Zoosphaerium arborealis, Wesener & Sierwald, 2005

Wesener, Thomas & Sierwald, Petra, 2005, New giant pill-millipede species from the littoral forest of Madagascar (Diplopoda, Sphaerotheriida, Zoosphaerium), Zootaxa 1097 (1), pp. 1-60 : 34-50

Zoosphaerium arborealis sp. nov.

Figs 19–29

Material: Holotype: 1 m., FMNH. L ocus typicus: Madagascar; Province Toliara; Mandena ; littoral forest; in leaf litter; 24°56.51’S, 046°59.70’E; IV.2003; leg. T. Wesener.

Paratypes: 2 m., 8 f. (mature) FMNH ; 1 m., 2 f. (mature) CAS ; 1 m., 2 f. (mature) ZSMC ; 3 f. SMNG VNR 13554 ; Madagascar; Province Toliara; Mandena ; littoral forest; in leaf litter and on trees; 24°56.51’S, 046°59.70’E; IV.2003; leg. T. Wesener. 2 m., 2 f. FMNH . Madagascar; Province Toliara; Sainte Luce ; littoral forest; in leaf litter; 24°46.77’S, 047°10.28’E; 07.IV.2003; leg. T. Wesener.

Other Material: 29 f. (mature) Université de Antananarivo. Madagascar; Province Toliara; Mandena ; littoral forest; in leaf litter; on trees; many inside of dead stems of Pandanus sp. ; 24°56.51’S, 046°59.70’E; IV.2003; leg. T. Wesener. 7 m., 11 w. (immature), FMNH. Madagascar; Province Toliara; Mandena ; littoral forest; in leaf litter; on trees; many inside of dead stems of Pandanus sp. ; 24°56.51’S, 046°59.70’E; IV.2003; leg. T. Wesener. 1 m., 2 w. (immature), FMNH. Madagascar; Province Toliara; Sainte Luce ; littoral forest; in leaf litter;; 24°46.77’S, 047°10.28’E; 07.IV.2003; leg. T. Wesener. 3 m., 13 w. (mature) FMNH. Locality: Province Fianarantsoa; Parc National de Andringitra , Forêt d'Ravaro , 12.5 km SW Antanifotsy, 22°12.7’S, 46°50.7’E, 1500 m, 9–16.i.2000, undisturbed mid­elevation forest /w Acanthaceae , leg. S. Goodman.

Diagnosis: Medium­sized pill­millipede up to 40 mm in body length. Males distinctly smaller than females. Tergites brown, legs and antennae red ( Fig. 29a ). Body smooth or with a few hairs, anal shield slightly tapered ( Fig. 19a ). Antennae with 7–24 sensory cones ( Fig. 22b ), first and second joint with invagination, all joints at least basal with sclerotized teeth ( Fig. 22a ). First sternite at inner margin straight ( Fig.19d ). Anal shield ventrally on each side with two well­developed black locking carinae. Anterior locking carinae short, posterior one 3–4 times longer than anterior carina ( Fig. 19c ). Anterior telopods with two stridulation ribs, number of ribs on female washboard variable ( Figs. 20b , 21a ).

Similar species: Z. arborealis is closely related with Z. lambertoni ( Brolemann, 1922) . Nevertheless, Z. arborealis the inner horns and inner lobes of the posterior telopods are unique in shape ( Figs 21e, f ). Additionally, the locking carinae of the anal shield are strongly developed in Z. arborealis , but weakly developed in Z. lambertoni ( Brolemann, 1922: 235–236, " font défaut en tant quíarêtes pigmentées [...]"). The type specimen of Z. lambertoni ( Brolemann, 1922) , deposited at the L`Académie Malgache in Antananarivo / Madagascar, cannot be located. Thus, the species cannot be compared to Z. arborealis . All other species of Zoosphaerium with similar posterior telopods like Z. anomalum ( DeSaussure & Zehntner, 1897) have a differently formed anal shield. The lower margin at the posterior end of the anal shield is never tapered in Z. arborealis .

