–50 (39) [n = 10] 16–56 (31) [n = 97] Vitelline reservoir l 94–128 (111) 60–136 (86) [n = 18] w 58–100 (79) 80–180 (119) [n = 18] Uterus l 745–778 (762) 575–1,134 (853) w 180–332 (256) 296–548 (420)

w 316–454 (385)	365–745 (567)
Post-uter- ine	l 1,158–1,540 (1,349)	551–1,420 (980) [n = 19]
region (PUR)
Anterior testis (AT)	l 132–244 (188)	120–320 (203)

Posterior testis (PT)	l 156–340 (248)	160–340 (246)
w 256–336 (296)	280–524 (425)
AT to PT	44–92 (68)	0
Post-testicular	l 689–800 (745)	211–810 (522) [n = 19]
region (PTR)	w 437–720 (579)	583–1,0 37 (766) [n = 19]
Post-caecal region	l 146–340 (243)	89–405 (241) [n = 17]
Egg	l 88–96 (92) [n = 10]	80–102 (93) [n = 90]
Excretory vesicle	w 52–60 (55) [n = 10] l 1,458 [n = 1] w 36–56 (46)	40–56 (48) [n = 84] 851–1,240 (1,024) [n = 3] 10–52 (24) [n = 5]
Forebody %3	30.1–33.5 (31.8)	27.3–38.8 (34.3) [n = 18]
Sucker width ratio OS:pharynx width ratio	1.1–1.5 (1.3) 2.4–2.5 (2.5)	1.2–2.0 (1.5) [n = 18] 1.2–2.0 (1.6) [n = 19]
Oesophagus %3	8.7–10.7 (9.7)	8.3–17.8 (12.9) [n = 17]
VS to OV %3	8.2–9.3 (8.8)	7.1–20.0 (11.7) [n = 17]
PUR %3	45.6–52.0 (48.8)	32.8–49.6 (39.3) [n = 18]
Width at PT %3	21.4–26.6 (24.0)	25.9–51.3 (38.5) [n = 17]
PTR %3	27.0 (27.0)	12.5–38.5 (21.6) [n = 18]

1These specimens were collected by Dr. James M. McCauley (deceased), Oregon State University, and housed at the Harold W. Manter Laboratory (HWML) under these accession numbers. 2 l, length; w, width; mean (parentheses); number [n] of measurements indicated where different from [n] in column heading. 3 Proportion of body length. Ovary deeply 3- to 4-lobed and clover-leaf-shaped, flattened longitudinally in several individuals, median to submedian, intercaecal, immediately pretesticular, contiguous with anterior testis, postequatorial in posterior portion of middle third of body. Oötype located anterodorsal to ovary. Seminal receptacle canalicular, anterosinistral and dorsal to ovary. Laurer's canal opening proximate to left cecum. Vitellaria follicular, circumcaecal, circular or elongate oval or globular in shape, extending posterolaterally from level anterior to intestinal bifurcation to posterior extremity; interruption in vitelline field approximate to ventral sucker variable in number (0, 1 or 2 gaps), symmetry (gaps directly opposite ventral sucker, oblique to ventral sucker, or displaced longitudinally to near level of gonads) and location (near body margin or displaced medially to near midline of worm), producing two paired, non-confluent, isolated patches of vitelline follicles extending from prebifurcal level to region spanning distance between ovary and posterior margin of ventral sucker; remainder of vitelline follicles running posterolateral to ovary and testes, not confluent but encroaching somewhat in to immediate preovarian region, space between ovary and anterior testis and in to intertesticular area, completely confluent in posttesticular region. Vitelline reservoir elongate oval to subtriangular, median to submedian, dorsally overlapping anterior margin of ovary or immediately anterosinistral to it. Vitelline ducts overlap lateral margins of uterus, ovary and anterior testis. Uterus winding, intercaecal and filling up almost entire space between ovary and ventral sucker, proximal loops running anteriorly from ovary and narrowing over ventral sucker, distal loop turning anterosinistrally to terminate at genital pore. Metraterm straight, distal end noticeably curved toward genital pore in a few individuals, thin-walled, weakly developed, longitudinal fibers evident along wall. Eggs smooth, oval, slightly collapsed or crenulated in some specimens, yellow, non-filamented, operculate, with conspicuous knob or boss on one pole. Excretory vesicle tubular, I-shaped, thin in width, reaching to ovary along midline of worm. Excretory pore dorsal, subterminal, opening via a small sphincter; dark-stained cells surrounding pore. Remarks: Based on the same combination of diagnostic characteristics given above, these specimens key out to the genus Tellervotrema within Plagioporinae ( Gibson & Bray 1982 ; Cribb 2005 ). We also have identified those individuals of Tellervotrema collected from A. pectoralis and Coryphaenoides sp. as T. beringi . As far as we are aware, there exists only one published description of T. beringi - the brief type description, given in Russian and originally named Plagioporus beringi by Mamaev (1965) , who found intensities of 