Tuatara: Volume 9, Issue 3, January 1962
New Zealand Land Slugs — Part I
New Zealand Land Slugs — Part I
To most people, the word slug conjures up a picture of a rather repulsive, brownish-grey slimy animal, passionately addicted to eating cabbages. There are in New Zealand, however, representatives of two widely differing families of slugs, the introduced European Limacidae, and the native Athoracophoridae which are found only in the Western Pacific area. External differences between the two are easily observed: the Limacidae have two pairs of tentacles, a mantle area covering the anterior aspect of the back, a brown or grey coloration, and carnivorous or herbivorous habits, whereas the Athoracophoridae have only one pair of tentacles, a smaller, much less obvious mantle area, a distinct pattern of dorsal grooves, and a highly developed dorsal tracheate lung of a nature found in no other mollusc. The native slugs may grow up to six inches in length, are often more attractively coloured than their introduced counterparts, and frequently have numerous dorsal papillae.
New Zealand slugs are fairly common in bush and grassland, and are frequently found under logs, in leaf mould, and in the leaf bases page 88 of flax bushes and nikau palms. The mainland native slugs, and those found in the subantarctic islands, are closely allied to those found on New Caledonia, New Hebrides, New Britain, the Admiralty Islands, and the eastern coast of Australia. In a recent paper (Solem, 1959) the New Zealand slugs are regarded as primitive members of the group isolated by the submergence of a land bridge which, it is claimed, previously connected the North Island with the islands of Melanesia. During recent work on the native slugs of New Zealand the writer has found no evidence to suggest that the structure of our slugs is ‘primitive’, and the origin of the group and its dispersal cannot be determined from our present knowledge.
There are in New Zealand four genera of native slugs (one genus newly described — Burton, Trans. Roy. Soc. N.Z. in press) containing twenty-two known species (eleven newly described — Burton, Trans. Roy. Soc. N.Z. in press). There are some wide ranging common species such as Pseudaneitea papillata in the South Island and southern North Island, and Athoracophorus bitentaculatus which is widespread in both islands, but in general the species tend to be restricted in range, for example Pseudaneitea dendyi found as yet only in Mid-Canterbury, and Pseudaneitea schauinslandi, only in the Marlborough Sounds area. Slugs are rare or absent in very dry areas such as Central Otago and in the volcanic central plateau of the North Island, but are otherwise fairly common.
The distribution of the subantarctic Athoracophoridae poses interesting problems. Five species are known from four islands, but none as yet have been found on the mainland. Only one species occurs on more than one island. This species is found on both Campbell and Macquarie Islands, and its mode of dispersal is as yet unknown. Dispersal over a land bridge seems unlikely for two reasons. First, the slugs would have to survive the Pleistocene glaciation subsequent to the loss of the bridge, and secondly, the broad expanse of deep water between Macquarie and Campbell Islands makes a land bridge between the two improbable. Furthermore, oceanic wind drift dispersal of eggs or adults among rafting masses of vegetation does not seem probable, as this envisages the raft either moving against the West Wind Drift or completing a circumpolar journey. However, it is possible that Macquarie Island has been colonised by animals drifting from the coast of Australia, and if this is so the colonisation of Campbell Island would easily follow.
The four species found are contained in two genera, one of which, Pseudaneitea, is common on the mainland. The other genus, however, is only found in the subantarctic islands. If the slugs have been on the islands only since the Pleistocene, this points to a high rate of speciation. Generic differentiation appears to be considerably slower.
The slugs eat only fungi, and usually select encrusting fungi. For example Athoracophorus bitentaculatus is often found at night feeding on Capnocdium moniliforme on the leaves of Pseudowintera axillaris. The jaw is elasmognathic, having a horny plate held vertically in the anterior portion of the buccal mass and protruded through the mouth to scrape up fungus as the slug moves.
As the animal moves successive waves of contraction and relaxation traverse the sole from posterior to anterior. The expanded, relaxed parts of the sole stay fixed with mucous while the contracted zone is in forward motion.