Description: Males (14 specimens): length: 19.0–26.45, width of thoracic shield: 9.65–13.15, height of thoracic shield 5.5–7.2. Females (45 specimens): length: 21.0–40.0, width: 10.75–20.0, height: 6.75–11.35.

Habitus: tergites more posterior higher than anterior ( Fig. 19a ). Tergites very smooth, sometimes with a broad patch of hairs at the anterior and posterior margin.

Coloration: tergites brown, posterior margin darker ( Figs. 29a–b ), smaller specimen olive­brown. Antennae and legs dark­orange to red. Red color fades in alcohol.

Head: with numerous hairs and hair­pits especially around the labrum and lateral of eyes. A few single, long hairs around the eyes and distributed on the entire head. Posterior margin of head towards the collum with a patch of short hairs ( Fig. 23d ). Edges of antennal groove with 5–6 small spines and sclerotized teeth ( Fig. 23b ). Head with up to 90 ocelli on each side ( Fig. 23c ). Tömösváry organ inside with a coral­like structure ( Fig. 23e ).

Antennae: shaped as described for the genus. Length of antennomeres: 1>2>3=4=5<6; sixth antennomere longest, of cylindrical shape ( Figs. 22a ) with 7–24 sensory cones ( Fig. 22b ). First antennomere much broader than the others ( Fig. 22c ). Sclerotized teeth at the base of antennomeres one through six, reaching the apical border at first antennomere. First and second joint with invaginations ( Fig. 22c ).

Mandible: with seven rows of pectinate lamellae; number of teeth declining proximally ( Fig. 27b ). Condylus with two strongly developed steps near the apical margin ( Fig. 27c ). Gnathochilarium: ventral side with bristles, only few on the lingual lamella ( Fig. 24a ). With a field with three sensory cones lateral to the palpi ( Fig. 24b ). Two different types of sensory cells on the central pads: long ones without a pit and smaller, cylinder­shaped ones with a central pit ( Fig. 25a ). Sensory cones on palpi distributed regularly over the tip ( Fig. 25b ). Epipharynx: shaped as in other members of this genus ( Figs. 26b , 27a ).

Collum: Anterior margin bald, in the middle with a row of very small, dark­brown sclerotized teeth. Posterior margin on each half with 4–6 hairs, inserting lateral and at the edges. Rest of collum hairless. Thoracic shield: A few hairs in the concave lateral extension of the thoracic shield, especially near the margins. Anterior marginal brim broader than the rest of the brim ( Fig. 19a ).

Anterior paratergite depression of tergites 3–12 with many hairs, on the anterior margin with a few ribs ( Fig. 19a ), otherwise tergites are almost hairless and smooth. Tips of the posterior margins of paratergites 8–12 projecting posteriorly.

Endotergum with two or more rows of marginal bristles. Internal part with short spines and few, isolated bristles. Bristles scaly ( Fig. 25c ). Marginal ridge straight. Interior of marginal ridge one row of round flat nodules ( Fig. 26a ).

Anal shield: lower margin at posterior end tapered ( Fig. 19a ). Only in some males near posterior margin with many short (sensory?) hairs. Ventral side carries two black locking carinae on both sides, anterior one similar to those of tergites, posterior one more than three and a half times longer than anterior one, at posterior end nearer to the margin than anteriorly. Locking carinae separated from each other by a distance equal to the double length of the shorter carina. Distinct suture present between both carinae. Where the suture reaches the margin of the anal shield, a small, distinct triangular invagination is visible ( Fig. 19c ).

Legs: tarsi of first pair of legs with 4–6, those of second with 6–9 ventral spines, weakly curved claws and without apical spine. Tarsi of legs 3–21 with curved claws, 10–14 ventral spines and one apical spine. 9th leg pair without coxal lobe but with a few small, black triangular spines ( Fig. 19b ). Coxae of all legs at the inside margin covered with many long hairs, the following leg joints with a few isolated, long hairs at the inner margin. Femur with a dark crenulated ridge ( Fig. 19b ).

