Synonymy

Vaginula stuhlmanni Simroth, 1895 (original combination)

Eleutherocaulis stuhlmanni (Simroth, 1895)

Vaginula schnitzleri Simroth, 1895

Vaginula aequatorialis Simroth, 1896

Vaginula brauni Simroth, 1913

Laevicaulis stuhlmanni aegypti Ali and Robinson, 2017 (nomen nudum)

General description of external morphology

The slug has a dorsal-ventrally flattened body; the notum has a dark brown background, with a light longitudinal colour band running down the centre; in some specimens, it is reduced to punctation (Fig. 1). Some specimens have a darker band on both sides of the notum, these bands being connected together on the head and in the back and could be thick or thin or as rows of dark spots (Figs 1, 2). The hyponata are uniform light brown. The head has two pairs of tentacles that are hidden under the notum, the first (lower) shorter chemotactic pair and a longer (upper) pair of ocular tentacles. The adult specimens of Laevicaulis stuhlmanni preserved in alcohol have been measured (n = 15): mean length 44 mm (range: 36–52 mm), mean width 16 mm (range: 12–19 mm), mean foot length 38 mm (range: 23–48 mm), mean foot width 6 mm (range: 4-9 mm), mean width of right hyponota 5 mm (range: 3–7 mm), mean width of left hyponota 5 mm (range: 3-7 mm).

Figure 1.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt; external morphology and colouration.

Figure 2.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt.

Genitalia description:

The female genital pore is located on the right hyponotum, posterior to the middle of the total length and the male genital pore opens in the anterior portion just below the right ocular tentacle. The anterior male genital complex is composed of two elements, the phallus sensu stricto and the phallic gland, both enclosed in a muscular sheath sharing a common atrium that opens through the genital pore. The phallus is slender (Figs 3, 4) and has a sub-distal annular swelling. In some specimens, the phallus is less slender, with a distal swelling, caused by the invagination of the distal part. The phallic gland is composed of a conical papilla that arises from a vase-shaped base. On the proximal part, there are a number digitiform tubules, numbering from ten to seventeen, averaging 12.5 ± 1.8 tubules. In three specimens, it was noticed that one of the tubules branched into two smaller tubules (Fig. 3). The papilla gland is at the same level as the phallus papilla tip in some samples or distally forward (Figs 5, 6). However, in two specimens, the phallus papilla stalk was distally more forward than the gland papilla or not at the same level (Fig. 7). The papilla of the phallic gland is pointed conical and different in length and width relative to its base in each individual; at the base of the papilla, typically four to five thin lines of wrinkles can be seen, possibly produced by the contraction and expansion of the papilla. Some specimens have up to seven to twelve thin lines of wrinkles (Fig. 7). The posterior genitalia are characterised by a more or less oval hermaphroditic gonad (ovotestis) made up of rounded acini; from it arises a large convoluted hermaphroditic duct that connects to the albumen gland, the latter being conical and very large. The vas deferens can be divided into four parts: the proximal posterior vas deferens (from the fertilisation complex to the prostatic gland), the distal posterior vas deferens (from the prostate to the ligament duct), the middle vas deferens (from the ligament duct, in anterior direction inside the integument) and the anterior vas deferens (from the exit of the tegument to the phallus). The prostatic gland is dark yellow to pale coffee colour with a smooth surface; the ligament duct is a short duct that connects the middle vas deferens to the short duct of the bursa copulatrix; the bursa copulatrix is large and oval (Fig. 8).

Figure 3.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt, transverse dissecting view of the phallic sheath; the arrow points to tubule branched into two smaller tubules.

Figure 4.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt, phallus.

Figure 5.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt, the verge with contracted distal part, the phallus gland tip is at the same level as the phallus tip.

Figure 6.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt, the verge with erected distal part, the phallic gland tip is not at the same level as the phallus tip.

Figure 7.  

Laevicaulis stuhlmanni (Simroth, 1895), transverse dissecting view of the phallic sheath; on the base of papilla, there are four to five thin lines of wrinkles.

a

b

Figure 8.

