Peronia madagascariensis ( Labbe , 1934a)

Dayrat, Benoit, Goulding, Tricia C., Apte, Deepak, Aslam, Sadar, Bourke, Adam, Comendador, Joseph, Khalil, Munawar, Ngo, Xuan Qu ảng, Tan, Siong Kiat & Tan, Shau Hwai, 2020, Systematic revision of the genus Peronia Fleming, 1822 (Gastropoda, Euthyneura, Pulmonata, Onchidiidae), ZooKeys 972, pp. 1-224 : 1

Peronia madagascariensis ( Labbe, 1934a) Figs 21 , 22 , 23 , 24 , 25

Paraperonia madagascariensis Labbé, 1934a: 199, fig. 15.

Paraperonia jousseaumei Labbé, 1934a: 198, figs 12-14. Syn. nov.

Type material.

Holotype ( Paraperonia madagascariensis ). Madagascar • holotype, by monotypy, 40/40 mm; Fort Dauphin [Taolagnaro]; 1932; Décary leg.; MNHN-IM-2000-33680. Originally, no jar clearly labeled as the type material of P. madagascariensis was found at the MNHN, but the holotype could be traced back. The original description of P. madagascariensis is based on a single individual (40/38 mm) from Fort-Dauphin collected by Décary (the French botanist Raymond Décary [1891-1973]) in 1932. Only one old jar was found at the MNHN with a specimen collected from Fort-Dauphin (MNHN-IM-2000-33680). The information on the label (specimen collected by Décary in 1932) matches the information provided in Labbé’s original description of P. madagascariensis , and even the specimen size matches. Therefore, that specimen is considered to be the holotype by monotypy of P. madagascariensis . The holotype was dissected by Labbé. The radula, the posterior (hermaphroditic) reproductive parts, and the male parts are all missing. The intestinal loops are of type V (Fig. 21A ).

Syntypes ( Paraperonia jousseaumei ). The type material of Paraperonia jousseaumei could not be located at the MNHN. The original description of P. jousseaumei was based on ten individuals (45/38 to 40/30 mm) from the Red Sea ("Mer Rouge") collected by Jousseaume in 1892. Only two old jars were found at the MNHN with that collecting information. One of them contains specimens that are part of the type series of P. gondwanae because the specific name " gondwanae " is written on an old label (MNHN-IM-2000-33683). The three labels of the other jar (MNHN-IM-2014-7993) say: "Peronia Mer Rouge Mr Jousseaume n°15, 1892," "Oncidium [written over “Oncidiella”] peronii Cuvier Mer Rouge M. Jousseaume n°15-1892," and, for unknown reasons, “60.” This jar contains six specimens of Peronia , from 60/45 to 25/15 mm, two of which were dissected, possibly by Labbé. The intestinal loops of the two dissected specimens are of type I and thus are not in agreement with Labbé’s (1934a: fig. 12) original illustration of the intestinal loops of type V in P. jousseaumei . Also, the sizes and the number of individuals do not match the original description of P. jousseaumei . Those specimens could possibly be some of the eight non-type specimens that Labbé (1934a: 190) mentioned in his re-description of Peronia peronii collected by Jousseaume from the Red Sea ("Mer Rouge") in “1852” (likely a mistake for 1892). Given that Labbé does not specify their size, it is not possible to know to what species Labbé thought those specimens belong exactly (MNHN-IM-2014-7993).

Additional material examined.

South Africa • 2 specimens 35/23 mm [5841] and 18/13 mm [5842]; KwaZulu-Natal, Durban, Treasure Beach; 29°57.294'S, 30°59.514'E; 18 Nov 2010; D Herbert and L Davis leg.; rocky intertidal zone; NMSA W7547.

Mozambique • 1 specimen 42/37 mm [735]; Cabo Delgado Province, Pemba, Wimbi Beach, Pemba Beach Hotel; 12°58'S, 40°32'E; 14 Jul 2006; DG Reid leg.; on shady rock at base of limestone cliff, in upper eulittoral behind intertidal platform; NHMUK 20060414.

