Onchidium typhae Buchannan, 1800

Dayrat, Benoit, Goulding, Tricia C., Apte, Deepak, Bhave, Vishal, Joseph Comendador,, Qua, ng, Ngo Xuan, Tan, Siong Kiat & Tan, Shau Hwai, 2016, Integrative taxonomy of the genus Onchidium Buchannan, 1800 (Mollusca, Gastropoda, Pulmonata, Onchidiidae), ZooKeys 636, pp. 1-40 : 7-17

Onchidium typhae Buchannan, 1800 Figs 3, 4, 5, 6, 7, 8

Onchidium typhae Buchannan, 1800: 132-134, plate V, figs 1-3; Stoliczka 1869: 90-103, plate xiv, figs 1-6.

Type locality.

“Bengal.” Bengal is a vast region of eastern India (and Bangladesh) around the delta of the Ganges. Collecting specimens in West Bengal was the best that could be done to try to go back to the type locality.

Type material.

The original type material could not be located and is likely lost. Given that the identity of Onchidium typhae is no longer problematic, there is no need to designate a neotype.

Additional material dissected.

Bangladesh, Sundarbans, delta, October 1927, 1 specimen [25/15 mm], leg. Konietzko, det. as Onchidium (ZMH 27506/2); India, West Bengal, Sundarbans, Bally, Datta River, 21°59.277'N, 088°45.213'E, 04 January 2011, 5 specimens (45/25 to 40/25 mm), leg. B. Dayrat & V. Bhave, [station 48, very narrow band of mud with a few sparse Avicennia trees, between the edge of the river and the walls protecting the village, no old logs since firewood is a precious resource] (BNHS); Sundarbans, Amlamethi Island, Bidyadhari River, 22°04.923'N, 088°41.882'E, 05 January 2011, 1 specimen (40/30 [DNA 1064] mm), leg. B. Dayrat & V. Bhave, [station 49, very soft mud on the shore with recently-planted Avicennia trees; uninhabited island] (BNHS); India, Andaman Islands, Middle Andaman, Rangat, Yerrata, Saban, 12°27.451'N, 092°53.792'E, 10 January 2011, 3 specimens (45/20 to 35/20 mm), leg. B. Dayrat & V. Bhave, [station 56, open, impacted mangrove patch by a creek, near village, with medium trees and old logs] (BNHS); Middle Andaman, Rangat, Shyamkund, 12°28.953'N, 092°50.638'E, 11 January 2011, 25 specimens (55/30 to 30/15 mm; 40/20 [DNA 1089] mm), leg. B. Dayrat & V. Bhave, [station 57, by a large river, deep mangrove with tall trees, small creeks, and plenty of old muddy logs, next to a road and a small cemented bridge for creek] (BNHS); Middle Andaman, Shantipur, Kadamtala, 12°19.843'N, 092°46.377'E, 12 January 2011, 25 specimens (65/30 to 30/20 mm; 40/20 [DNA 1109]), leg. B. Dayrat & V. Bhave, [station 58, open area with hard mud and many old logs, next to a mangrove with medium trees] (BNHS); South Andaman, Bamboo Flat, Shoal Bay, 11°47.531'N, 092°42.577'E, 13 January 2011, 7 specimens (50/35 to 40/25 mm), leg. B. Dayrat & V. Bhave, [station 59, open mangrove with medium trees, hard mud, old logs, next to a road and a small cemented bridge for creek] (BNHS); Malaysia, Peninsular Malaysia, Merbok, 05°39.035'N, 100°25.782'E, 12 July 2011, 1 specimen (35/24 mm), leg. B. Dayrat & T. Goulding, [station 21, deep Rhizophora forest with old, tall trees, hard mud, many small creeks and many old logs] (USMMC 00001); Langkawi Island, Tanjung Rhu, 06°25.771'N, 099°49.436'E, 13 July 2011, 2 specimens (60/35 [#1] and 27/18 mm), leg. B. Dayrat, [station 23, dense forest with young trees, a few creeks] (USMMC 00002); Langkawi Island, Tanjung Rhu, 06°25.317'N, 099°50.106'E, 15 July 2011, 2 specimens (45/40 and 27/17 [DNA 967] mm), leg. B. Dayrat, [station 26, open forest (mostly Rhizophora ) with high mud lobster mounds] (USMMC 00003); Peninsular Malaysia, Matang, off Kuala Sepatang, Crocodile River, Sungai Babi Manpus, 04°49.097'N, 100°37.370'E, 19 July 2011, 4 specimens (32/20 to 20/17 mm), leg. B. Dayrat & T. Goulding, [station 28, old and open Rhizophora forest with tall trees, hard mud, creeks, and many old logs] (USMMC 00004); Matang, close to the jetty, facing fishermen’s village on the other side of river, 04°50.154'N, 100°36.368'E, 20 July 2011, 18 specimens (42/24 [#1] to 28/18 [#2] and 15/10 [DNA 965] mm), leg. B. Dayrat & T. Goulding, [station 29, oldest and open Rhizophora forest of tallest and beautiful trees, with hard mud, many creeks, and many old logs] (USMMC 00005); Singapore, Semakau Island, 01°12.083'N, 103°45.585'E, 4 April 2010, 1 specimen (40/22 [DNA 1007] mm), leg. B. Dayrat & S. K. Tan, [station 8, artificial, landfill island with low and very dense newly-planted Rhizophora trees; muddy areas in between Rhizophora patches and coral rubble close to the shore] (ZRC.MOL.6396);, Lim Chu Kang, 01°26.785'N, 103° 42.531'E, 5 April 2010, 3 specimens (40/20, 38/22 [#1], and 19/10 mm), leg. B. Dayrat & S. K. Tan, [station 9, mangrove east of the jetty; open forest with medium trees and medium mud; ended on sun-exposed mudflat outside the mangrove with soft mud; very polluted with trash] (ZRC.MOL.6397).

