Corresponding author: Thomas Wesener (
Academic editor: D.V. Spiegel
The Malagasy giant pill-millipede genus
Wesener T, Le DM-T, Loria SF (2014) Integrative revision of the giant pill-millipede genus
Madagascar, the world’s third largest island, is famous for its endemic and endangered fauna and flora (
Despite their conspicuousness, it was only recently that the millipede biodiversity on Madagascar became better known.
In giant pill-millipedes, all species known from Madagascar were redescribed (
The third Malagasy giant pill-millipede genus
An expedition to Madagascar conducted by TW in 2007, as well as sorting through different natural history collections, led to the discovery of 12 additional
Important structures of the
DNA was extracted from 18 specimens: 12 of them preserved in 95% ethanol, the remaining ones in 75% ethanol. The HCO/LCO primer pair (
Species | Specimen Catalog # | Locality | Genbank # | GenSeq |
---|---|---|---|---|
QVMAG 23:45801 | Tasmania | genseq-4 | ||
FMNH-INS 56005 | Madagascar, Andasibe | genseq-4 | ||
FMNH-INS 56000 | Madagascar, Petriky | genseq-3 | ||
FMNH-INS 8650 | Tanzania, Usambara Hills | genseq-4 | ||
FMNH-INS 56016 | Madagascar, Andrahomana | genseq-4 | ||
FMNH-INS 56016 | Madagascar, Andrahomana | genseq-4 | ||
FMNH-INS 56008 | Madagascar, Mangatsiaka | genseq-4 | ||
FMNH-INS 56212 | Madagascar, Tsimelahy | genseq-4 | ||
ZFMK MYR 2273 | Madagascar, Tsimelahy |
|
genseq-4 | |
ZFMK MYR 2276 | Madagascar, Tsimelahy |
|
genseq-4 | |
FMNH-INS 6702 | Madagascar, Sainte Luce S9 | genseq-3 | ||
FMNH-INS 56031 | Madagascar, Sainte Luce S9 | genseq-3 | ||
FMNH-INS 56033 | Madagascar, Enato | genseq-4 | ||
FMNH-INS 61090 | Madagascar, Enato |
|
genseq-4 | |
CASENT 9032789 | Madagascar, Manombo, |
|
genseq-1 | |
FMNH-INS 8184 | Madagascar, Ivohibe |
|
genseq-1 | |
FMNH-INS 56208 | Madagascar, Gr. Lavasoa | genseq-2 | ||
FMNH-INS 61143 | Madagascar, Gr. Lavasoa |
|
genseq-2 | |
FMNH-INS 61142 | Madagascar, Gr. Lavasoa |
|
genseq-2 | |
FMNH-INS 61135 | Madagascar, Isaka-Ivondro |
|
genseq-2 | |
FMNH-INS 61137 | Madagascar, Isaka-Ivondro |
|
genseq-2 | |
ZFMK MYR 2322 | Madagascar, Isaka-Ivondro |
|
genseq-1 | |
FMNH-INS 61136 | Madagascar, Isaka-Ivondro |
|
genseq-2 | |
FMNH-INS 61132 | Madagascar, Manantantely |
|
genseq-4 | |
FMNH-INS 61138 | Madagascar, Manantantely |
|
genseq-4 | |
FMNH-INS 56210 | Madagascar, Malio | genseq-4 | ||
FMNH-INS 56210 | Madagascar, Malio |
|
genseq-4 | |
ZFMK MYR 2323 | Madagascar, Malio |
|
genseq-4 | |
ZFMK MYR 889 | Madagascar, Sainte Luce S8 |
|
genseq-1 | |
FMNH-INS 56211 | Madagascar, Andrahomana | genseq-4 | ||
FMNH-INS 56214 | Madagascar, Ankapaky Plateau |
|
genseq-1 | |
CASENT 9032816 | Madagascar, Vevembe |
|
genseq-4 |
To find the best substitution model, modeltest implemented in MEGA 5.05 (
California Academy of Sciences, San Francisco, California, U.S.A.