Sternite: first sternite lobe broad and short, reaching the apical edge of the coxae of first leg pair, covered sparsely with hairs ( Fig. 19d ). Apical margin rounded regularly and covered with many long hairs. Basal margin with few hairs ( Fig. 19d ). Inner margin of sternite remarkably straight. Sternites three and beyond with a spine like process which reaches about the stigma opening of the anterior sternite.

Female sexual characters: second leg pair without coxal lobe, but on exterior margin with some short, triangular black spines ( Fig. 20a ). Vulvae well­developed, covering more than 2/3 of the coxa ( Fig. 20a ). Operculum small, ending before the apical edge of coxae. Apical margin of operculum constricted in the middle (subreniform) with two broadly rounded equally sized lateral tips. Both parts of operculum of same height. Basal margin almost straight. Exterior and inner plates (EP, IP) of vulva below the operculum surrounding the basal margin of the operculum. Inner plate very long and broad, reaching almost 2/3 of height of operculum. Exterior plate not as long as the inner one, reaching only the basal 1/2 part of the operculum. Cyphopod sclerites consisting of two triangular apical sclerites and a much larger third sclerite formed like a tuning­fork; all visible as dark structures near the suture of the vulva between inner and exterior plate ( Fig. 20a ). Subanal plate with washboard, consisting of irregular, asymmetrical 1–4 stridulation ribs. Length of ribs very variable ( Fig. 20b ).

Male sexual characters: second leg pair without coxal lobe, but on exterior margin with some short, triangular black spines and covered with many hairs ( Fig. 21d ). Male gonopore covered half with a sclerotized, undivided, rounded plate, which is slightly excavated at apical margin. Gonopore plate covered with hairs. Apical part of plate membranous ( Fig. 21d ). Anal shield without any invagination or other sexual dimorphism, but in some cases with patch of (sensory?) hairs at posterior margin.

Anterior telopods: syncoxite of anterior telopods with few isolated hairs. First joint with a stridulation harp and two stridulation ribs. Inner ridge short, reaching only 1/2 of the length of the more laterally ridge. Lateral ridge long, beginning at the basal margin of the first joint and ending just at its apical margin ( Fig. 21a ). Posterior side of the first joint inside with an impression. Margins of impression laterally with one row of hairs. First joint with exception of margins on both sides bold. Second joint on posterior side with a lobe­like apically stout process ( Figs. 21b ). Tip of process reaching only slightly above the third joint. Towards the third joint with sclerotized spots ( Fig. 21c ). Third joint inner margin drawn out, at apical margin broad. Apical margin almost straight, only slightly excavated near the middle, tip of second joint process visible. Inner margin of third joint towards second joint process with some spines and sclerotized spots, juxtaposed to the spots on the second joint ( Fig. 21c ). Third joint apically with some thick bristles ( Figs 21a–b ).

Posterior telopods: movable finger (third joint) of chela long and slightly curved towards the immovable finger (process of second joint, Fig. 21e ). Invagination towards the immovable process of the second joint with 4–5 small, non­sclerotized spines, after one third of length of third joint with one big spine, after half of length with one fingershaped process. Third joint on posterior side with 17 th sclerotized teeth, size of teeth declining basally ( Fig. 21f ).

Immovable digit (process of second joint) almost straight with slightly curved tip. Anterior side basally with one spine, apically with numerous sclerotized spots juxtaposed the invagination of the third joint. Chelae only basally with hairs, on rest of surface hairs absent ( Figs. 21f ). Inner horns (IH) of syncoxite with a pointed tip ( Figs 21e–f ).