Distribution

(Fig. 2). India: Bengal (type locality; Stoliczka 1869; present study), Andaman Islands (present study). Bangladesh (present study). Singapore (present study). Malaysia (present study).

Habitat

(Fig. 3). In West Bengal, Onchidium typhae was collected at both sites on soft mud, just next to the river (brackish water) and a few sparse Avicennia trees. In the Andaman Islands, it was collected directly on the mud, on the muddy surface (most often at the base) of tree trunks and roots, and on muddy old logs, inside old and deep mangroves with tall trees as well as more open muddy areas; it was also found on the cemented walls of small bridges (under a road next to mangrove). In Singapore, it was collected on muddy old logs. In Malaysia, it was most often found on muddy old logs and on muddy tree trunks and roots, as well as on the surface of the mud (especially that of mud lobster mounds). Onchidium typhae is a very cryptic species, especially when it is on the surface of the mud, and one needs to patiently look for it to find it, especially because it is rarely abundant (see below).

Abundance.

In the Sundarbans, Onchidium typhae was found in two of the four mangrove sites that were visited, but for a total of only six specimens. In the Andaman Islands, it was found in four of the five mangrove sites visited. The mangrove site where Onchidium typhae was not found was not at all muddy but rather, comprised a sandy patch of Avicennia by a coral rubble sandy beach. It was especially abundant at two sites (many specimens were observed but not collected), mostly on or near old logs. In Malaysia, Onchidium typhae was found in only five of the 18 mangroves that were visited and it was abundant (17 specimens collected) only at one site, which happens to be one of the best, oldest, most pristine, and most diverse mangrove forests we have ever seen anywhere. In Singapore, Onchidium typhae was found in three of the five mangroves that were visited (the two sites mentioned above, and one site by the Mandai River where one specimen was collected but ultimately escaped). However, it is rare there (only five specimens collected in total).