2–34 of these worms parasitizing seven individuals of Coryphaenoides sp. from the Bering Sea. Gibson & Bray (1982, p. 550–551) gave a brief list and table of features used to distinguish T. armstrongi from T. beringi , including in the latter species a larger egg size (100–110 × 50–60 µm vs 50.6–64 × 24–35 µm), a smaller sucker width ratio (1:1.4 vs 1:1.6–2.1), a more posteriorly situated genital pore (opening at the level of intestinal bifurcation vs opening at the level of about 30% of the distance between the intestinal bifurcation and the pharynx), a more posteriorly-extended cirrus-sac and lateral gaps in the vitelline fields (cirrus sac reaches the rear edge of the ventral sucker and the vitelline gap is near this same level vs a cirrus-sac that is entirely anterior to or only reaches to the middle of the ventral sucker and the vitelline gap is at midacetabular level) and T. beringi possesses entire (smooth) rather than irregularly lobed testes. In almost all of these features as well as in overall appearance, our specimens described herein more closely match T. beringi than T. armstrongi . Also, the type host ( Coryphaenoides sp.) and locality (Bering Sea) for T. beringi is more similar to the hosts ( Coryphaenoides sp. and A. pectoralis ) and locality (Pacific Ocean off Oregon) of our specimens; T. armstrongi is known primarily from macrourids of the genus Nezumia from the North Atlantic Ocean. Finally, these particular specimens possess a conspicuous knob or boss on one pole of the egg ( Fig. 17 ), described by Mamaev (1965) as a “носик” or “little nose, spout or bill” (Shporkin pers. comm.). This feature is also apparent on the eggs of our specimens of T. armstrongi and was noted by Armstrong (1974) on the egg of “ Plagioporus sp. n. #1”; however, this knob or boss was not mentioned in Gibson & Bray (1982) , probably because their material contained collapsed or severely distorted eggs. There are a few minor differences between the type description of T. beringi and our specimens (see Table 3 ). Tellervotrema beringi was described and illustrated by Mamaev (1965, Fig. 1 ) as possessing in-part the following characteristics: a short prepharynx; large and smooth testes; a vitelline gap at the level of the posterior margin of the ventral sucker; and a large egg (100–110 × 50–60 µm). Observations of our specimens of T. beringi revealed more variability in these features. Some individuals possessed a distinct, short prepharynx ( Fig. 4 ), yet we were not able to observe this feature in others (0–80 µm long). While the absence of a prepharynx may be the result of contraction, we were unable to locate this feature in several specimens of T. beringi that showed no sign of contraction and the apparent lack of a prepharynx was noticeable in 1/3 of the measured specimens parasitising A. pectoralis . The testes in our specimens were somewhat smaller (120–340 × 180–548 µm vs 360–380 × 750–780 µm) and irregularly indented to deeply lobed; we did not observe any that were smooth. This might reflect the plasticity of this character in this genus as testes texture varied in T. armstrongi from smooth to irregularly indented to lobed. Combining our observations with Mamaev (1965) , the testes texture of T. beringi varied from smooth to irregularly indented to deeply lobed (see Figs. 22–23 ). A third difference was the highly variable location of the vitelline gap which produced contrasting appearances in the Tellervotrema -like, paired, isolated, anterior vitelline groups. While we observed the presence of a vitelline gap at about the level of the posterior margin of the ventral sucker, the gap itself was quite variable in number (0, 1 or 2 gaps), symmetry (gaps directly opposite ventral sucker, oblique to ventral sucker, or displaced longitudinally to near level of gonads) and location (near body margin or displaced medially to near midline of worm) (see Figs. 11–16 ). Mamaev (1965) noted that almost all the trematodes of T. beringi that he found had the same gap within the vitelline field at the level of the ventral sucker, as seen in the “ type form” ( holotype ), yet in several “copies” ( paratypes or other specimens), he also noted that [they] did not have [this same pattern of vitelline follicles], indicative of the variability in the position of the vitelline gap. Finally, while the egg size of our specimens was smaller in length and barely overlapped that of the type measurement (80–102 µm vs 100–110 µm), the width of the egg was the same as in T. beringi (40–60 µm vs 50–60 µm) and the egg of our specimens of T. beringi was larger than that of T. armstrongi (50.6–64 × 24–35 µm [ Gibson & Bray 1982— Table 1 ] and 47.5–66 × 25–42 µm in specimens described herein). FIGURES 8–10. Circumcaecal vitelline follicles in a single specimen of Tellervotrema beringi (Mamaev, 1965) from the giant grenadier, Albatrossia pectoralis . 