Field Museum, Chicago, Illinois, U.S.A.
Muséum national d’Histoire naturelle, Paris, France.
Queen Victoria Museum and Art Gallery, Launceston, Australia.
Zoologisches Forschungsmuseum A. Koenig, Bonn, Germany.
See
Genus of small to medium-sized (15–45 mm length)
Photographs of living
Male gonopore typical of
Anterior telopod consisting of syncoxite plus four telopoditomeres. First telopoditomere enlarged, carrying the male stridulation organ (harp) consisting of 3–6 stridulation ribs, number of ribs independent of the size of the male, species specific. Second telopoditomere posteriorly with a process protruding up to the start of telopoditomere 4. Third telopoditomere short, sometimes with a spine juxtaposed to process of telopoditomere 2. Telopoditomere 4 larger than 3 and 4 combined, conical, basally with a field of sclerotized spots juxtaposed to process of telopoditomere 2, apically with a large, triangular lobe-like spine, usually three smaller spines distributed across the joint.
Posterior telopods always consisting of syncoxite with inner horns and inner lobes and pair of telopodites each consisting of three telopoditomeres forming chelae. First telopoditomere unremarkable, second telopoditomere forming the immovable finger of the chela. Immovable finger basally wide, apically tapering, always curved toward telopoditomere 3 (movable finger). Immovable finger as long as, or in some species overlapping movable finger. Membrane of telopoditomere 2 often extended into lobe, an anterior side juxtaposed to telopoditomere 3 with a dense field of sclerotized spots. Telopoditomere 3 curved or straight, relatively slender, margin juxtaposed to immovable finger with 20–40 small black crenulated teeth, three or four spines, and one, rarely two (
Female vulva atypical for
1 | Male harp on the anterior telopod with 3 stridulation ribs ( |
2 |
– | Male harp on the anterior telopod with 4–6 stridulation ribs ( |
7 |
2 | Body length <20 mm. Midbody legs without a coxal lobe ( |
3 |
– | Body length >20 mm. Midbody legs at least with weak coxal lobe ( |
4 |
3 | Colour pink, surface shiny. Process of telopoditomere 2 of anterior telopods in anterior view visible laterally. Littoral forest of Mandena and rainforest of Enato |
|
– | Colour light brown, surface dull. Process of telopoditomere 2 of anterior telopods in anterior view not visible ( |
|
4 | Body length >30 mm, light brown. Endotergum with single row of marginal bristles ( |
|
– | Body length 21–28 mm, black or dark brown. Endotergum with two rows of marginal bristles ( |
5 |
5 | Midbody legs with strongly developed coxal process. Tergite surface shiny. Littoral forest of Sainte Luce, fragment S9 |
|
– | Midbody legs with barely developed coxal process ( |
6 |
6 | Endotergum with strongly developed cuticular patterns ( |
|
– | Endotergum with weakly developed cuticular patterns ( |
|
7 | Unique black pattern on orange-reddish basic colour ( |
|
– | Colour different, either uniformly black or brown ( |
8 |
8 | Harp with 4 stridulation ribs ( |
|
– | Harp with 5 or 6 stridulation ribs ( |
9 |
9 | Harp with 5 stridulation ribs ( |
|
– | Harp with 6 stridulation ribs ( |
5 ♂ & ♀, ZFMK MYR2273, Madagascar, Province Toliara, PN Andohahela, Tsimelahy,
Localities. S. musicus is apparently widespread in the southern spiny forest ecosystem. Different colour morphs from the same locality (
1 ♀ paratype,
Only recorded from the littoral rainforest at Sainte Luce, fragment S9 (
3 ♂ & ♀, ZFMK MYR2275, Enato,
Only recorded from the littoral rainforest of Mandena (
Type material.
By far the largest known
Colouration of tergites dark brown with black posterior margin. Paratergite impressions and groove of thoracic shield orange. Legs, antennae and pleurites orange, head and collum dark brownish-black, eyes green.
