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The World of Protozoa, Rotifera, Nematoda and Oligochaeta

Henlea

Henlea Michaelsen, 1889 (ref. ID; 1257, 3692)

Family Enchytraeidae (ref. ID; 1257, 1928, 5971, 6650)

ref. ID; 1923

Setae simple pointed and usually straight, spermathecae open between segments 4/5 or 3/4 and 4/5. Usually whitish in appearance and seldom more than 25 mm in length. Setae arranged in 4 bundles per segment. Esophagus expanding abruptly into the intestine. (ref. ID; 1923)

ref. ID; 5783

Henlea was defined by Nielsen and Christensen (1959) as comprising those species of enchytraeids with: Setae straight or slightly bent, unequal or equal in size within the bundle; nodulus absent. Head pore at 0/1. Dorsal pores absent. Oesophagnus expanding abruptly into the intestine (possibly with the exception of ... Hepatogaster...). Peptonephridia absent but oesophageal appendages present in VI or IV + VI. Intestinal diverticula present or absent. Nephridia with well developed intestinal tissue. The dorsal vessel arises in the anteclitellar region. Blood colourless. The brain is slightly longer than wide and more or less incised posteriorly. Lymfocytes [sic] uniform in size and shape (discoid to slightly oval). Seminal vesicle absent. Egg sac absent. Spermathecae simple, usually without glands and diverticula ... the ental ducts unite before the attachment to the oesophagus. Individually, none of these characters uniquely distinguishes the genus. Some, such as well-developed nephridial tissue, are characteristic of the entire family. However, if the states of these same characters were resolved, some distinguishing characteristics for Henlea may be found. Even characters that are homoplasious, as presently resolved within the Enchytraeidae (Coates 1989), could be diagnostic for Henlea if its sister-taxon shared a character state with the immediate outgroup to Henlea and its sister, but not with Henlea. The identity of the sister-taxon of Henlea is not known; however, some of the genera suggested as being closely related to it Buchholzia Michaelsen, 1886, Bryodrilus Ude, 1892 (Cernosvitov 1937), Punahenlea Nurminen, 1980, and Aspidodrilus Baylis, 1914 (Coates 1990), and comparisons with these may prove phylogenetically illuminating. Species in Henlea, its possible sister-taxa, and other enchytraeid genera, have multisetate bundles. However, many Henlea species have distinctly unequal setae within one bundle arranged so that the inner setae of the bundle are progressively shorter. A comparable arrangement of unequal setae within a bundle is not found in the sister-taxa and is otherwise recorded only for species of Fridericia Michaelsen, 1889, Marionina tubifera Nielsen and Christensen, 1959, and Marionina dirksi Bell, 1942. In Fridericia species, setae of equal length are disposed pairwise within a bundle, whereas they are not symmetrically paired in species of Henlea or Marionina. In addition, the classification of several species of Marionina obscures phylogenetic relationships because Marionina is polyphyletic (Coates 1989) and some species may be as closely related to species of Henlea as to any other species of Marionina s.l. Thus, the setal length distribution within a bundle that is found in Henlea species could uniquely characterize this taxon. Henlea also includes some species with bundles of setae of equal length, which may be plesiomorphic. The presence of oesophageal appendages is also not unique to Henlea. However, we know of no species in other genera that have rather diffuse oesophageal appendages extending along the gut through several anterior segments, such as are found in Henlea species. According to Stephenson (1930) "the form of the peptonephridia [oesophageal appendages] in the genus is characteristic - irregular tubes often branching, closely applied to the oesophagus and in intimate relation to the dorsal vessel and blood-sinus, without open mouth, situated in the regions of segments V and VI". In their discussion of the genus, Nielsen and Christensen (1959), do not emphasize the unique form of these organs and details of the form of the appendages are not included in the generic description. According to Nielsen and Christensen (1959), "some species" also have separate, unpaired dorsal and ventral appendages appendages in IV; however, the few records we have found are all for a single species, H. nasuta. The form of these elongate