8. Photograph of vitelline follicles located ventral to cecum. 9. Photograph of cecum located directly dorsal to vitelline follicles in Fig. 8. 10. Photograph of vitelline follicles located dorsal to vitelline follicles and cecum in Figs. 8 & 9. Abbreviations: C, cecum; V, vitelline follicles; VS, ventral sucker. Scale-bars: 8–10, 110 µm. We noted some variability between our specimens of T. beringi from A. pectoralis and from Coryphaenoides sp. Most conspicuous are those characteristics in which there is little or no overlap in measurements or proportions between both sets of T. beringi specimens (see Table 3 ); however, we believe these differences to be attributable to intraspecific variability and minimized in importance when compared to the inherent intraspecific variability already noted by previous authors for T. armstrongi ( Gibson & Bray 1982 ) . For example, there was an apparent difference in inter-testicular distance (AT to PT) between those specimens of T. beringi from Coryphaenoides sp. (44– 92 µm) and from A. pectoralis (testes are contiguous). However, this species and T. armstrongi are known to have testes that can be either contiguous or that can be separated by a short distance. The distance that the cirrus-sac extended beyond the anterior margin of the ventral sucker in T. beringi also varied: 52–122 µm (1/5 to 1/3 ventral sucker length) in worms from Coryphaenoides sp. vs 112–360 µm (1/3 to 3/4 ventral sucker length) in worms from A. pectoralis . While variable (Δ = 55% of ventral sucker length), both sets of specimens are comparable to the variability in this same feature described by Gibson & Bray (1982) for T. armstrongi (cirrus-sac entirely anterior to (0%) or extending to 50% of ventral sucker length beyond anterior margin of ventral sucker). We discerned a difference in the length of the excretory vesicle between both sets of specimens of T. beringi (1,458 µm vs 851–1,240 µm). This can be attributed in-part to a very low number of observed measurements for this feature (n = 1 & n = 3, respectively) due to the gonads and, at times, the uterus occluding the view of the anterior extent of the excretory vesicle. Had more measurements been able to be obtained, this difference might have been nullified. The critical taxonomic importance of this feature in distinguishing Tellervotrema from other genera, the excretory vesicle extends to the level of the ovary ( Gibson & Bray 1982 ; Cribb 2005 ), was confirmed for both sets of specimens of T. beringi . Perhaps the least explainable difference in Table 3 was the oral sucker (OS) to pharynx width ratio (2.4– 2.5 vs 1.2–2.0). While there is overlap in the width of the oral sucker (244–260 vs 164–332), there is a difference in the width of the pharynx (96–108 µm vs 124–192 µm) between both sets of specimens. There is also a dissimilarity in the relationship of pharynx length to width between T. beringi from each host: 124–148 × 96–108 µm (length> width) vs 76–168 × 124–192 µm (width> length). The variability in these measurements may in-part explain the difference in OS:pharynx width ratio, but we remain uncertain as to the cause of this difference. We stress that the majority of all other dimensions measured, including egg size (see Table 3 ), between both sets of specimens of T. beringi overlapped in size and / or were practically identical to each other. Lastly, while one set of T. beringi had a low number of specimens (n = 2), these same specimens were collected from the type host genus ( Coryphaenoides ) and locality (North Pacific Ocean) as originally reported by Mamaev (1965) . To further support our analysis, more congeneric parasite material is needed from species of Coryphaenoides inhabiting the deep waters off Oregon and elsewhere in the North Pacific Ocean (i.e. Kuramochi 2001 , 2009 , 2011 ). FIGURES 11–14. Variability in number, symmetry and location of vitelline gap(s) in Tellervotrema beringi (Mamaev, 1965) from the giant grenadier, Albatrossia pectoralis . 