The slug breathes mainly through the skin of the back, which is kept moist by a renal secretion passing along the grooves. The role of the lung in respiration is not yet known, but it is probably not very effective. The eggs (Pl. 3, fig. 3) are round, gelatinous, papillated, and a light translucent yellow. They vary in diameter according to the species, ranging from 3-4 mm. in Athoracophorus bitentaculatus to 7 mm. in Pseudaneitea papillata. They are laid in batches of up to fifty in damp, cool surroundings from the beginning of spring through to late summer, and take up to three months to hatch. The young slug develops in a curled position, with the mouth opposite the posterior tip of the sole. When the slug is due to hatch, it attempts to straighten out, as though exerting pressure opposite the head, which soon breaks through the egg wall. The slug then crawls away.
Specimens deprived of water shrink and soon die. One specimen which escaped at night was found as a small heap of dried-up tissue at the end of a forty-yard slime trail.
It is usually necessary to narcotise the slugs carefully before preserving them, otherwise the buccal mass will be protruded through the mouth and the animal may contract and distort so much that many features will be obscured. The most readily available narcotic is an infusion of tobacco in water. One large pinch of tobacco to a pint of water is sufficient, and after the container is thoroughly shaken the narcotic is ready for use. Specimens should be immersed for at least eight hours, preferably longer if they are large. Other narcotics may be better for large specimens; a dilute solution of Blackleaf 40, which also contains nicotine, is suitable. When properly narcotised the slugs will be relaxed and extended, sometimes with their tentacles protruding. They may be preserved in either 70% alcohol or 4-6% formalin solution. In general formalin is preferable, as the tissues remain softer and colour retention is slightly better.page 90
For injection of the circulatory system, freshly narcotised specimens only can be used, otherwise the arteries become constricted and burst under pressure. A fine capillary tube drawn from glass tubing and fitted with a rubber pipette bulb is best for this purpose. Slugs may be injected with a gelatin solution stained with indian ink, or with coloured latex; injections are usually made into the ventricle or common aorta (Pl. 2, fig. l).
To prepare a whole mount of the radula, remove the entire buccal mass and macerate it in strong caustic soda. The radula should not be left too long after the flesh around it has dissolved, otherwise the basement membrane disintegrates. Wash the radula in water, then transfer to concentrated aniline blue for two minutes. Wash in lactic acid. Unroll and flatten the radula before mounting in polyvinyl alcohol.
A detailed account of one species only (Pseudaneitea papillata) is given. This species is common and anatomically typical.
External Features (Plate 1, fig. 1)
PLATE I : Pseudaneitea papillata (Hutton). Fig. 1: Externals — dorsal aspect. Fig. 2: Buccal mass and associated structures. Fig. 3: Sub-buccal arteries and nerves. Fig. 4: Sub-buccal arte:ies, ganglia removed. Fig. 5 : Radula — central and lateral teeth.
an., anus; ao, anterior branch of aorta; b.a., buccal artery; b.g., buccal ganglion; b.m., buccal mass; c.a.v., cerebral arterial vesicle; c.g., cerebral ganglion; ga.a., ganglionic artery; g.o., genital orifice; h.s., head shield; l.gr., lateral groove; b.a., mantle area; m.gr., median groove; mo., mouth; o.a., oral artery; od., odcntophore; oes., oesophagus; o.n., oral nerve; ov., oviduct; p.a., pulmonary aperture; ped.g., pedal ganglion; ped.gl., pedal mucous gland; ped.n., pedal nerve; pen., penis; ph.a., pharyngeal artery; r.o., renal orifice; sal.d., salivary duct; ten., tentacle; ten.a., tentacular artery; ten.n., tentacular nerve; vag., vagina; v.d., vas deferens; v.g., visceral ganglion; I, II, III, IV, visceral nerves.