Madagascar • 1 specimen 55/40 mm [5500]; Ambatobe, près Soamanitse; 25°27.4'S, 44°57.4'E; 24 May & 7 Jun 2010; MNHN Expedition Atimo Vatae leg.; st BM02, 0-1 m; MNHN-IM-2009-16391. • 1 specimen 40/35 mm [5504]; same collection data as for the preceding; MNHN-IM-2009-16412. • 1 specimen 40/30 mm [5501]; Ambatomainty; 25°26.3'S, 44°56.5'E; 25 May 2010; MNHN Expedition Atimo Vatae leg.; st BM03, 0-1 m; MNHN-IM-2009-16392. • 1 specimen 55/40 mm [5502]; same collection data as for the preceding; MNHN-IM-2009-16393. • 1 specimen 55/40 mm [5503]; Ambatobe, Bavarama; 25°27.9'S, 44°57.6'E; 28 & 29 May 2010; MNHN Expedition Atimo Vatae leg.; st BM06, 0-1 m; MNHN-IM-2009-16396. • 1 specimen 40/35 mm [5506]; same collection data as for the preceding; MNHN-IM-2009-16418.

Oman • 1 specimen 10/7 [703]; Muscat, Cemetery Bay; 23°37.250'N, 58°36.016'E; 9 Feb 2004; G Paulay & M Claereboudt leg.; coral community, reef slope, on ophiolitic bedrock and rubble; UF 332088.

Additional material examined

(historical museum collections). Oman • 3 specimens 80/60 mm; Qurm Beach, near Muscat; 23°37.56'N, 58°28.86'E; 26 Jan 2005; V Bonito, M Claereboudt & G Paulay leg.; intertidal rocky shore; UF 368019.

Iran • 3 specimens 80/65 mm to 75/65 mm; Persian Gulf, Strait of Hormuz, Qeshm Island; 18 Apr 1937; G Thorson leg.; st 69; NHMD 635302.

Yemen • 1 specimen 55/55 mm; Socotra, off Quadub; 12°39.015'N, 53°55.730'E; 18 Mar 1999; Salim Al-Moghrabi (from N Yonow’s personal collection) leg.; intertidal, ST-064 SAM-1; SMF 358305.

South Africa • 1 specimen 70/45 mm; Port Natal, Durban; 30S, 31E; Wahlberg leg.; littoral rocky bottom; SMNH 180711.

GenBank and BOLD sequences.

One COI sequence was obtained from BOLD (LGEN099-14) for an individual identified as Onchidium verruculatum and collected from Dwarka, Gujarat, on the western coast of India (ca. 22°N), which is the easternmost known locality for P. madagascariensis . A second COI sequence was obtained from GenBank (LC027608) for an individual identified as Peronia sp. and collected from the coast of Iran in the Persian Gulf. Both sequences were unpublished.

Distribution

(Fig. 6 ). From South Africa to the Red Sea and western India (ca. 22°N): South Africa, Mozambique, Madagascar (type locality of P. madagascariensis ), Gulf of Oman, Iran (Strait of Hormuz), Yemen (Socotra), India (Mumbai, Gujarat), Red Sea (type locality of P. jousseaumei ). All records are new except for the type locality in Madagascar. Peronia madagascariensis is, so far, not present in Mauritius.

Etymology.

Peronia madagascariensis was named after its type locality, Madagascar. Peronia jousseaumei was named after Félix Pierre Jousseaume [1835-1921], a medical doctor and malacologist who collected many specimens from the Red Sea preserved at the MNHN and which Labbé (1934a) studied for his monograph on onchidiids.

Habitat.

Peronia madagascariensis is found in the rocky intertidal, like most other Peronia slugs.

Color and morphology.

No picture of live animals was available. The color of preserved specimens is not different from other species (greyish brown and mottled with darker and lighter areas dorsally, and light brown greyish ventrally). The dorsal notum of live animals is covered by dozens of papillae of various sizes. In large individuals, dorsal papillae can be particularly tall (easily up to 4 mm), even in preserved specimens, and are evenly distributed over the entire notum. Preserved, they are very difficult to distinguish from retracted dorsal gills in the posterior half of the notum, but they are regular papillae with or without eyes. Some papillae bear black dorsal eyes at their tip. The number of papillae with dorsal eyes is variable (from 12 to 18). Dorsal gills seem taller and denser than in other species. The largest specimens in our fresh material are 55 mm long but two additional museum specimens are much longer (80 mm).

Digestive system

(Figs 21A-D , 22 ). Examples of radular formulae are presented in Table 5 . The median cusp of the rachidian teeth is approximately 55 μm long. The hook of the lateral teeth is approximately 100 to 130 μm long. The intestinal loops are of type V.