11. Ventral view of horizontally symmetrical gaps (2; gaps indicated by arrows) at about level of posterior margin of ventral sucker producing Tellervotrema -like, paired, isolated, anterior vitelline groups. 12. Ventral view of 1 gap, located on left side at level of posterior margin of ventral sucker; no gap on right side. 13. Dorsal view of diagonally symmetrical gaps (2) at level of ventral sucker. 14. Ventral view of asymmetrical gaps (2) located oblique to ventral sucker; complete horizontal gap on right side (arrow) and incomplete gap on left side with medially-displaced vitelline follicles (bar). Abbreviations: C, cecum; O, oesophagus; V, vitelline follicles; VS, ventral sucker. Scale-bars: 11, 490 µm; 12, 575 µm; 13, 640 µm; 14, 500 µm. FIGURES 15–19. 15. Ventral view showing 0 vitelline gaps in specimen of Tellervotrema beringi (Mamaev, 1965) from the giant grenadier, Albatrossia pectoralis . 16. Ventral view of vitelline gaps (3) distributed randomly (diagonal gap running anterosinistral to ventral sucker; horizontal gap on right side just posterior to ventral sucker; horizontal gap on left side displaced longitudinally to level of testes) in specimen of T . beringi from Coryphaenoides sp. 17. Ventral view of eggs showing conspicuous knob or boss on one pole of each from specimen of T. beringi from A. pectoralis . 18–19. Ventral views of 4- and 3- lobed ovary from T. armstrongi Gibson & Bray, 1982 from the common Atlantic grenadier, Nezumia aequalis . Abbreviations: C, cecum; O, oesophagus; OV, ovary; T, testes; U, uterus; V, vitelline follicles; VS, ventral sucker. Scale-bars: 15, 600 µm; 16, 280 µm; 17, 80 µm; 18, 150 µm; 19, 100 µm. FIGURES 20–23. Variability in testes texture and position in species of Tellervotrema . 20. Smooth and barely separated testes in T . armstrongi from the common Atlantic grenadier, Nezumia aequalis , ventral view. 21. Slightly indented and separated testes in T. armstrongi from N. aequalis , ventral view. 22. Lobed and contiguous testes in T. beringi from the giant grenadier, Albatrossia pectoralis , ventral view. 23. Deeply lobed and contiguous testes in T. beringi from A. pectoralis , ventral view. Scale-bars: 20, 105 µm; 21, 400 µm; 22, 315 µm; 23, 280 µm. We were unable to provide ecological data (prevalence, intensity, mean intensity and relative density/abundance) for T. beringi in A. pectoralis . After investigating records at the HWML for Collection # 42665, we were unable to obtain data on the total number of specimens of A. pectoralis collected by JEM, the number of A. pectoralis infected with T. beringi , or the intensity of infection. As a result, we were unable to calculate mean intensity and relative density/abundance for this host species. We were unable to find in Mamaev (1965) any indication of what type specimens were deposited for T. beringi (as Plagioporus beringi ). Two of us (CKB & NOD) obtained a published list ( Mamaev 1975 ) of specimens housed at the Laboratory of General Helminthology (now the Laboratory of Parasitology) in Vladivostok, Russia , but T. beringi (listed as Plagioporus beringi , see p. 229 of Mamaev 1975 ), the type host, Coryphaenoides sp. and locality (Bering Sea), were all that was listed with no accession numbers. We then attempted to obtain type material by contacting the Laboratory of Parasitology in Vladivostok, Russia , where helminths of fish from the Bering Sea are housed and where Dr. Yu. L. Mamaev was curator. We were informed that the type specimens of P. b e r i n g i are believed to be lost (Ermolenko pers. comm.). Thus, we were neither capable of obtaining specimens for comparative examination nor able to acquire accession numbers for the type specimens of T. beringi . Because we are unaware of a holotype or other type materials for T. beringi , we have designated a neotype (HWML 49709 [McCauley ID # OTB-42-F-1-11]) to serve as the single, name-bearing type specimen for this species and assigned 21 additional adult specimens as paraneotypes (HWML 42665, 42743, 42855). This represents the first report of a species of Tellervotrema from the giant grenadier, A. pectoralis ; the only species in the macrourid genus Albatrossia Jordan & Evermann. This study also represents a new locality record (off Oregon) for Tellervotrema , a parasite genus that until now only has been documented in the Bering Sea ( Mamaev 1965 ) and off Japan ( Kuramochi 2001 , 2009 , 2011 ).