Color and morphology of live animals

(Fig. 4). Live animals are abundantly covered with mud and the color of their dorsum can hardly be seen at all. In fact, if it were not for their fecal pellets and their long ocular tentacles, they would be really difficult to find because they can be very cryptic. Once the mud is washed out, their dorsum is brownish, with no particular pattern. The color of the foot and of the hyponotum is important because it differs from the other species described here. The foot and the hyponotum vary from gray to yellow in color, and show sometimes even a greenish hue. The color of the foot and the hyponotum may or may not have the same color. It is remarkable that the color of the foot and of the hyponotum of a particular individual can change rapidly, especially when disturbed. The lateral sides of the foot remain dark grey. Distally, the long ocular tentacles are reddish brown. Proximally, they are darker brown and less reddish, speckled with many tiny white dots. The ocular tentacles are extremely long (easily 2 cm when the animal is undisturbed). The ocular tentacles of all Onchidium species described here are significantly longer than in other onchidiids, which is a useful character in the field to identify a slug as an Onchidium . The head is reddish brown to black, with many white dots evenly distributed.

When animals are not disturbed, the dorsum is typically covered by large pointed papillae that rest on larger, hemispherical bases. Those pointed papillae are unique to Onchidium and extremely useful for identification in the field. For a long time (before we realized those slugs were Onchidium in the strict sense), we called them the “spiky” slugs to refer to the unique pointed papillae. Those papillae may seem to be arranged in two to four longitudinal ridges (each with five to ten papillae), but this is not the rule. They bear from one to four black "dorsal eyes" at their tip but some papillae do not bear dorsal eyes (especially on the dorsum margin). As in many other onchidiids, there is a central peduncle entirely retractable within the notum. The central peduncle bears three or four "dorsal eyes" but its size is similar to the large pointed papillae (i.e., it is not significantly larger than the other large papillae). The large pointed papillae are surrounded by small papillae as well, which may be rounded or pointed. As soon as the animal is disturbed (by walking on the mud on which it crawls or by touching its dorsum), all dorsal papillae rapidly retract and the animal looks completely different. It then is evenly covered with minute pointed papillae. The body of disturbed animals also is more humped and their ocular tentacles are entirely retracted. One has to patiently wait for a long time for a disturbed slug to relax again (easily 10 or 15 minutes) so the rule is "take a picture first and then touch it!" Interestingly, the appearance of the dorsum of live, disturbed animals is very close to the appearance of preserved animals, which was quite useful when examining type materials of existing species and recognizing them as Onchidium species. Crawling individuals can easily measure 30 to 40 mm in length (largest individuals measured 65 mm).

External morphology

(Figs 5 A–C). Preserved specimens no longer display the distinct color traits seen in live animals. The color of preserved animals is meaningless and uninformative. The body is not flattened. The notum is elongated, occasionally oval. Dorsal gills are absent. The notum is evenly covered by papillae. Large papillae with hemispherical bases are typical for live animals but, in preserved animals, those papillae are pointier and smaller. These larger papillae are surrounded by even smaller papillae. As in live animals, papillae with so-called 'dorsal eyes’ are present. There is a central, retractable peduncle in the center of the notum, but it can only be seen in live animals in the field. The hyponotum is horizontal. The width of the hyponotum relative to the width of the pedal sole varies among individuals. The width of the hyponotum ranges from about 1/3 to 1/2 its total width, occasionally extending to 4/5 its total width. The anus is posterior, medial, close to the edge of the pedal sole. On the right side (to the left in ventral view), a peripodial groove is present at the junction between the pedal sole and the hyponotum, running longitudinally from the buccal area to the posterior end, a few millimeters from the anus and the pneumostome. The pneumostome is medial. Its position on the hyponotum relative to the notum margin and the edge of the pedal sole varies among individuals but averages in the middle. The position of the female pore (at the posterior end of the peripodial groove) does not vary much among individuals. In the anterior region, the left and right ocular tentacles are superior to the mouth. They are outside if specimens were relaxed before preservation. Otherwise they are retracted. Eyes are located at the tips of the ocular tentacles. Inferior to the ocular tentacles, superior to the mouth, the head bears a pair of oral lobes. On each oral lobe, there is an elongated bump, likely with sensitive receptors. The male aperture (opening of the copulatory complex) is inferior to the right ocular tentacle, slightly to its left (internal) side.