Reproductive system

(Figs 21E , 23 - 25 ). In the anterior (male) parts, the muscular sac of the accessory penial gland is less than 15 mm long. The hollow spine of the accessory penial gland is narrow, elongated, and straight or slightly curved, and its shape (including at its tip) varies between individuals. Its length ranges from 2 mm ([5502] MNHN-IM-2009-16393) to 2.4 mm ([5500] MNHN-IM-2009-16391). Its diameter at the conical base ranges from 200 to 230 μm. Its diameter at the tip ranges from 70 to 80 μm. The retractor muscle is shorter or longer than the penial sheath and inserts near the heart. Inside the penial sheath, the penis is a narrow, elongated, soft, hollow tube. Its distal end bears conical hooks which are less than 100 μm long.

Diagnostic features

(Table 4 ). Peronia madagascariensis is characterized by a unique combination of two anatomical traits: intestinal loops of type V and a spine of the accessory penial gland longer than 2 mm.

Remarks.

The name Paraperonia madagascariensis clearly applies to a Peronia species because of the dorsal gills on the notum of the holotype. The holotype was entirely dissected by Labbé. The radula, the posterior (hermaphroditic) reproductive parts, and the anterior copulatory apparatus are missing. The intestinal loops are of type V (Fig. 21A ), as illustrated by Labbé (1934a: fig. 17). The name Peronia madagascariensis applies to the species described here because it is, according to our molecular data, the only Peronia species with intestinal loops of type V along the eastern African coast, from South Africa to the Persian Gulf and western India, including Madagascar. Note that some of our fresh material was collected only 150 km east of the type locality in southern Madagascar. Some internal characters described by Labbé (1934a: 199) could not be verified on the holotype because most internal parts are missing, but they are similar to the species described here. In particular, the length of the spine of the accessory penial gland (2 mm) is compatible with what was observed in our material.

Additional, non-type specimens were found in historical museum collections which could be identified as P. madagascariensis due to the presence of intestinal loops of type V, from Oman (UF 368019), the Strait of Hormuz (NHMD 635302), and Socotra (SMF 358305). Those localities, however, are all already included within the known distribution of P. madagascariensis based on our DNA sequences, as the Strait of Hormuz is very close to the Gulf of Oman. Finally, one of the " a " paralectotypes of Labbé’s (1934a: 199) Paraperonia gondwanae from Bombay (MNHN-IM-2000-33682), with intestinal loops of type V (Fig. 21B ), belongs to P. madagascariensis . Note that two of those museum specimens are longer (80 mm) than our fresh material (less than 55 mm).

Peronia slugs with intestinal loops of type V are without doubt present in the Red Sea. For instance, one of the " c " paralectotypes of Labbé’s (1934a: 200) Paraperonia gondwanae from Suez (MNHN-IM-2000-33683) is characterized by intestinal loops of type V (Fig. 21C ), which means that it does not belong to P. verruculata (characterized by intestinal loops of type I). Labbé’s (1934a) Paraperonia jousseaumei , with the Red Sea as type locality, is also characterized by intestinal loops of type V. Even though the type material of P. jousseaumei could not be located at the MNHN, Labbé’s (1934a: fig. 12) drawing of the internal anatomy of P. jousseaumei clearly illustrates intestinal loops of type V. Given that P. madagascariensis is widespread from South Africa all the way to western India, including the Strait of Hormuz, it is accepted here that it also is distributed in the Red Sea. That, however, will still need to be confirmed with fresh material from both the Red Sea and the Gulf of Aden. If it appears that the populations of Peronia slugs with intestinal loops of type V from the Red Sea are a distinct species, then the name P. jousseaumei could apply to them and be valid. Finally, given that P. madagascariensis is present in the Strait of Hormuz, it most likely also is distributed in the rest of the Persian Gulf, which hopefully will be confirmed at some point with fresh material.

Even though the names Peronia madagascariensis and Peronia jousseaumei were never used prior to the present contribution, they are not regarded as new combinations because Paraperonia has already been regarded as a synonym of Peronia by Britton (1984: 182) and because it has also been made clear that the genus Peronia included all species of slugs with dorsal gills (e.g., Dayrat et al. 2017: 1861).

The specimen [703] from Oman was tentatively identified as Peronia sp. 2 by Dayrat et al. (2011) but it clearly belongs to P. madagascariensis (Fig. 2 ). Also, note that its COI sequence was resubmitted to GenBank because the old one (GenBank HQ660044) was inaccurate. The specimen [735] from Mozambique was tentatively identified as Peronia cf. peronii by Dayrat et al. (2011). This identification should be disregarded because the specimen [735] belongs to P. madagascariensis (Fig. 2 ).