Laevicaulis stuhlmanni (Simroth, 1895). AG, albumen gland; BC, bursa copulatrix; BCD, bursa copulatrix duct; DPD, distal posterior vas deferens; FGP, female genital pore; HG, hermaphroditic gonad; HD, hermaphroditic duct; LD, ligament duct; MD, medium deferens; OV, oviduct; PPD, proximal posterior vas deferens; PR, prostatic gland; TO, tube leading to oviduct.

a: Photograph of female reproductive system.  
b: Drawing of the female reproductive system.  

Laevicaulis stuhlmanni was first collected from the indoor ornamental plants garden of a hotel located in El Gezira Street, on Gezira Island, Cairo, El Zamalek District, Cairo, Egypt (30°03’27.4”N 31°13’28.1”E). There have been subsequent unconfirmed reports from anthropochorus environments elsewhere in Egypt. The distribution map of Laevicaulis stuhlmanni, Laevicaulis alte and Laevicaulis striatus is illustrated in Africa (Fig. 9).

Figure 9.  

Distribution map of Laevicaulis stuhlmanni (red dots), Laevicaulis alte (yellow triangle) and Laevicaulis striatus (green dots) in Africa.

The species Laevicaulis stuhlmanni was reported for the first time in Egypt under the nomen nudum L. stuhlmanni aegypti (Ali 2017a, Ali 2017b) and the biological attributes, such as life cycle, pre-oviposition period, oviposition period, post-oviposition period, reproductive output, incubation period, generation period and life span, were documented and described.

As in all veronicellid species, the slug is a hermaphrodite species that possessing both male and female genitalia and self-fertilisation can occur. However, mating or cross-fertilisation was not observed for this species under laboratory conditions. The reproductive season of this species starts in March, when the seasonal temperature rises and lasts until November (Ali 2017b). The incubation period for the eggs to hatch averaged 15 days with ranges from 10 to 19 days at a temperature of 29 to 31°C and a humidity between 52% and 64%. Laevicaulis stuhlmanni reaches sexual maturity after an average of 86 days with ranges 53 to 115 days after hatching, depending on the surrounding conditions. Total life span averaged 155 days with ranges between 127 to 188 days. The oviposition period averaged 46 days with ranges one to 74 days; each slug can produce around five egg clutches ranging from one to twelve egg clutches/slug with an average of 47 eggs/clutch (range 10 to 120 egg/clutch) under laboratory conditions. Generation period averaged 102 days with ranges 69 to 127 days (Ali 2017b). This species laid multiple egg masses during its activity months. In Figs 10, 11, 12, the eggs are oval to spherical elongate shape and translucent. The eggs are joined together by a thin interconnecting thread producing a gradually spiral-like egg mass with distinct faecal pellets ribbon deposited on the top of the eggs.

Figure 10.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt; the photos include the egg masses of this species. The eggs are joined together by a thin interconnecting thread that forming spiral-like egg mass.

Figure 11.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt; the species during the egg-laying process under laboratory conditions.

Figure 12.  

Laevicaulis stuhlmanni (Simroth, 1895) Gezira Island, Cairo, Egypt; the species deposited eggs that are darker in colour ready to hatch and covered with a distinct faecal ribbon on the top of the eggs.

Laevicaulis stuhlmanni is a native slug of Eastern and Central Africa (Congo, Rwanda, Burundi, Kenya, Tanzania) (Forcart 1953). Veronicellids have been recorded throughout the tropics on a number of ornamental plants including flower beds and seedlings causing significant economic losses (Robinson and Hollingsworth 2005 , Gomes et al. 2013). It is a phytophagous species and often occurs in large numbers beneath decaying vegetation in its natural habitat; however, through this study and from other growers and farmers’ observations, the species was also found in commercial plantations. L. stuhlmanni is usually active during the night, while it is buried in the ground during the day (Ali 2017b). It is a hermaphrodite and member of a genus that includes some widespread and invasive pests, such as Laevicaulis alte (Raut 1999, Das and Parida 2015).