oesophageal appendages seems to be truly distinctive for the genus. Unfortunately, descriptions of Henlea species made more recently than the revision by Nielsen and Christensen (1959) rarely include any details of the structure of the oesophageal appendages, and even their presence may not be positively indicated. A detailed reexamination of the elongate oesophageal appendages found in Henlea species could help to substantiate the monophyly and distinctiveness of the genus and differentiate species, some of which may be characterized by dorsally and ventrally paired appendages. It remains to be determined whether the oesophageal appendages found in IV in H. nasuta are just extensions of the usual elongate appendages or are indeed separate structures. If separate, they are reminiscent of the oesophageal appendages described for Buchholzia, although in that taxon the appendages are laterally paired, whereas in H. nasuta they are dorsal and ventral. Henlea (Nielsen and Christensen 1959) includes species with a variety of forms of diverticula originating at a marked anteclitellar expansion of gut. In earlier revisions of the genus (Stephenson 1922, 1930; Cernosvitov 1937), three or four subgenera or genera were recognized for the nominal species of Henlea with different types of intestinal diverticula: Henleanella Friend, 1913 for species without diverticula, Henlea Michaelsen, 1889 for species with two pairs of diverticula, Michaelseniella Cernosvitov, 1934 for species with one pair of diverticula, and Hepatogaster Cejka, 1910 for species with diverticula comprised of masses of branched tubules, possibly with several posterior opening into the gut. Gut diverticula are found in species of other genera of enchytraeids, including Buchholzia, Guaranidrilus Cernosvitov, 1937, and Aspidodrilus but the diverticula of each taxon differ in details of structure and (or) location. The possibility remains, however, that gut diverticula with a multitubular substructure, as found in Henlea, Buchholzia, and Aspidodrilus, is a shared synapomorphy and thus that tubular substructure of the intestinal diverticula is pleisomorphic for Henlea. To date, characters of Henlea have not been used to uniquely distinguish the taxon from other species-groups in the Enchytraeidae. Many of the species of Henlea must be reexamined and our understanding of the phylogeny of the Enchytraeidae improved before a better diagnosis of the genus can be made. The characters of Henlea, taken as a whole, place this group of species among the more highly derived enchytraeid taxa, usually with the spermathecae attached to the oesophagus and complex glandular-muscular structures at the male pore. A revision of the genus awaits resolution of synapomorphies of the taxon and a corroborated phylogeny of the species. (ref. ID; 5783)
  1. Henlea californica Eisen, 1904 (ref. ID; 5783)
  2. Henlea californica monticola Eisen, 1904 (ref. ID; 5783)
  3. Henlea dicksoni (Eisen) (ref. ID; 1928)
  4. Henlea dicksonia (Eisen, 1878) (ref. ID; 1257)
  5. Henlea diverticulata Cejka, 1912 (ref. ID; 5971)
  6. Henlea ehrhorni Eisen, 1904 (ref. ID; 5783)
  7. Henlea eiseni Bell, 1942 (ref. ID; 5783)
  8. Henlea glabra Altman, 1936 (ref. ID; 5783)
  9. Henlea glandulifera Nurminen (ref. ID; 6567)
  10. Henlea helenae Eisen, 1904 (ref. ID; 5783)
  11. Henlea heleotropha Stephenson, 1922 (ref. ID; 5783)
  12. Henlea hibernica Southern, 1907 (ref. ID; 1928) or 1909 (ref. ID; 1257)
  13. Henlea irkutensis Burow, 1929 (ref. ID; 3692)
  14. Henlea moderata Welch, 1914 (ref. ID; 5783)
  15. Henlea moderatoidea Altman, 1936 (ref. ID; 5783)
  16. Henlea nasuta (Eisen, 1878) (ref. ID; 1257, 5783) reported year? (ref. ID; 1928)
  17. Henlea ochracea (Eisen, 1878) (ref. ID; 5783)
  18. Henlea perpusilla Friend, 1911 (ref. ID; 1257, 5783, 5971, 6650)
  19. Henlea scharffi Southern, 1910 (ref. ID; 5783)
  20. Henlea similis Nielsen & Christensen (ref. ID; 6913)
  21. Henlea stolli Bretscher, 1900 (ref. ID; 3692)
  22. Henlea tubulifera Welch, 1914 (ref. ID; 5783)
  23. Henlea udei (Eisen, 1904) (ref. ID; 5783)
    Syn; Bryohenlea nuda Bell, 1962 (ref. ID; 5783)
  24. Henlea urbanensis Welch, 1914 (ref. ID; 5783)
  25. Henlea ventriculosa (d'Udekem, 1854) (ref. ID; 1257, 1928, 3692, 5783) reported year? (ref. ID; 1928, 4491)
  26. Henlea welchi Bell, 1942 (ref. ID; 5783)
  27. Henlea yukobnensis Tynen & Coates, 1991 (ref. ID; 5783 original paper)