With scissors make a lateral incision along the left side just dorsal to the perinotum, and continue it over the dorsal aspect of the head. Carefully reflect the skin, except for the region around the mantle area to which the circular lung, bilobed renal organ, shell rudiments, and thin-walled atrium are attached. The lung and renal organ may be reflected with the skin, but the atrium must be carefully detached from the ventral wall of the dorsal blood sinus before the skin can be completely reflected and pinned down. Remove the thin, membranous wall to expose the viscera in the haemocoele.page 93
PLATE II: Pseudaneitea papillata (Hutton). Fig. 1 : Anatomy — in situ. Fig. 2: Alimentary system and associated blood vessels.
alb., albumen gland; at., atrium; b.m., buccal mass; g., ganglionic mass; her., hermaphrodite gland; int., intestine; liv., liver; od., odontophore; oes., oesophagus; p.ao., posterior branch of aorta; ped.gl., pedal mucous gland; ped.n., pedal nerve; pen., penis; ren., renal organ; r.m., retractor muscle; sal.a., salivary artery; sal.d., salivary duct; sal.gl., salivary gland; st., stomach; vag., vagina; vas def., vas deferens; ven., ventricle.
The mouth opens into a buccal chamber in the highly muscular buccal mass (Pl. 2, fig. 1; Pl. 3, fig. 2). A thin-walled oesophagus traverses the dorsal aspect of the buccal mass, passes ventral to the connective between the cerebral ganglia, and expands into an elongate, thin-walled stomach, which extends posteriorly to the liver. Here it recurves to merge into a thicker-walled, narrower intestine, which extends forwards to loop around the common aorta, passes back to the liver, then recurves to extend anteriorly to the rectum. The stomach and the loops of the intestine spiral around each other. The lobulate liver, orange in fresh material, occupies the posterior third of the body cavity. A pair of off-white, lobulate salivary glands flank the anterior wall of the stomach, and give off from their anterior ends each a tubular, convolute salivary duct, passing ventral to the supraoesophageal connective to merge into the anterior aspect of the buccal mass.
Reproductive System (Pl. 3, fig. 1)
The genital orifice, a short, narrow, slightly curved slit in the margin of the head shield lateral to the right tentacle, opens from a broad, short, often thin-walled vagina, to the end of which are attached the broad, long, muscular, slightly sinuous oviduct and the muscular, twisted penis. A thin-walled, rounded receptaculum seminis is attached to the oviduct near its anterior end by a narrow stalk. The convolute glomerate gland, of unknown function, is attached to the oviduct near its posterior end.
Attached at the posterior end of the oviduct are four structures: a rounded bulbose gland of unknown function, a yellow, U-shaped albumen gland, the end of the vas deferens, and the end of the highly convoluted hermaphrodite duct. The other end of the hermaphrodite duct arises from a large, oval, lobed ovotestis, which lies dorsally, posterior to the rectum. From the oviduct the vas deferens runs to the bulbose gland, and then along the course of the oviduct, under the right tentacular nerve, and out to the distal tip of the penis, which is marked by the insertion of a long retractor muscle with its origin in the dorsal midline.page 95
PLATE III : Pseudaneitea papillata (Hutton). Fig. 1 : Reproductiva system. Fig. 2 : Buccal mass — sagittal section. Fig. 3 : Eggs. Fig. 4 : Elasmognathic jaw. Fig. 5 : Head-ventral aspect.
Ib.gl., albumen gland; ant.ao., anterior aortic branch; ant.gen.a., anterior genital artery; a.p., accessory plate; b.c., buccal cavity; bulb.gl., bulbose gland; gen.a., genital artery; glom.gl., glomerate gland; her.d., hermaphrodite duct; her.gl., hermaphrodite gland; j., elasmognathic jaw; m.c., median cusp; mo., mouth; od., odontophore; oes., oesophagus; ov., oviduct; ov.a., oviducal artery; pen., penis; rec.sem., receptaculum seminis; r.m., retractor muscle; vag., vagina; vas def., vas deferens; w., wing.
The accessory glands, that is, the glomerate and bulbose glands, and the albumen gland are subject to an annual cycle, during which they grow to a very large size in May and June, and then diminish in size during the summer. Only when these glands reach their maximum development do the viscera fill the entire body cavity. During summer and autumn, the posterior tip of the liver lies at about two-thirds body length, and the body cavity posterior to this is unoccupied.
