Helobdella lineata (Verrill, 1874) Albemarle

Sawyer, Roy T., 2024, Biology, morphology and taxonomy of a snail-feeding leech from North Carolina, USA, provisionally identified as Helobdella lineata (Verrill, 1874) (Glossiphoniidae): First evidence for extra-oral digestion in the Hirudinea, Zootaxa 5453 (2), pp. 151-182 : 162-164

Description of Helobdella lineata

External features

A single adult specimen (HL-5A) is selected as being representative of the snail leech indigenous to the Albemarle region ( Fig. 4 ). The following description of this relatively large individual (12.8 mm) (representing pigment variant #1) is supplemented by observations on eleven additional specimens collected at the same location (HL-5) in Pasquotank County. These twelve cohorts are remarkably homogeneous in size (9.8–12.8 mm), and state of feeding (empty gut) and reproduction (not gravid). External variability is based on examination of the additional 392 specimens of this species collected throughout the Albemarle region during this study .

Typical of H. lineata , all twelve individuals in the archetype series had quickly faded in the preservative with the consequence that pigmentation is generally lost. The pigment pattern described in this section is based primarily on additional specimens photographed in life (HL-24, HL-26)( Fig. 6 ) or recorded at time of capture.

Size Inexplicably, the three largest individuals of H. lineata (18.5, 16.5 and 15.5 mm, respectively) collected in the 12 years of this study came from precisely the same locality, namely Williams Mill Pond in Wayne County (HL-6). In contrast, the leeches collected in the rest of the Albemarle region were significantly smaller (mean, 7.2 mm; range, 2.2–12.5 mm; N = 63), with exception of one large individual (15.5 mm) collected in a diked canal in Tyrrell County (HL-15A).

Body shape Living individuals of H. lineata are generally flat.At rest they are widest in the posterior third of the body, and the head and oral sucker are somewhat rounded, not pointed. Interestingly, preserved individuals change body shape, becoming noticeably more narrow and rounded after preservation.

The reference specimen (HL-5A) is straight (12.8 mm) and well preserved but its pigment has faded entirely ( Fig. 4 ). Consequentially, the proboscis (length, 2.8 mm) and atrium are prominent landmarks visible through the translucent body wall. The maximum body width (3.3 mm) is located toward the posterior end of the body at about segment XIX. From this point the body narrows anteriorly slightly to about segment XI. From here the body narrows increasingly to the oral sucker (width, 0.8 mm). The distance from the atrium (male gonopore) to the tip of the oral sucker is 3.8 mm, and the width of the body at the male gonopore is 2.1 mm.

Gravid and brooding individuals are recognisable because the lateral margins of the body curve downward and inward to form a slight protective cavity. This swells the line of the mid-body.

Oral sucker and mouth Dorsally the oral sucker is almost indistinguishable from the rounded head. From a ventral perspective, however, the oral sucker is clearly outlined as a broad triangular rim (0.5 x 0.9 mm).

The mouth of H. lineata differs from most other glossiphoniids in being a conspicuous slit located noticeably closer to the centre of the oral sucker than to the sucker apex. This peculiar anatomy probably reflects the unusual feeding habits of this snail-feeding leech. In this context, it is proposed that the open slit functions as a distensible jaw, capable of receiving the relatively large proboscis when the latter is everted ( Fig. 12A ). In fact, as discussed elsewhere, the proboscis can expand further upon imbibing fluid from a pre-digested snail. Structure of the mouthproboscis complex of this species is of considerable taxonomic significance and contrasts with the small pore located very near the apex of the oral sucker as found in the sanguivorous allied species, H. ghilianii (pers. obs.).

Mouth-like slits occur in virtually all specimens of this species collected in the Albemarle region and is considered a non-variable character for taxonomic purposes. Most individuals have closed slits, but the mouth of the reference specimen (HL-5A) is slightly open to reveal a puckered inner lining. Open slits are found in a few other individuals (for example, HL-13A, HL-15A).

Eyes As a rule H. lineata has two and only two well-separated eyes ( Fig. 9A,B ). This is also the case for the sympatric congener species H. stagnalis and H. elongata , and is considered characteristic of the genera Helobdella (Blanchard, R. 1896) and Haementeria ( Filippi, 1849) ( Sawyer, 1986, 654). In this context the reader is referred to an informative study on the underlying genetics, development and evolution of Helobdella eyes (Kwak, et al. 2023).

The reference specimen has no visible eyes, as is the case for many of the faded specimens in this collection but in a comparable specimen (HL-15A) a single pair of well-separated eyes lies in the posterior part of segment III (i.e. on annulus III (a2+a3) ( Fig. 10B ). Functionally, the distance between the eyes is variable in H. lineata but they never adjoin at the midline. A previously unreported observation in Helobdella is that when the relatively large proboscis is everted the distance between the eyes adjusts spatially. In other words distance between eyes is maximal when the proboscis is everted ( Fig. 9A ), unlike when the proboscis is at rest, internally ( Fig. 9B ). In contrast the eyes of a sympatric turtle leech P. multilineata coalesce physically at the mid-line and are not moveable relative to each other ( Fig. 9C ). The immutability of the distance between eyes in the turtle leech may be attributable in part to the lack of need for spatial adjustment required by its long slender proboscis in P. multilineata (pers. obs.).