Henlea diverticulata Cejka, 1912 (ref. ID; 5971)

Descriptions

Segments 57 and 59. Setae straight with ental hook, and of unequal length within the bundles. Septal pattern 1,2-1,2: 1,2-1,2. Brain not incised posteriorly, lateral margins parallel. Three pairs of primary septal glands. Chloragogen cells dark brown. Cutaneous and clitellar glands irregular and indistinct. Dorsal blood vessel originates in X. Blood colorless. The lymphocytes are regular discoidal and light brown granular in appearance. Nephridia with a small nephrostome and a large postseptale. Sperm funnel 3/4 times as long as body width at the clitellum. Spermathecae attached to the esophagus by a common ental duct. A cluster of glands at the ectal opening and prominent diverticula exactly as described and figured by Cejka. Four hollow pulsating esophageal diverticula in VII. Sudden expansion in IX and four intestinal diverticula in IX also. These two specimens had the dorsal blood vessel originating in X, although Cejka lists it as starting in VII. The dorsal vessel in Henlea is known to pulsate along most of its length and a counting error could have arisen in this way. Cejka collected his specimens from the New Siberian Islands. We found it only in the mountain site at Chaun Bay. (ref. ID; 5971)

Henlea hibernica Southern, 1907 (ref. ID; 1928) or 1909 (ref. ID; 1257)

Diagnosis

This species is closely related to H. nasuta. The chief differences are the following. H. hibernica; two oesophageal glands in the 8th segment, leaving the 7th segment unoccupied; dorsal vessel rises in the 9th segment, and has three contractile swelling in segments 8, 7, and 6; duct of spermatheca is half total length; setae of anterior ventral bundles 5-9. H. nasuta; two glands in the 7th segment, just behind the last pair of septal glands; dorsal vessel rises in the 8th segment, and has two contractile swelling in segments 7 and 6; duct of spermatheca is only quarter total length; setae 4-7. (ref. ID; 1928)

Henlea nasuta (Eisen, 1878) (ref. ID; 1257, 5783) reported year? (ref. ID; 1928)

Descriptions

This specimen was very dark, each segment having several rows of irregular glands. (ref. ID; 1928)

Henlea perpusilla Friend, 1911 (ref. ID; 1257, 5783, 5971, 6650)

Descriptions

Length 7.4 mm (fixed), 8.5 mm (living); segments 36. Chaetae 2-7 per bundle. Clitellum over XII-1/2XIII, with gland cells irregularly arranged. Posterior of brain slightly incised. Three oesophageal appendages, dorsal pair short and unbranched, ventral piece branching into two long twigs. No intestinal diverticula. Dorsal vessel originating in posterior of VIII. Sperm funnels cylindrical, 2-3 times as long as width. Spermathecal ampullae spindle-shaped, without glands at ectal pore. (ref. ID; 6650)