Distribution & Ecology: This species has an extraordinarily wide distribution. It is the only species described from littoral forests, which is not restricted to one forest site. Zoosphaerium arborealis was also discovered in another ecosystem, in the montane forest of PN Andringitra at over 1200 m elevation.

In the littoral forests this species was collected in the fragments of Mandena and Sainte Luce. In both forests Z. arborealis is associated with a species of the giant pillmillipede genus Sphaeromimus splendidus Wesener & Sierwald (in press) and it also occurs in Sainte Luce sympatrically with Zoosphaerium sp. Sainte Luce.

To date, all 33 species of Malagasy pill millipede genus Zoosphaerium were known from museum material only. Observation of living specimens are presented here for the first time. During an expedition in beginning of April 2003 to the Malagasy southern littoral forests, the first author observed the activity, diversity, behavior and habitats of Zoosphaerium arborealis in the littoral forest fragment near Mandena ( Fig. 30 ).

This species was common in the littoral forest of Mandena. On 18 collection days> 300 specimens were observed. Smaller individuals were often found in dead, rotten wood, especially in dead, excavated stems of Pandanus sp. (Pandanaceae) , normally 5– 15 specimen of almost the same size in a single stem. These stems were hollow, filled with numerous fecal pellets, indicating that the species feeds on the soft and stringy contents of the stems. Numerous smaller specimens were discovered in piles of dead wood, which were common in this forest, especially near the tracks. In these piles of dead wood, the giant pill­millipedes occurred together with larvae of Scarabaeidae and Cestonidae ( Insecta: Coleoptera ) and spirostreptids ( Diplopoda), the most common arthropods.

The leaf litter was thin in the littoral forest of Mandena, after 1–2 cm the soil was strongly riddled with fine roots of trees. Below 20 cm the soil is sandy. After a few dry days, the soil and root layer and leaf litter dry out. Apparently, the sandy ground cannot hold the water and the layer of leaf litter is too thin to prevent moisture loss of the layers below. Only a few animals could be detected in this dry leaf litter, in some places Blattodea ( Insecta) were found.

More leaf litter accumulates in some dips and under special trees (Phyllexylon xyophylloides, Fabaceae ; Homalium albiflorum , Flavouriaceae; Ophiocolea delphinensis , Bigoniaceae).

Adult specimens of Z. arborealis were collected in such places or under wood during drier days. Numerous pellets show that the animals use these moist microhabitats as retreats and for feeding. In the moist patches some Isopoda and Amphipoda (both Crustacea) could be found as well.

Adults of Z. arborealis were collected at dawn after rainfall during the night and also after heavy rainfalls in the thin leaf litter. A day earlier, before the rain, no specimens were observed at these sites. Numerous specimens of all sizes could be observed after heavy rainfalls walking on the tracks. It must be noted that adult specimen were observed climbing tree trunks more than 150 cm high, feeding on the stem ( Fig. 29a ). While climbing on trees, members of this species do not roll into a ball after mechanical disturbance, only the head is tucked under the thoracic shield. Such arboreal behavior was previously reported only from South­African giant pill­millipedes of the genus Sphaerotherium ( Haacker & Fuchs 1972) .

No eggs were found in dissected females. The smallest juvenile stadium had 19 leg pairs. No matings were observed.

Predation: Tergites of smaller specimen of Z. arborealis were found in a layer of arthropod remains around ant holes of a big, red ant species in Mandena. This layer contained mostly seeds of plants and body rings of "juliform"­diplopods. Living rolled­up specimens of Z. arborealis were placed near ants and ant holes, but the ants did not attack the millipedes. One big (– 35 mm body length) specimen of Z. arborealis was placed in a cage with a small mongoose (Viveriidae, Galidia elegans ) from the forest of Mandena. The rolled­up pill millipede was detected immediately, broken with lateral teeth and eaten by the mongoose, except for the intestines and tergites. It is quite possible that Galidia elegans is a natural predator of pill millipedes. One female collected in the littoral forest of Sainte Luce had fungi on the antennae. Specimens of all three localities were strongly covered with mites (Arachnida: Acari), it is unknown if this mites are commensals or parasites.