Circulatory System (Pl. 1, 2 and 3)
The heart, situated dorsally, consists of a thin-walled, transparent atrium which communicates with the smaller, thick-walled, white, muscular ventricle, from the left side of which the common aorta arises. This short vessel divides almost immediately into anterior and posterior aortic branches. The anterior branch gives off a genital artery which supplies the hermaphrodite gland, oviduct, and accessory glands, and then gives off a salivary artery to the salivary glands, before expanding to form a small vesicle between the visceral and pedal ganglia. From the vesicle arise paired tentacular and oral arteries, median buccal and pharyngeal arteries, and the anterior genital artery on the right side. The posterior aorta, before terminating in the liver, gives off numerous branches which ramify to supply the stomach and intestine. Blood collects in the large ventral sinus, which encloses the alimentary and reproductive systems, and in two small dorsal sinuses enclosing the renal organ and the pulmonary diverticula. Blood passes into the pulmonary sinus, and thence to the atrium for recirculation.
Nervous System (Pl. 1, fig. 2; Pl. 2, fig. 1)
The cerebral ganglionic mass is composed of paired cerebral, visceral, and pedal ganglia, just posterior to the buccal mass. The cerebral ganglia are smooth, white, rounded structures, superimposed on the lateral aspects of the paired visceral ganglia. The paired pedal ganglia are posterior and ventral to the visceral ganglia.
The cerebral ganglia give off paired tentacular nerves, paired nerves to the buccal ganglia situated on either side of the dorsal aspect of the buccal mass, and three pairs of nerves, arising in a common root on either side, to the oral region. The visceral ganglia, composed of numerous small ganglia just visible to the naked eye, give off four nerves from the posterior side, numbered I-IV from left to right. N. I runs on the left side of the stomach to enter the muscles of the back close to the renal organ. N. II runs along the anterior branch of the aorta to enter the back posterior to the renal organ. N. III at first follows N. II, but then runs posteriorly, following the coiling of the intestine; it gives branches to the hermaphrodite gland and the intestinal loop. N. IV runs over the dorsal aspect of the rectum into the skin. A major pedal nerve arises from the lateral page 97 aspect of each pedal ganglion to run down the side of the body cavity to the tail. Short nerves arise from the lateral aspects of the pedal ganglia to supply the anterior muscles of the sole.
Surprisingly, no nerve supplying the penis, vagina, and oviduct has been found.
The pulmonary aperture lies in the centre of the mantle area, and is bordered by a sphincter muscle. Lying immediately below it is an expanded pulmonary chamber, its floor and walls lined with muscle tissue. Several passages through this muscle branch to form numerous thin-walled, fingerlike diverticula which radiate out to form the roof of the pulmonary sinus. The effectiveness of the lung as a respiratory structure is not yet known. Some workers believe that it is primarily secretory in function. Probably the major part of air exchange takes place through the skin, which is kept moist by a secretion from the renal organ. The secretion is pumped from the renal orifice at intervals ranging from 2-20 seconds, and runs over the entire back, aided by contractions of the muscles bordering the grooves.
The Radula (Pl. 1 and 3)
The radula is saddle-shaped, inrolled dorsally at the sides, and expanded anteriorly to form a broad rasping surface in the buccal chamber. When flattened out on a slide, it forms a broad chevron with 130-150 rows of teeth, each row with up to 150 teeth on either side; these figures are variable. In each row there is only one central tooth; all others are laterals.
Each tooth consists of a broad, flat stem rooted proximally in the transparent basement membrane, and a distal recurved head bearing a number of denticulate reflections. The denticle number in any given specimen is subject to wide variation, and is unsuitable for diagnosing species.
Tooth formation takes place at the root of the odontophores, located at the posterior end of the radula; teeth here are rudimentary, with very long denticles in proportion to stem length. They remain clear when the radula is stained in aniline blue, presumably because they are still surrounded by non-staining basement membrane.