Head: Eyes with >70 ocelli. Antennae short, protruding back to coxa 6. Antennomeres 1–4 with few longer setae, 5 and 6 densely pubescent (
Collum glabrous except few setae at margins.
Thoracic shield smooth and glabrous, few setae in grooves. Grooves deep (
Anal shield massive, with a steep edge (
Endotergum inner section with numerous short triangular spines and long setae (
First stigma-carrying plate with a well-rounded projecting apex (
Leg 1 with 2 or 3, 2 with 4–6, 3 with 10 ventral spines. Leg pairs 4–21 with 11–14 ventral spines. Coxa process strongly developed (
Male gonopore typical for the genus (
Anterior telopod (
Posterior telopod (
SEM, Endoterga of mid-body tergite.
Female sexual characters: Vulva massive. Operculum well-rounded, protruding up to basal half of prefemur (
‘titanus’, adjective, referring to the large size of the species.
Only known from the eastern lowland rainforest of Manombo, which is now isolated by vast areas of pseudosteppe from all other remaining rainforests.
Type material.
Five stridulation ribs on the male harp, a character only shared with the spiny forest species
Measurements: Female paratype: 21.1 mm long, 10.2 mm wide (2nd), 5.8 mm height (2nd), male broken, not measured but slightly smaller.
Colouration influenced by 70 years in preservative, faded dark brown without any discernable pattern (
Head: Eyes with >60 ocelli (
Collum glabrous, with few setiferous points at its margin (
Endotergum inner section with numerous short triangular spines and long setae (
First stigma-carrying plate with a well-rounded apex.
Leg 1 with 2–4, 2 with 3–5, 3 with 8 ventral spines. Leg pairs 4–21 with 10–12 ventral spines. Coxa process of midbody legs weakly developed. Femur 1.8, tarsus 3.3 times longer than wide (
Male gonopore inconspicuous.
Anterior telopod (
Posterior telopod (
Female sexual characters: Coxa process on leg 2 well-developed. Vulva massive. Operculum apically emarginate, protruding up to basal half of prefemur (
‘vatovavy’, noun in apposition, referring to the type locality, located in the area of Vatovavy-Fitovinany (Fort Carnot).
Only known from the eastern lowland rainforest of Tsianovoha. Satellite images do not show much remaining natural vegetation in the area.
Type material.
Small shiny-black
Measurements: male holotype: 21.7 long, 10.4 (2nd), 11.2 (8th - widest) wide, 5.6 (2nd), 6.8 (10th - highest) height. Largest female (with eggs): 23.1 mm long, 11.4 mm (2nd), 12.1 (8th - widest) wide, 6.35 (2nd), 8.55 mm (10th, highest) high.
Colouration of tergites black. Collum and head light brown (
Head: Eyes with >60 ocelli. Antennae very short, protruding as far as leg 6. All antennomeres densely pubescent (
Collum glabrous except 3 or 4 short isolated setae on the surface and few at margin.
Thoracic shield smooth and glabrous, few setae in grooves. Tergites 3–12 smooth, paratergite tips of midbody tergites only weakly projecting posteriorly (
Anal shield massive, well-rounded, lacking pubescent area.
Endotergum inner section with numerous short triangular spines and very few setae (
First stigma-carrying plate with a well-rounded apex.
Leg 1 with 3 or 4, 2 with 5 or 6, 3 with 8 or 9 ventral spines. Leg pairs 4–21 with 11–13 ventral spines. Coxa process weakly developed (
Male gonopore inconspicuous.
Anterior telopod (
SEM, Endoterga of mid-body tergite.
Posterior telopod (
Female sexual characters: Second leg pair with well-developed coxal lobe.Vulva massive. Operculum well-rounded, protruding up to basal half of prefemur (
‘Lavasoa’, noun in apposition, after the Lavasoa (also called Ambatotsirongorongo) mountain, to which this species is endemic.
Endemic to the Lavasoa Mountain, where it could be recorded from two of the three remaining fragments. The species was common in the largest fragment of Grande Lavasoa, but only a single female could be collected at Petit Lavasoa.
