Alboglossiphonia levis, Gouda, Hanaa A., 2010

Gouda, Hanaa A., 2010, A new Alboglossiphonia species (Hirudinea: Glossiphoniidae) from Egypt: Description and life history data, Zootaxa 2361, pp. 46-56 : 47-53

Alboglossiphonia levis n. sp.

Holotype: 7 mm long and 3 mm wide specimen from Al-Sont canal, Assiut, Egypt. BM (NH) 2007. 66–68. deposited in the British Museum (Natural History), London.

Paratypes: Five specimens from the same locality; three dissected and two sectioned are deposited in The Educational Museum for the Egyptian Fauna ( DEMEF), Assiut University, Department of Zoology. Code number: 1A1H1194.

Etymology: levis is Latin for smooth, due to the absence of papillae on the surface of the leech body.

Diagnosis: Greenish in color, sluggish. Both dorsal and ventral surfaces of the body were smooth without papillae. Three pairs of eyes, diffuse salivary cells, gonopores separated by two annuli and 4 pairs of testisacs. Proboscis stout, seven pairs of crop caeca, anus opened dorsally at the furrow between annuli 72/73 leaving one annulus behind.

Description:

Body shape ( Figs. 1 –3): Body ovate-lanceolate, dorsum arched, venter flat. Head with nuchal constriction ( Fig. 1 b), anterior sucker was cupuliform with thickened margin; proboscis pore small and opened in the centre of the sucker. Posterior sucker small, circular; its diameter less than one third of maximum body width and directed ventrally. Preserved specimens; 5 to 8 mm long and 2 to 3 mm wide.

Color and pigmentation ( Fig.1 a): Ground color greenish with deep green chromatophores arranged in irregular pattern dorsally. Venter appeared much lighter in color.

Annulation ( Fig. 2 a): The total number of annuli was 73 from the dorsum. I uniannulate and comparatively large, II uniannulate, III triannulate, there was nuchal constriction on IV/V. IV–XXV completely triannulate. XXVI biannulate and XXVII uniannulate.

Eyes ( Figs.2 b–f): Three pairs, first pair coalesced medially in IV, eyes of the second and third pairs are widely separated from each other, but eyes of consecutive pairs are coalesced at the furrow IV/V. Beside the normal pattern in fig. 2b (about 70% of examined leeches), there were different ocular patterns ( Figs. 2 b–f).

Papillae: Both dorsal and ventral surfaces of the body smooth and without papillae, except for some minute salivary papillae found in the hollow of the anterior sucker.

Gonopores (Figs. 3a, 5a): Male pore at a 3 XI /a 1 XII and female pore at a2 /a 3 XII. Gonopores are separated by two annuli.

Digestive system ( Fig.2 a): Proboscis pore small and found in the centre of the anterior sucker; proboscis cylindrical, stout and relatively short, in relaxed specimens reaches to four complete somites length. Esophagus short and straight, about two segments in length (XIII–XIV), no esophageal organ. Salivary cells are diffused from XI to XV. Crop extended from XV to XIX; seven pairs of crop caeca; first six pairs from XV to XVIII are bilobed, directed laterally and confined to their respective somites. The seventh pair in XIX is elongated, deflected posterior and lateral to the intestine reaching to XXIII; each with several secondary lobes. Intestine with four pairs of unlobed lateral intestinal caeca from XX to XXII. Hind gut saccate, rectum narrow, tapering into anus which opened dorsally at furrow XXVI/XXVII, leaving one annulus in behind

Reproductive system (Figs. 3a, b). Male: Four pairs of testisacs which are intersegmentally arranged at XIII/XIV to XVI/XVII. These testisacs could only be clearly detected in serial longitudinal sections (Fig. 3b). Vas deferens looped; ejaculatory ducts extended forward, then, both cornua united to form the atrium that opened finally into the male pore at XI a 3 / XII a1.

Female: Two thin-walled ovisacs, extending in brooding specimens posteriorly to XIX. Both ovisacs united anteriorly into a relatively elongated atrium which ended to the female pore at a2/a 3 XII.