Conservation: This species has a wide distribution. One of the sites where Z. arborealis was collected is already protected. Nevertheless, the distribution of this species is scattered due to the vast destruction of natural forests on Madagascar.

Figures

FIGURES 21 a–f: Z. arborealis sp. nov., male holotype. a: right anterior telopod, anterior view; b: right anterior telopod, joint 1–3, posterior view; c: right anterior telopod, joint 2–3, inner view; d: 2nd left leg coxa and prefemur with male gonopore, posterior view; e: left posterior telopod, anterior view; f: left posterior telopod, posterior view. IH = inner horns. Scale bars = 1 mm

FIGURES 22 a–c: Z. arborealis sp. nov., female paratype, SEM: right antennae. a:, 6th joint lateral; b: apical view on sensorial cones; c: 1st and 2nd joint.

FIGURES 23 a–e: Z. arborealis sp. nov., female paratype, SEM. a: right antennae, sensorial cone, detail; b: edges of the antennal grove, A = insertion of antennae, arrow = spines; c: right field of ocelli, arrow = aberrant ocellus; d: posterior border of the head towards the collum with patch of small hairs, C = collum; e: Inner view of the thömösvary­organ.

FIGURES 24 a–b: Z. arborealis sp. nov., female paratype, SEM, gnathochilarium. a: ventral view; b: apical view on right palp, arrow = field of sensorial cones, cP = central pads, LL = lingual lamella, P = palpus.

FIGURES 25 a–c: Z. arborealis sp. nov., female paratype, SEM. a: gnathochilarium, two types of sensorial cones on the central pads; b: detail of palpus tip; c: bristle of endotergum

FIGURES 26 a–b: Z. arborealis sp. nov., female paratype, SEM. a: endotergum, (1) = marginal ridge with external row of marginal bristles, (2) = band of flattened nodules, (3) = internal area.; b: basal view on ventral side of epipharynx.

FIGURES 27 a–c: Z. arborealis sp. nov., female paratype, SEM. a: epipharynx, distal view; b: right mandible, distolateral view, arrow = condylus; c: right mandible, view on condylus, aT = apical tooth, cT = comb teeth, mp = molar plate, mpp = molar plate process,.

FIGURES 29 a–g: Z. arborealis sp. nov., paratypes. a: left female coxa and prefemur with vulva, immature female of 10,5 mm body length, posterior view; b: left female coxa and prefemur of immature female of 14,15 mm body length, posterior view; c: left female coxa and prefemur of mature female of 21,75 mm body length, posterior view; d: left anterior telopod, joint 1–3, immature male of 14,3 mm body length; e: right posterior telopod joint 1–3 with inner horns of syncoxite of immature male of 14.3 mm body length; f: 1st leg right coxa with 1st sternite of mature specimen (female paratype); g: 1st leg right coxa with 1st sternite of immature female of 14,15mm body length. Abbreviations: IH = inner horns; S = sternite Scale bars = 1 mm

FIGURES19 a–e: Z. arborealis sp. nov., female paratype. a: habitus; b: right 9th legpair, posterior view; c: posterior view on anal shield; d: coxa of 1st right leg with 1st right sternite, posterior view; e: collum (1st tergite). As = anal shield, Pl = pleurite, S = sternite. Scale bars = 1 mm

FIGURES20 a–b: Z. arborealis sp. nov., female paratype. a: coxa of 2nd right leg with vulva, posterior view; b: subanal plate with washboard. EP = exterior plate, IP = inner plate, O = operculum. Scale bars = 1 mm

FIGURES 28 a–b: Z. arborealis sp. nov., female paratype, digital photo. a: living animal, climbing on small branch; b: living animal, rolled in a ball.

FIGURE30: Distribution map.