Visceral cavity and pallial complex

(Fig. 5D). Marginal glands (found in Onchidella ) are absent. The anterior pedal gland is oval and flattened, lying free on the floor of the visceral cavity below the buccal mass. The visceral cavity is not pigmented internally and not divided (the heart is not separated from the visceral organs by a thick, muscular membrane). The heart, enclosed in the pericardium, is on the right side of the visceral cavity, slightly posterior to the middle. The ventricle, anterior, gives an anterior vessel supporting several anterior organs such as the buccal mass, the nervous system, and the copulatory complex. The auricle is posterior. The kidney is more or less symmetrical, the right and left parts being equally developed. The kidney is intricately attached to the respiratory complex. The lung is in two left and right, equally-developed, more or less symmetrical parts.

Digestive system

(Figs 5 E–G, 6). There are no jaws. The left and right salivary glands, heavily branched, join the buccal mass dorsally, on either side of the esophagus. The radula is in between two large postero-lateral muscular masses. Each radular row contains a rachidian tooth and two half rows of lateral teeth of similar size and shape. Examples of radular formulae are: 58 × 73-1-73 in USMMC 00005 #1 (42 mm long), 58 × 65-1-65 in USMMC 00005 #2 (28 mm long), 53 × 80-1-80 in USMMC 00002 #1 (60 mm long), and 65 × 70-1-70 in ZRC.MOL.6397 #1 (38 mm long). The rachidian teeth are tricuspid: the medial cusp is always present; the two lateral cusps, on the lateral sides of the base of the rachidian tooth, are small and inconspicuous. Rachidian teeth tend to be about half the size of the lateral teeth (with a length of the rachidian tooth usually not exceeding 40 µm). The lateral aspect of the base of the rachidian teeth is straight (not concave). The half rows of lateral teeth form an angle of 45° with the rachidian axis. With the exception of the few innermost and few outermost lateral teeth, the size and shape of the lateral teeth do not vary along the half row, nor do they vary among half rows. The lateral teeth seem to be unicuspid with a flattened and curved hook with a rounded tip (the length of the hook is between 50 and 60 µm), but there also is an outer pointed spine on the lateral expansion of the base. In most cases, the basal lateral spine cannot be observed because it is hidden below the hook of the next, outer lateral tooth. It can only be observed when the teeth are not too close (such as in the innermost and outermost regions) or when teeth are placed in an unusual position. The inner and outer lateral aspects of the hook of the lateral teeth are straight (i.e., not wavy and not forming any protuberance).

The esophagus is narrow and straight, with thin internal folds. The esophagus enters the stomach anteriorly. Only a portion of the posterior aspect of the stomach can be seen in dorsal view because it is partly covered by the lobes of the digestive gland. The dorsal lobe is mainly on the right. The left, lateral lobe is mainly ventral. The posterior lobe covers the posterior aspect of the stomach. The stomach is a U-shaped sac divided in four chambers. The first chamber, which receives the esophagus, is delim ited by a very thin layer of tissue, and receives the ducts of the dorsal and lateral lobes of the digestive gland. The second chamber, posterior, is delimited by a thick muscular tissue and receives the duct of the posterior lobe of the digestive gland. It appears divided externally but consists of only one internal chamber. The third, funnel-shaped chamber is delimited by a thin layer of tissue with high ridges internally. The fourth chamber is continuous and externally similar to the third, but it bears only low, thin ridges internally. The intestine is long, narrow, and of type II. A rectal gland is present. It is a long, narrow, and coiled tube that opens in the left portion of the pulmonary complex. Its function is unknown.