Life history ( Figs. 4–5 ). Reproductive activity in Alboglossiphonia levis is externally marked by swelling of the tissues surrounding the gonopores forming opaque, white and dome shaped elevations around both male and female gonopores ( Fig. 5 a). In the laboratory, A. levis was found to be semelparous, it reproduced only once before death. In the field, it could be collected, only, from December to February where the canal water was shallow since it hidden within the mud of the bottom. It was observed that many of the leeches, collected from the field, were carrying embryos during the three months; December, January and February. The number of eggs within the transparent ovisacs ranged from 13 to 25. Fertilized eggs are deposited individually, each attached to the parent's venter by the attachment organ, later, they develop into hatchlings attached to the parent’s venter by their posterior suckers.

FIGURE 3. Alboglossiphonia levis n. sp. a) Ventral dissection showing reproductive systems in situ; mouth opening (m), anterior sucker (as), male gonopore (mg), atrial horn (h), ejaculatory duct (ej), vas deferens (vd), four pairs of testisacs (t1–t4), female gonopore (fg), oviduct (od), ovisac (o), posterior sucker (ps); b) Longitudinal section through the mid-body region showing testisacs (t1-t4). Scale bar = 1 mm.

Copulation: In the laboratory, copulation couldn’t be detected but groups of mature leeches (15–40) were aggregated together; the dorsal body surface of the leech was covered by the ventral surface of the other.

Laying egg ( Fig. 4 a): In the laboratory, leeches that could lay eggs were 2.7 mg wet body weight (mean), while those in the field were 4.2 mg wet body weight. Fertilized eggs could be easily seen within the thin delicate ovisac through the transparent body wall. Before laying egg, the leech searched for a hard substrate as a stone, snail’s shell or even the wall of the jar and attached to it by its anterior and posterior suckers. Behind the anterior third of the body, the parent widened and had thin lateral margins which inflected downwards and inwards, forming a trough around the coming eggs to protect them. The anterior third of the body raised and constricted. Eggs were deposited individually; each egg was attached by a thin, flexible, transparent and short cord ( Fig. 5 b). The diameter of the deposited egg was 250 μm (mean). The scanning electron microscopy revealed that egg’s surface was wrinkled with numerous minute pores ( Figs. 5 b, c). Laying egg occurred at intervals, each one lasted some minutes, after which the parent rested for another minutes, then continued to lay the following egg. The eggs were arranged on the parent’s venter filling the region behind the gonopores and in front of the posterior sucker. Water current passed over the embryos on the parent’s venter by undulating ventilator movements of the lateral edges of the brooding leeches ( Figs. 4 a, b). Laying eggs lasted about one to two days depending on the number of eggs laid (13– 25 eggs), affected by the amount of food and water temperature. While food was supplied in sufficient amounts during all stages of the experiment (ad libitum), the temperature was the factor affecting the reproduction. It was observed that during the egg laying period, the greater number of eggs (25 eggs) was laid at 28o C, while the lesser number (13 eggs) was laid at 16o C.

Hatching ( Figs. 4 b–d): Hatching occurred within ten to fifteen days after laying eggs (depending on the water temperature). Rounded eggs changed into more elliptical embryos, which developed attachment organs ( Figs. 5 d, e) used to adhere themselves to the ventral body wall of the parent. They remained there, digested their own reserves of yolk and developed into hatchlings attached to the parent’s venter by their posterior suckers, until their final liberation (after another four weeks); the anterior ends were extended free for searching food. The hatchlings had well developed eyes, suckers and digestive tract. Green pigment cells could be easily observed through the transparent body wall. Thus, the young were ready to feed their first meal. Hatchlings body weight were about 1–1.2 mg before taking their first post embryonic feeding. Just before laying egg, the parent stopped feeding and stayed resting till hatching, when the digestive tract and posterior sucker of the hatchlings developed and attached to the parent’s venter, then the parent searched for preys to feed its hatchlings.

Parental care: The parent incubated the fertilized ova within its trough - like venter till hatching. During this period the brooded parent stopped feeding, moving, attached to the substrate and remained quiescent till hatching. The hatchlings attached to the parent’s venter by their posterior suckers while the rest of the body moved freely. After hatching, the parent started to crawl and search for prey, especially Tubifex sp. and small Allolobophora sp. (60 x 3 mm which was available only at shallow waters; where the present leeches could be found). Then, the parent attached itself on the prey’s body by its posterior sucker and closed its venter to enable its attached hatchlings of ingesting the body fluids of the prey by their proboscis. The ingested food was easily observed within the crop caeca through the transparent body wall of the hatchlings. It was observed that the young remained attached to the parent's venter for another four weeks after hatching, although these young are independent in their feeding. This resulted in much larger size of the young when they left their parent.