A specimen from Durban (30°S), South Africa, preserved in Stockholm (SMNH 180711) identified as O. verruculatum by Hoffmann (1928: 44, 73) is identified here as P. madagascariensis because of its intestinal loops of type V (Table 4 ). Various records of Onchidium peronii , O. savignyi , and Onchidium verruculatum from Natal, South Africa ( Krauss 1848: 72; Sturany 1898: 73; Collinge 1910: 171-172; Connolly 1912: 224-225, 1939: 454; Webb 1969) most likely are records of Peronia madagascariensis , although P. verruculata (unit #5) could also be present in northeastern South Africa because it is known in Maputo, southern Mozambique (ca. 26°S).

Figures

Figure 2. Phylogenetic relationships between Peronia species based on concatenated mitochondrial COI and 16 S DNA sequences. Numbers by the branches are the bootstrap values (maximum likelihood analysis) and the posterior probabilities (Bayesian analysis). Only the values> 50 % (ML) and> 0.9 (Bayesian) are indicated. Numbers for each individual correspond to unique identifiers for DNA extraction. Information on specimens can be found in the lists of material examined and in Table 2. The color used for each species or mitochondrial unit is the same as the color used in Figs 3 - 6.

Figure 6. Geographical distribution of the Peronia species A distribution of all Peronia species except for P. peronii B distribution of P. peronii. The colors are the same as those used in Figs 2 - 5. Colored areas correspond to hypothetical geographical ranges based on confirmed records only. Distinct colors are used for each unit of P. verruculata. The distribution of P. verruculata in the Indo-West Pacific is actually continuous. However, because it is unclear which units are present in regions from where we have no fresh material of P. verruculata (red areas), no unit of P. verruculata is shown there. For P. peronii, black dots correspond to material identified based on anatomical characters and blue dots correspond to material with DNA sequences. Details on species distribution can be found in each species description.

Figure 21. Peronia madagascariensis A-D digestive system, dorsal view, with intestinal loops of type V E posterior, hermaphroditic (female) reproductive system A holotype, Paraperonia madagascariensis, Madagascar (MNHN-IM- 2000 - 33680) B paralectotype, Paraperonia gondwanae, Mumbai, western India (MNHN-IM- 2000 - 33682) C paralectotype, Paraperonia gondwanae, Red Sea (MNHN-IM- 2000 - 33683) D Madagascar, [5501] (MNHN-IM- 2009 - 16392) E same as D. Scale bars: 5 mm (A-D), 2 mm (E). Abbreviations: dd deferent duct, ddg dorsal digestive gland, fgm female gland mass, hg hermaphroditic gland, i intestine, ov oviduct, pdg posterior digestive gland, rs receptaculum seminis, sp spermatheca, st stomach.

Figure 22. Radula, Peronia madagascariensis, South Africa, [5841] (NMSA W 7547) A right half rows of teeth B rachidian and innermost lateral teeth C rachidian and innermost lateral teeth D lateral teeth E lateral teeth, frontal view F outermost lateral teeth. Scale bars: 200 μm (A), 20 μm (B, E, F), 40 μm (C), 100 μm (D).

Figure 23. Anterior, male, copulatory apparatus, Peronia madagascariensis A Madagascar, [5501] (MNHN-IM- 2009 - 16392) B South Africa, [5841] (NMSA W 7547). Scale bars: 5 mm (A), 2 mm (B). Abbreviations: ag accessory penial gland, dd deferent duct, ms muscular sac, ps penial sheath, rm retractor muscle, v vestibule.

Figure 24. Penial hooks, Peronia madagascariensis, Madagascar A, C [5500] (MNHN-IM- 2009 - 16391) B, D [5504] (MNHN-IM- 2009 - 16412) E [5506] (MNHN-IM- 2009 - 16418) F [5501] (MNHN-IM- 2009 - 16392). Scale bars: 60 μm (A), 100 μm (B), 20 μm (C, D), 40 μm (E), 10 μm (F).

Figure 25. Accessory penial gland spine, Peronia madagascariensis, Madagascar A, E [5500] (MNHN-IM- 2009 - 16391) B, F [5502] (MNHN-IM- 2009 - 16393) C, G [5504] (MNHN-IM- 2009 - 16412) D, H [5506] (MNHN-IM- 2009 - 16418). Scale bars: 400 μm (A-D), 20 μm (E-H).