Remarks

Adults at Magadan had a mean segment count of 29 (n=12, SD 3.1). The individuals at the Chaun Bay mountain site appeared to have more segments, but too few adults were encountered. This places this population toward the lower end of the range given by Nielsen and Christensen (1959); otherwise, it has the usual specific characteristics. The 2X and 4X cytotypes described by Nielsen and Christensen (1959) were both present. Found at Magadan and Chaun. At Magadan it occurred in bog, old stream bank, lowland larch, and riparian birch sites. At Chaun it occurred in the mountain site. (ref. ID; 5971)

Material examined

One whole mount and two live specimens from T7. (ref. ID; 6650)

Henlea yukobnensis Tynen & Coates, 1991 (ref. ID; 5783 original paper)

Descriptions

  • External: Body tapering from clitellum to prostomium and over posterior 7 or 8 segments; cream to greyish, no red blood, 2 or more eggs; very sluggish and "fat". Cuticle thick, 11-11.5 µm over most of body, including clitellum many-layered, 7 or more lamina visible, fibre layers rotated at 90 degrees to adjacent layers, with "pores" through fibre matrix. With dorsal groove across short prostomium. Head pore large, at or just anterior to 0/1. Spermathecal pore at 4/5, in midlateral line, pore surrounded by glandular epidermal ring. Clitellum thick but single-layered, over XII and XIII; no regular arrangement of gland cells into transverse rows; gland cells sparse between male pores. Male pores ventral in XII, visible as small depressions on laterally paired, protruded papilla, papilla of each side delimited by anterior and posterior transverse grooves; female pores in or just posterior to 12/13, slightly protruded, just medial to position of male pores. Postclitellar segments with pronounced intrasegmental groove, most distinct in segments anterior to those with protruding setae. Rarely with a few small, straight, single ventral setae in some of IV-IX, just barely protruding from epidermis (seen only in sections), length about 68 µm; with ventral and ventrolateral setal bundles in 2 or 3 posterior segments, some of (XLVIII)XLIV, XLV, and XLVI(XLVII-XLIX), bundles with 3, rarely 2, setae, middle seta of posterior bundles about the size of anterior setae, outer setae thicker and about 240 µm long. Pygidium 2.5-3 times as long as preceding segments; anus terminal, with tetrapartite aperture, anal canal cross-shaped in transverse section. (ref. ID; 5783)
  • Internal: Brain not obviously incised posteriorly. Dorsal blood vessel bifurcates anterior to brain. Coelomocytes discoid, of regular shape and size, about 40-58 µm (n=7, average 49.3) maximum diameter, granular. Pharyngeal glands diminishing in size from 4/5 to 6/7; narrowly connected dorsal to gut in 4/5, dorsal lobes of 5/6 and 6/7 reduced, not connected across gut, small separate ventral lobes in IV. Septa 5/6 to 7/8 strongly muscularized. Spermathecae paired; total length from pore to union with gut about 1.3-1.5 times body diameter at V, no diverticula, ectal duct nearly 100 µm in diameter, ampulla only about 1.2-1.5 times wider than ectal duct by with thinner, less muscular wall. Ectal duct with pronounced muscular layer, inner canal wall horizontally "pleated" around diameter just ectal to ampulla; with compact, basally fused, multicellular ectal glandular rosette. Sperm heads embedded in walls of ampulla. Spermathecae connecting across top of gut, common ental duct with diameter about 75-85 µm, connecting dorsally with gut in posterior of V, ental canal ciliate. Two pairs of tubular, spongy oesophageal appendages, paired dorsally and ventrally, extending along oesophagnus from just anterior to 4/5, about beginning of ciliated part of gut (i.e., just posterior to pharynx), to 7/8 at anterior of gut diverticulum; in VI and VII ventral appendages may fill up to half of coelom; dorsal and ventral appendages with short, irregular extensions of tissue into coelom; oesophageal appendages with integral blood sinuses. Interstinal diverticulum originating at 8/9, surrounding gut, tubular, digitate subdivisions extending anteriad from origin, each subdivision with ciliate canals. Developmentally (?) paired condition apparent in lateral regions. With abrupt widening of gut just posterior to origin of intestinal diverticulum; posterior to clitellum, gut changes from wide and linear to sinuous. With 3 pulsating expansions of dorsal blood vessel in VII-IX, becoming progressively larger anterior to posterior; dorsal blood vessel origin in IX. Nephridia with efferent ducts originating anteriorly on postseptal part and with preseptal part including some of canal. Anterior nephridia from 6/7. Sperm sac surrounding gut dorsally and laterally; extending from 10/11 to anterior of X, simply an extended section of the highly folded septum at 10/11. Egg sacs not extending much beyond one-half XI (extensions of 11/12) or one-half XIII (extensions of 12/13). As many as 2 mature eggs. Sperm funnel collar wide, convoluted; canal of funnel eccentric; funnel about 3-5 times as long as wide; about 1.3 times as long as body diameter at XI. Vas deferens long and irregularly coiled, diameter about 16 µm throughout most of length, slightly wider near sperm funnel. Vas deferens penetrating penial bulb somewhat posteriorly and dorsolaterally, then running anteroventrally through bulb to small male pore. Penial bulb glands well-developed, bounded laterally by longitudinal muscular layer and with lateral dorsoventral muscular insertions; minute epidermal invagination at male pore. Female funnel and duct more or less embedded in 12/13. (ref. ID; 5783)