Figure 6. Light photograph for feeding behavior showing 7 predatory leeches (arrowheads) feed on the annelid prey (asterisk). Note the reddish fluid within the gut of the fed leech (arrow).

Feeding Habit: In the laboratory, Alboglossiphonia levis was found to be a liquidosomatophagous predatory leech; in which the proboscis sucked up body fluids and soft parts of the prey. It was noticed that A. levis was able to feed on any of the prey provided as gastropods namely: Bulinus sp., Physa sp., Limnaea sp. and Theodoxus sp., or the annelids Allolobophora sp. and Tubifex sp. although, the latter was preferred to the leech (Fig. 6). The brooding leeches which carried eggs didn't feed at all till hatching and seemed quiescent and attached to the jar's wall. A. levis is moved by inchworm crawling when they were hungry or carrying young. The latter behavior is considered, a foraging behavior, for searching prey to feed its young; as a part of the parental care. In laboratory studies the young were noticed clinging upside down, for a little time, by their anterior and posterior suckers, just below the water surface, moving in this manner, since they could not swim. This behavior happened after young left the parent and before they met the prey. In the laboratory, feeding habit of young after they left their parents was similar to that of the adult.

Ecological Observations: A. levis was collected from December to February, from Al-Sont canal; a highly polluted drain in Assiut city, where water was shallow and there was an increase in its preys: The annelids ( Tubifex sp. and Allobophora sp.), gastropods ( Bulinus sp., Limnaea sp., Bellamya sp. and Theodoxus sp.). Also, some rotifers and a considerable number of arthropods as Daphnia sp., Cyclopidae , could be observed. The mean of various ecological parameters was recorded weekly as follows: The total dissolved salts (TDS): 155 ppm, pH: 6.8 and water temperature was 22o C. In this drain, juvenile, mature and brooding mature A. levis were observed in considerable numbers. Other leeches were found with A. levis : Alboglossiphonia polypompholyx Oosthuizen , et al., 1988, Batracobdelloides tricarinata (Blanchard, 1897) , Helobdella conifera (Moore, 1933) , Helobdella stagnalis (Linnaeus, 1758) , Babronia assiuti Hussein and El- Shimy, 1982 and Salifa delicata (Moore, 1939) . A. levis was often sluggish, found on stones and snails’ shells when they are satiated or carrying eggs and moved by inchworm crawling when they were hungry or carrying young. It was noticed that A. levis was negatively phototropic, tending to be on the undersides of plastic sheets, in the umbilicus of snails’ shells and within mud away from the light. During rearing, some of the brooding A. levis were found to be attacked by the oomycete Saprolegnia hypogyna Pringsheim (1874) leading to the death of these leeches.

Figures

FIGURE 1. Alboglossiphonia levis n. sp. a) A Dorsal view of a newly fed leech with its normal pigments; b) A fixed specimen (holotype) showing: anterior sucker (as), eyes (e), crop (cr), crop caeca (1 – 7), intestine (int), intestinal caeca (1 – 4), posterior sucker (ps). Note the nuchal constriction (arrows) in (b).

FIGURE 2. Alboglossiphonia levis n. sp. a) Dorsal dissection showing digestive system in situ; proboscis (pr), salivary cells (sc), esophagus (es), crop (cr), crop caeca (1 – 7), intestine (int), intestinal caeca (1 – 4), rectum (r), anus (a); b – f) Different ocular patterns, the normal pattern is (b).

FIGURE 4. Alboglossiphonia levis n. sp. Life cycle showing: Brooding parent with different developmental stages of progeny; a) Fertilized eggs newly deposited each of which individually attached to the parent's venter; b) The embryos became elongated and still attached to the parent's venter; c) After 10 days of laying eggs the hatchings (h) attached to the parent's venter by their posterior suckers (arrowheads); d) One-month old young showing: Eyes (e), digestive tract (dt). Note the undulating lateral edges of the brooding parent (arrows) in a, b) to make a respiratory current for the incubated embryos. Scale bar = 1 mm.

FIGURE 5. Scanning electron micrographs showing: a) male (mg) and female (fg) gonopores at maturity; b) A newly deposited fertilized egg, note its thin membrane with numerous minute pores (arrowheads) and its terminal delicate cord by which the egg is attached to the parent's venter (arrows); c) A higher magnification of (b) showing the thin membrane of the fertilized egg with some minute pores (arrowheads); d, e) One-week old embryo. Note the attachment organ (arrowheads).