Caudal sucker The caudal sucker of the reference specimen (HL-5A) is almost circular (1.5 mm). In lateral view the posterior end of the body has a pronounced concave curve to meet the caudal sucker. This curve rides high over the centre of the sucker such that upon dorsal view only a small portion (0.24 mm) of the caudal sucker is exposed. This peculiar, somewhat humped, configuration may reflect the state of contents of the underlying large rectum.

Annulation In the reference specimen annuli of the neck region are irregularly sub-divided in keeping with extensibility of the neck ( Figure 10B ). On the other hand annuli of the mid-body region are more evenly expressed, but these too are occasionally subdivided. Often in some specimens (HL-5G) the subdivision is in the posterior third of the annulus rather than in the middle. In other words annular subdivision is an incompletely expressed (variable) character in H. lineata .

Incompletely expressed subdivision of annuli also occurs in the two sympatric congener species, H. stagnalis and H. elongata ( Fig. 3B,C ). As a variable character in all three clades annular subdivision is taxonomically unreliable and should not be used to define these or closely allied forms of Helobdella . In this context several ‘species’ of Helobdella and even allied ‘genera’ have been defined in terms of subdivided annuli, for example, H. scutifera , H. longicollis and H. diploides ( Siddall & Borda, 2003; Ringuelet, 1978).

Figures

FIGURE 3. Three co-existing species of Helobdella indigenous to the Albemarle region of the Outer Banks, North Carolina. A, H. lineata, the subject of this paper, photographed in life, pigment and papillar pattern intact (HL-26); B, H. stagnalis (sensu lato) (Hst-1A); C, H. elongata (HE-2A). Scale bar: 1.0 mm.

FIGURE 4. The archetype or reference specimen (HL-5A) on which the description of H. lineata is based. This specimen has faded and become translucent following preservation with 5% formalin. The type locality is in Pasquotank County, NC [36.191176, -76.228516] A, dorsal view. B, ventral view. Abbreviations: a, atrium; cs, caudal sucker; ic, intestinal caecum; pc, post caecum; pr, proboscis; r, rectum; rb, rectal bladder; sv, seminal vesicle; tp, tip of proboscis. Scale bar: 1.0 mm.

FIGURE 6. Variation in dorsal pigmentation and papillation in H. lineata. Two individuals collected from the same location. A, (HL-4), lightly pigmented with metameric spots. B, (HL-26), darkly pigmented with metameric spots. By far the majority of individuals throughout the Albemarle region were lightly pigmented with metameric white dots as illustrated in A. Note: pigmentation disappeared quickly after preservation making the specimen translucent. Abbreviations: b, brooding depression on ventral side; e, eye; m, medial stripe; p, posterior crop caecum; rectum; pa, papilla; ws, metameric white spot. Scale bar: 1.0 mm

FIGURE 9. Taxonomic significance of eyes of Helobdella compared to Placobdella. A, B, Helobdella lineata; C, Placobdella multilineata. A, Distance between eyes is maximal when the proboscis (pr) is everted. B, When the proboscis is retained internally the eyes are closer together. C, In the turtle leech P. multilineata the eyes coalesce physically at the mid-line and are not moveable relative to each other. Furthermore, each apparent ‘eye’ of P. multilineata on each side is composite, being comprised of a larger anterior eye and a smaller posterior eye. Scale bars: A, B, 0.3 mm; C, 0.1 mm.

FIGURE 10. Evidence that the neck region of H. lineata is capable of extending and swelling (see section on feeding biology). A, proboscis everted; B–D, proboscis at rest, i.e. not everted. A (HL-9D), neck region narrows (white arrow) when proboscis is extended; B (HL-15A), annulation of the neck region at rest is more subdivided than annuli in mid-body region; C (HL-13A), ventral nerve cord (blue) between ganglia VIII–IX and IX–X is characteristically sinuous (black arrow) when individual is at rest. D (HL-13A), single salivary ductules are sinuous (black arrow) within the proboscis when individual is at rest. Abbreviations: co, circumpharyngeal commissure (brain); sd, single salivary ductule (brown); sb, salivary bundle (brown). Scale bar: 10 mm.

FIGURE 12. Terminal structure of the proboscis of H. lineata at increasing magnifications. A (HL-9L), ventral view. Everted proboscis showing unusually large mouth; tip of proboscis with circular array of lobules; the proboscis and its lumen widens near the tip. B, C, salivary ductules and close-up of lobules at the proboscis tip; D, salivary pores with secretions at tip of proboscis. Abbreviations: lu, lumen of proboscis; lt, lobule of tip of proboscis; mo, mouth; os, oral sucker; ot, opening of tip of proboscis; sd, salivary ductule; sp, salivary pores at tip of proboscis. Scale bars: A, 1.0 mm; C, 0.1 mm.