    Notes

    The new species has clear affinities with Henlea as defined by Nielsen and Christensen (1959), viz. an abrupt widening of the gut demarcating the oesophagnus from the intestine; intestinal diverticula at this junction; anteclitellar origin of the dorsal vessel, which contains colourless blood; coelomocytes uniform in size and shape; oesophageal appendages; spermathecae lacking diverticula on ampulla and uniting before joining gut; setae of unequal size within a bundle. However, the worm departs in some ways from Nielsen and Christensen's (1959) description. The paucity of setae seen in H. yukonensis, though unusual for the genus, has been reported previously. The reduction of setal numbers and numbers of bundles is also found in species of several other genera of Enchytraeidae. The presence of sperm sacs and egg sacs in H. yukonensis presents a more complex problem. There is apparent confusion in recent literature as to what constitutes a sperm sac or seminal vesicle and, as a result, confusion in determining their presence or absence. Henlea species are reported to lack seminal vesicles (Nielsen and Christensen 1959). In describing Bryohenlea nuda, a synonym, for Henlea udei, Bell (1962) notes the presence of seminal vesicles. Holmquist (1968), who proposed the specific synonym, redescribes H. udei from some of the original material (Eisen 1904) and notes that seminal vesicles are absent. She appraises this difference between her observations and those of Bell as not of taxonomic importance and as "presumably being due to a displacement of ... septa" (Holmquist 1968, p.152) in material examined by Bell. Earlier Stephenson (1930) had differentiated two types of sperm-containing sacs found in enchytraeids. One of these he calls seminal vesicles and the other testis sacs. In microdriles, the seminal vesicles are described as simple pouchings of the septa enclosing the testis-bearing segments. Could these be the same as those recognized by Holmquist as displaced septa but not as seminal vesicles? Seminal vesicles in the Yukon worm match Stephenson's (1930) description. Testis sacs, found in species of Lumbricillus and Enchytraeus, are described by Stephenson (1930) as sacs that enclose the testes but exclude the sperm funnel. Stephenson suggests that the peritoneal layer, derived from the testis itself, forming the membrane of the testis sac must rupture before spermatozoa can enter the funnel and thus become available of transfer during copulation. Gametes released by the rupture of the testis sac might then be contained in a seminal vesicle. In Lumbricillus spp. each testis is cut up into lobes and each lobe is surrounded by a membrane. These is some evidence that whole testis lobes may be transferred to the spermathecae during copulation (Tynen 1969). Division of the testes and testis sacs was not seen in the Yukon worm. Stephenson (1930) also observed, as we have, that the extent of the seminal vesicles or sperm sacs may depend only upon the quantity of sperm they contain at the time of examination. Also, the amount of sperm produced may vary not only over time but from individual to individual. It has been noted that sperm sacs and the contained spermatozoa are not always easily seen in living or unstained mounted material. Such preparations have been the sole basis of many modern (post- 1959) species descriptions. Distended septa at 11/12 and 12/13 that form eggs sacs also vary with reproductive state. It is doubtful whether a characteristic showing the kind of temporal variation known for sperm sacs has unambiguous diagnostic value. The presence of seminal vesicles was used by Nurminen (1980) to distinguish Punahenlea from Henlea, but our investigations do not support that distinction. The new species described here is clearly better