Nervous system

(Fig. 7A). The circum-esophageal nerve ring is post-pharyngeal and pre-esophageal. The two cerebral ganglia touch and the cerebral commissure is short. However, the length of the cerebral commissure does vary among individuals. Pleural and pedal ganglia are also all distinct. The visceral commissure is short but distinctly present and the visceral ganglion is more or less medial. Cerebro-pleural and pleuro-pedal connectives are short and pleural and cerebral ganglia touch each other. Nerves from the cerebral ganglia innervate the buccal area and the ocular tentacles, and, on the right side, the penial complex. Nerves from the pedal ganglia innervate the foot. Nerves from the pleural ganglia innervate the lateral and dorsal regions of the mantle. Nerves from the visceral ganglia innervate the visceral organs.

Reproductive system

(Fig. 7B). Sexual maturity is correlated with animal length. Mature individuals have large female organs (with a large female gland mass) and fully-developed, male, copulatory parts. Immature individuals may have inconspicuous female organs (or simply no female organs at all) and rudimentary anterior male parts. The hermaphroditic gland is a single mass, joining the spermoviduct through the hermaphroditic duct (which conveys the eggs and the autosperm). There is a large, bent, and approximately oval receptaculum seminalis (caecum) along the hermaphroditic duct. The female gland mass contains various glands (mucus and albumen) which can hardly be separated by dissection and of which the exact connections remain uncertain. The hermaphroditic duct becomes the spermoviduct (which conveys eggs, exosperm, and autosperm) which is not divided proximally, at least not externally. A prostate, not distinct externally, may be located within the walls of the spermoviduct. The spermoviduct is completely embedded within the female gland mass, at least proximally. Distally, the spermoviduct branches into the deferent duct (conveys the autosperm up to the anterior region, running through the body wall) and the oviduct. The free oviduct conveys the eggs up to the female opening and the exosperm from the female opening up to the fertilization chamber, which should be near the proximal end of the spermoviduct. The ovate-spherical spermatheca (for the storage of exosperm) connects to the oviduct through a wide and strong duct. The oviduct is narrow, only slightly elongated and convoluted. The vaginal gland is absent.

Copulatory apparatus

(Figs 7 C–D, 8). The male anterior organs consist of the penial complex (penis, penial sheath, vestibule, deferent duct, retractor muscle) and penial accessory gland (flagellum, and hollow spine). The penial complex and the penial accessory gland share the same vestibule and the same anterior male opening.

The penial gland is a long, tube-like flagellum with a proximal dead end. The length of the flagellum of the penial gland varies among individuals but it is always heavily coiled. Distally, the flagellum ends in a hard, hollow spine protected by a sheath which is fused distally with the vestibule. The hollow spine is narrow and elongated, slightly curved. Its diameter is between 20 and 30 µm but it narrows down distally. The diameter of the opening at its tip is between 4 and 6 µm. Its length ranges from 0.7 mm (ZRC.MOL.6397 #1) to 1.2 mm (USMMC 00005 #1). The hollow spine does not open directly into the vestibule. Instead, the end of the tube of the accessory gland is a disc which is more or less flat (between 0.4 and 0.6 mm in diameter) and bears approximately 20 conical papillae in its center. The hollow spine thus must go through that disc in order to be outside and shared with the partner.

The penial sheath is long and very strongly coiled in spirals. In less mature individuals, the coils may not be as strong and numerous but they are present. The penial sheath protects the penis for its entire length. The insertion of the retractor muscle marks the separation between the penial sheath (and the penis inside) and the deferent duct. The retractor muscle is shorter than the penial sheath and runs straight to the posterior half of the visceral cavity. The insertion of the retractor muscle varies among individuals: in the posterior half of the visceral cavity in all specimens but those from India; in the anterior half of the visceral cavity (just anterior to the heart) in the specimens from India. The deferent duct also is highly convoluted with many loops. In immature specimens, the deferent duct is significantly less coiled. The penis is elongated, round, narrow, and hollow; its diameter is less than 200 µm, and its distal part covered with hooks. When the penis is retracted inside the penial sheath, the hooks are inside the tube-like penis. During copulation, the penis is exerted like a glove and the hooks are then on the outside. Hooks are very densely packed inside the penis, with multiple, irregular rows of an average of 15 hooks around the circumference of the penis. Hooks are conical, slender, sharply pointed, and measure up to 300 µm in length.