Type material.
Small matte-black pill millipede with a dark brown head and collum and light brown appendages. Male harp with three stridulation ribs.
Measurements: male holotype: 20.2 long, 9.2 (2nd), 9.8 (8th) wide, 4.9 (2nd), 6.1 (10th = highest) high. Largest female (with eggs): 21.1 mm long, 9.6 mm (2nd), 10.75 (8th = widest) wide, 5.7 (2nd), 7.5 mm (10th = highest) high.
Colouration of tergites black, matte not shiny. Collum and head dark brown (
Head: Eyes with >60 ocelli. Antennae quite long, protruding as far as leg 8. Antennomeres 1–5 with few setae, 6 densely pubescent (
Collum glabrous except few setae at its margin.
Thoracic shield smooth and glabrous, few setae in grooves. Tergites 3–12 smooth, but not glossy, paratergite tips of midbody tergites only weakly projecting posteriorly (
Anal shield massive, well-rounded, lacking pubescent area.
Endotergum inner section with numerous short triangular spines and very few setae (
First stigma-carrying plate with a well-rounded apex.
Leg 1 with 2 to 4, 2 with 5 or 6, 3 with 10 or 11 ventral spines. Leg pairs 4–21 with 12–14 ventral spines. Coxa process weakly developed (
Male gonopore inconspicuous.
Anterior telopod (
Posterior telopod (
Female sexual characters: Second leg pair with well-developed coxal lobe. Vulva massive. Operculum well-rounded, protruding above basal half of prefemur (
Intraspecific variation: The endotergum differs slightly in the development of the cuticular impressions between the specimens from Isaka-Ivondro (
Genetic distances in the COI gene between the three populations are 2.9–4%, while even the two individuals from Malio show a variation at the population level of 3.6%. Future studies involving more localities and specimens should investigate whether or not gene flow occurs between the different populations of
‘andohahela’, noun in apposition, after the type locality, the rainforests of the national park Andohahela.
Widespread in the lowland and montane rainforests of the northern Anosy and Vohimena mountain chains.
Type material.
Small shining black pill millipede with orange-reddish appendages. Of all currently known
Measurements: male holotype: 20.6 long, 8.6 (2nd), 9.05 (8th = widest) wide, 5.2 (2nd), 6.1 (8th = highest) height.
Colouration of tergites shining black. Paratergite impressions and groove of thoracic shield dark greenish. Legs, antennae and pleurites orange-red, eyes green.
Head: Eyes with >60 ocelli. Antennae very short, protruding to coxa 5. Antennomeres 1–4 with few longer setae, 5 and 6 densely pubescent. Antennomere 6 towards disc with single row of sensilla basiconica. Male with 34/35 apical cones. Mouthparts not dissected.
Collum glabrous except few setae at margins.
Thoracic shield smooth and glabrous, few setae in grooves. Grooves deep. Tergites 3–12 smooth, except for paratergite depressions. Paratergite tips of midbody tergites weakly projecting posteriorly.
Anal shield well-rounded, lacking pubescent area.
Endotergum inner section with numerous short triangular spines and long setae (
First stigma-carrying plate with a well-rounded projecting apex (
Leg 1 with 2, 2 with 3, 3 with 8 ventral spines. Leg pairs 4–21 with 12 ventral spines. Coxa process visible, but not as well developed as those of anterior legs (
SEM, Endoterga of mid-body tergite.
Male gonopore typical for the genus (
Anterior telopod (
Posterior telopod (
Female unknown.
‘ivohibe’, noun in apposition, after the type locality, the national park Ivohibe.
Only known from the type locality.
Type material.
Measurements: male holotype: 15.8 long, 6.6 (2nd) wide, 4.1 (2nd) high.
Colouration of tergites dull brown. Paratergite impressions and groove of thoracic shield slightly lighter. Legs, antennae and pleurites orange-red, eyes green.