classified with Henlea, both because of its other characteristics and because Punahenlea is not a well-diagnosed taxon. Variation in the state of the seminal vesicles should not be ignored, however, nor is it taxonomically meaningless. More critical and specific definition of states of the character will help delimit the information inherent in the variation we now recognize. For example, in some species of Marionina Michaelsen, 1889, abundant sperm morulae float freely in several anterior segments and there is no distension of the septa of the segment containing the testes, whereas in most species without seminal vesicles, sperm are confined to XI. Within the morphological species Lumbricillus lineatus (Muller, 1774), which includes genetically isolated polyploids (?species), the amount of sperm produced and the degree of seminal vesicle development are often clear indications of ploidy level (Nielsen and Christensen 1959). There is possibly a case for placing the Yukon worm in a distinct subtaxon, Hepatogaster, including all North American and Siberian species of Henlea having intestinal diverticula comprised of numerous tubular components; however, many of these species are poorly known and a taxonomic revision of Henlea would be premature. The Yukon worm is placed instead in Henlea s.l., and Nielsen and Christensen's (1959) definition is adjusted slightly to include species lacking setae on several segments and having seminal vesicles. Among the few species of Henlea with composite tubular gut diverticula, the new species most like H. udei (Eisen, 1904), also known from the western North American Arctic. These two differ significantly in the form of their spermathecae as well as in the locations of the intestinal diverticula and dorsal blood vessel origins. In H. udei both these locations are reported to be one segment posterior to the usual locations for Henlea species, including H. yukonensis. The spermathecae of H. udei, in contrast to those of H. yukonensis, have very long, narrow ectal ducts and large saccate ampullae, extending somewhat beyond V and uniting with the oesophagus between VI and IX (Eisen 1904; Bell 1962; Holmquist 1968). There are also fewer glands at the ectal spermathecal pore of H. udei. In addition, the oesophageal appendages seen in H. udei are dilated and protrude markedly into the coelom of VI and no anterior septa are muscularized. Notable similarities between the two species are the reduction of setae, both in numbers per bundle and numbers of bundles, and the relatively thick cuticle. The judge from an illustration made by Holmquist (1968), the cuticle in at least one location on the body of H. udei is about 10 µm thick, compared with 11 or 11.5 µm found in various body areas of H. yukonensis. (ref. ID; 5783)

    Etymology

    For its geographic location: thus, Henlea of the Yukon. (ref. ID; 5783)

    Type locality

    Richardson Mounans, Yukon Territory, 65 degrees 45'N, 136 degrees 20'W (site 1), collected August 1985 by C.A.S. Smith; from the F. H. or Ah soil horizon. (ref. ID; 5783)

    Type slide

  • Holotype: ROMIZ (Royal Ontario Museum, Invertebrate Zoology) I1439, 1 mature specimen, anterior 14 segments sectioned longitudinally, on 11 slides, posterior segments sectioned transversely, on 19 slides. (ref. ID; 5783)
  • Paratypes: ROMIZ I1440, 1 mature specimen, anterior segments sectioned transversely, on 12 slides, posterior part in fluid; ROMIZ I1441, 3 very mature, 10 maturing, and 3 immature specimens in ethanol; from the F, H, and Ah soil horizon at site 1. (ref. ID; 5783)

    Measurements

    Living specimens about 10-60 mm long (fixed, 8-27 mm); 42-44 (6 specimens), 50-53 (12 specimens, 54 (1 specimen) segments; diameter of contracted fixed specimens 1.5-2.5 mm (n=22, average 1.9). (ref. ID; 5783)