Distinctive diagnostic features.

Externally, Onchidium typhae differs from other Onchidium species by the color of the hyponotum, which is not white but instead varies between grayish, yellowish, and even greenish (see below the dichotomous identification key, before the final conclusion). The color of the foot (yellowish, not bright orange) is not diagnostic. Internally, the spirally coiled penial sheath is not diagnostic. However, Onchidium typhae is the only Onchidium species known so far with an intestine of type II.

Remarks.

The original description of Onchidium typhae by Buchannan was brief but it was based on first-hand observation of live animals, which is quite unusual for onchidiids since most onchidiid species were described based on preserved material with no information on shape and color of live animals. Even though the type material is likely lost, two features described and illustrated by Buchannan support the identification of the material described here as Onchidium typhae . First, and most importantly, the long eye tentacles (only Onchidium species have such long eye tentacles) and the dorsal papillae of various sizes ( Buchannan’s "glandular tubercles"). Buchannan’s (1800: fig. 2) illustration of an elongated body of a crawling slug is perfectly compatible with what we observed in the field. Buchannan originally described Onchidium typhae as non-hermaphroditic; however, as pointed out by Cuvier (1804) shortly after Buchannan’s article, onchidiid slugs are in fact hermaphroditic.

Stoliczka (1869) re-described Onchidium typhae based on live animals that he collected himself near Calcutta. His identification is in agreement with Buchannan’s original description. Stoliczka provided some information on the internal anatomy, which is compatible with our observations. Semper (1885) examined two specimens from Calcutta which he identified as Onchidium typhae . According to Buchannan (1800), Onchidium typhae is found on leaves of Typha elephantina (hence the specific name), a common reed in brackish waters of the Ganges delta. Wild areas with reeds have become very rare because Bengal was heavily developed in the last century and most coastal areas were converted to rice fields. According to Stoliczka (1869), however, Onchidium typhae is also found "about old bricks" and "in ditches." Stoliczka also mentioned that it was the only species found near Calcutta, suggesting that in the past it could be found in brackish waters extending far inland. Finally, Stoliczka mentions Onchidium typhae from the banks of the Hooghly River, which is very close to where our own specimens were collected in West Bengal.

Semper accepted Stoliczka’s anatomical re-description of Onchidium typhae and added some detail on the anterior male parts. In particular, Semper illustrated some penial hooks and the spine of the penial accessory gland. However, the sizes described by Semper (a maximum size of 170 µm for the penial hooks and a length of 4.5 mm for the spine of the penial accessory gland) are not really compatible with the sizes observed for the present study (penial hooks up to 300 µm and a spine less than 1.2 mm long). Therefore, Semper likely examined individuals of a different species, which cannot be identified at this stage.

Hoffmann (1928) re-described a specimen that he identified as Onchidium typhae . That identification as an Onchidium is possibly correct (because of the presence of a rectal gland and of a penial accessory gland). However, the specimen examined by Hoffmann came from an unknown locality and it remains unclear whether Hoffmann did actually examine Onchidium typhae . Labbé (1934) simply mentions the name Onchidium typhae with no additional description or records. Dey (2006) illustrated a preserved (and not relaxed) specimen identified as Onchidium typhae from the Sundarbans. The identification is possibly correct (the photograph is fuzzy). However, it is unclear whether the brief comments on the natural history of Onchidium typhae refer only to Onchidium typhae or a mix of species because Dey claims that Onchidium typhae is found climbing on the trees, which is uncertain. Based on our observations, Onchidium typhae can be found on muddy old logs, but not actually climbing on trees.

Finally, a search for potential synonyms of Onchidium typhae revealed no synonyms (the available type materials of all onchidiid species were personally examined) and it does seem that it was named only once.