The validity of Laevicaulis Simroth, 1913 as the objective senior synonym of Eleutherocaulis Simroth, 1913 was recently confirmed by Sajan and Tripathy (2021). The type species, in both cases by subsequent designation, is Vaginulus comorensis Fischer, 1883, a junior synonym of Vaginulus alte A. Férussac, 1822.

The systematics of the Laevicaulis species are uncertain, due to the description of several taxa in the second half of the 1800s, based only on external characters such as body colour and body measurements of the slug or on inadequate descriptions of genitalia. Simroth (1895) described a subspecies Laevicaulis stuhlmanni atrolimbatus, but its validity is questionable.

Laevicaulis striatus and L. stuhlmanni have similar female genitalia and phallic glands. However, the phallus in the two species reportedly has a different apex. In Simroth 1895: 62, the original description of L. stuhlmanni describes a cylindrical phallus, slightly tapered distally, with a flat terminal disc, in the middle of which the sperm duct opens. The descriptions and figures of L. stuhlmanni in Simroth (1896: 18, Pl. 3, figs. 6 B-C) and the synonym Vaginula aequatorialis) and those of Forcart L (1953: 74-76, Pl. 5, figs. 1 A-E) are consistent with the original description of L. stuhlmanni. However, part of Forcart's description of L. stuhlmanni (Forcart 1953: 75, Pl. 4 figs. 10 A-B) is not consistent with L. stuhlmanni's original description, while it fits well with L. striatus in the same paper (Forcart 1953). Simroth (1896) described the new species Vaginula striata, based on external features of sexually immature specimens. Forcart (1953: 79-86, Pl. 5, figs. 3 A and C) reviewed L. striatus, based on adult specimens sampled in the type locality. These specimens are characterised by the phallus with a subdistal annular swelling. The important character given for L. stuhlmanni is that it has a phallus with a flat terminal disc, while L. striatus has a phallus with a subdistal annular swelling. Based on these data, Liberto et al. (2021) classified the Laevicaulis population from Libya as L. striatus.

However, as shown by Colosi (1927) for Laevicaulis somalicus (Colosi 1927) and as evidenced by Forcart (1953) (P1. 4, fig. 10; P1. 5, figs. 1, 3) for L. stuhlmanni and L. striatus, the length of the phallus and the shape of the phallic apex are variable according to the contraction or erection of the phallus; therefore, it cannot be excluded that L. striatus is a synonym of L. stuhlmanni. Pending a modern taxonomic review involving a molecular analysis of the stuhlmanni/striatus group, the authors attribute the population examined here and the one reported from Libya (as Eleutherocaulis striatus in Liberto et al. (2021) to the senior taxon L. stuhlmanni (Simroth, 1895). The length of the phallus stalk of L. stuhlmanni in Forcart (1953) (when not contracted) is similar to that measured in the population from Cairo (Egypt) i.e. one or one and a half times the length of the papilla of the phallic gland, whereas in the populations from Benghazi (Libya), it is longer, i.e. two and a half times. The L. stuhlmanni populations described by Forcart (1953) have a variable external colour: greyish, reddish, yellow, brown or blackish-brown, the sole is uniformly blackish and always much darker than the hyponota or light with blackish margin ("subspecies" atrolimabratus). L. stuhlmanni from Egypt and Libya has an external colouration more similar to that described by Forcart (1953) for L. striatus: notum reddish-brown, yellow or greenish-brown unicoloured or with a median stripe, flanked on each side by two rows of irregular dark spots or stripes; hyponota and foot lighter than the notum.

Recently, Ali and Robinson (2020) and Ali and Robinson (2022) recorded Laevicaulis alte from Abo Rawash, Giza, Egypt. L. alte is distinguished from L. stuhlmanni by having a very dark notum with a pale thin well-defined white or creamy line on the dorsal surface, running the length of the body; the lighter hyponota have a creamy or grey colour; both surfaces minutely granular; the phallus with a sub-basal annular swelling (Grimpe and Hoffmann 1925, Benthem-Jutting 1952,Forcart 1953, Brodie and Barker 2012, Prakash et al. 2015).