Head: Eyes with >45 ocelli. Antennae short, protruding to coxa 4. Antennomeres 1–5 with few longer setae, 6 densely pubescent. Antennomere 6 huge, large than 3 basal antennomere combined, towards disc with single row of sensilla basiconica. Male with 49/48 apical cones. Mouthparts not dissected.
Collum glabrous except few setae at margins.
Thoracic shield smooth and glabrous, few setae in grooves. Grooves deep. Tergites 3–12 smooth, except for paratergite depressions. Paratergite tips of midbody tergites weakly projecting posteriorly.
Anal shield well-rounded, lacking pubescent area.
Endotergum inner section with few short triangular spines and long setae (
First stigma-carrying plate with a well-rounded not-projecting apex.
Leg 1 with 2, 2 with 2, 3 with 4 or 5 ventral spines. Leg-pairs 4–21 with 7–10 ventral spines. Coxa process invisible (
Male gonopore typical for the genus.
Anterior telopod (
Posterior telopod (
Female unknown.
‘saintelucei’, adjective, after the type locality, and only area of occurrence, the littoral rainforest of Sainte Luce.
Only known from the only remaining southern lowland forest on basaltic soil, the tiny fragment S8 of Sainte Luce. In the nearby fragments on sandy soil,
Type material.
Small matte-black pill millipede with a dark brown head and collum. Similar to
Measurements (holotype): 21.1 mm long, 9.8 mm (2nd), 10.7 mm (8th - widest) wide, 5.5 (2nd), 7.0 mm (10th, highest) height.
Colouration of tergites black, collum and head brown. Paratergite impressions light brown to olive-greenish, legs and antennae olive green (faded to white in ethanol), pleurites light brown, eyes green.
Head: Eyes with >55 ocelli. Antennae short, posteriorly protruding to coxa 5. Antennomeres 1–5 with few longer setae, 6 densely pubescent. Antennomere 6 towards disc with single row of sensilla basiconica. Male with 58/61 apical cones. Mouthparts not dissected.
Collum glabrous except few setae at margins.
Thoracic shield smooth and glabrous, few setae in grooves. Grooves deep. Tergites 3–12 smooth, except for paratergite depressions. Paratergite tips of midbody tergites weakly projecting posteriorly.
Anal shield well-rounded, lacking pubescent area.
Endotergum inner section with few short triangular spines and long setae (
First stigma-carrying plate with a well-rounded not-projecting apex.
Leg 1 with 2 or 3, 2 with 5 or 6, 3 with 10 or 11 ventral spines. Leg pairs 4–21 with 12–14 ventral spines. Coxa process well developed (
Male gonopore typical for the genus.
Anterior telopod (
Posterior telopod (
Female unknown.
Etymology: ‘andrahomana’, noun in apposition, after the famous cave close to the type locality, the Grotte d’Andrahomana.
Relic occurrence in the Grotte D’Andrahomana. The single individual found close to the village Ankapaky might be an indication of a more widespread occurrence in the little explored Vohisandria and Amboalaingo hills N. of Ankapaky and S. of Ranopiso.
Intraspecific variations: The cave specimen shows a distinct colour pattern: tergites very light brown with dark brown posterior margins (
Despite the description of seven new species and numerous additional localities
Distribution map of the genus
The analysis of the barcoding fragment of the COI gene provided a good resolution at the species level; all
Maximum likelihood tree obtained from the COI dataset after 1000 bootstrap replicates under the GTR+I+G model. Habitus photograph shows
In the latter clade, all species show high genetic distances of 16–21% to one another and no sub-grouping receives any statistical support. More structure can be observed in the extreme southeastern clade.
Genetic distances between the species of
Nevertheless, the COI gene is a powerful taxonomic tool, greatly improving our systematic understanding and has led to the description of new species in the family
The interesting relationships and biogeographic patterns among the species of
Petra Sierwald (FMNH) is thanked for her continuous advise. James Boone and Jim Louderman (both FMNH) managed and inventoried most of the specimens on which this study is based. Betty Strack (FMNH), Karen Ulmen and Thorsten Klug (both ZFMK) provided assistance at the SEM. The material of