A new species and first record of the genus Triacanthella Schäffer, 1897 (Collembola, Poduromorpha, Hypogastruridae) for Africa

Abstract The first species of the genus Triacanthella to be recorded from Africa is described. Triacanthella madiba sp. n. belongs to the Southern Hemisphere group of the genus. It is morphologically closely related to Triacanthella vogeli Weiner & Najt, 1997 from Chile, and appears to be a gondwanian relict. The new species is also the first Triacanthella recorded from a guano habitat.


Introduction
The Cape Floristic Region in Western Cape Province of South Africa is the smallest Floral Kingdom in the world. Although its extraordinary rich flora has been well documented (Rebelo et al. 2006), studies have shown that its arthropods are not well known (Pryke and Samways 2008). Recent and extensive sampling of the Collembolan fauna of this region, undertaken within a bilateral project between South Africa and France, provided a wealth of new taxa in all groups (Janion et al. 2011). One of the most interesting discoveries was that of a new species of Triacanthella, a genus unrecorded from Africa so far. Here we provide the description of this new South African species along with its biogeographical considerations.
The genus Triacanthella is phyletically isolated among Hypogastruridae both from a morphological and a molecular point of view (D'Haese 2002(D'Haese , 2003a(D'Haese , 2003bGreenslade et al. 2011). It contains 22 species with an intriguing distribution, reflecting a complex and probably ancient history: six including the generotype are found in Europe and Asia, eight species in Australia and New-Zealand, seven species in South America and one species in North America. Almost all species are endemic or micro-endemic and restricted to narrow ecological niches (Salmon 1941;de Izarra 1971;Cassagnau and Deharveng 1974). They mostly occur in epigean habitats, from warm littoral habitats to permanently cold habitats of high Mediterranean mountains and humid and fresh lowland habitats in southern Australia and New-Zealand. The species T. perfecta Denis, 1926 has been found once in a cave in southern France, but its normal habitat is forest litter (Arbea and Jordana 1991). Christiansen and Bellinger (1980) also recorded T. copelandi (Wray, 1963) once from a cave, but its type locality is not given as a cave in the original description, and there has been no other records of the species so far. The presence of a Triacanthella species in the guano of an African cave is therefore a surprising and important discovery.

Identification key to the Southern Hemisphere
Description. Colour orange to pink alive, pinkish in ethanol even after one year (Fig. 1). Length 1.9 -2.5 mm. Habitus of Southern Hemisphere Triacanthella (Figs 1, 6A).
Dorsal integument ornamentation made of hemispherical and rather coarse secondary granules, with large areas devoid of secondary granules on head and tergites (Figs 2-3), symmetrically arranged; most noticeable are the long antero-axial one on head, those associated to classical suture zone of head (Fig. 2), the 1+1 amiboid ones on Th. II-III (Fig. 3A), and the triangular ones between Md and Mdl on Abd. I-III (Figs 3B-C); secondary granules smaller around these areas. Externally to ocular area is a large area where secondary granules are smaller and denser (Fig. 3D). Secondary granules larger along the axial zone (Fig. 3E). No rosette-like arrangement of secondary granules on Abd. VI. Ventral secondary granulation less coarse, more regular. Manubrium with secondary granules arranged in a characteristic linear pattern dorsally (Fig.  3F), and with large areas devoid of secondary granulation ventrally. Pseudopores not seen. Chaetotaxy characterized by a strong heterochaetosis dorsally and a moderate plurichaetosis on most body parts. Chaeta morphology described below, with macrochaetae, mesochaetae and S-chaetae on head and body, and various kinds of chaetae on antennae (Figs 4, 6C). No ordinary microchaetae except on praetarsus and genital plate.
No ventral chaetae on thoracic sternites. Number of ventral chaetae per half-tergite for Abd. II, III: 7, 13-17; anterior furcal subcoxa with 12-16 chaetae. All ventral chaetae are smooth ordinary chaetae. Lateral anal valves with 3 or 4 hr chaetae; upper anal valve with 7-9 hr chaetae. Leg chaetotaxy slightly plurichaetotic. Trochanter with 7 chaetae. Tibiotarsi I, II, III with (proximal + distal): 8 + 11, 8 + 11, 7 + 11 acuminate chaetae. No clavate tenent hair. Claw with two inner teeth at about 40% and 65% of claw basis, and 1 + 1 latero-distal teeth, appressed on the integument and difficult to see at about 85% of claw basis (Fig. 6D). Empodial appendage short and pointed, internal to empodial apical tubercle according to Fig. 6D, 1+1 small praetarsal microchaetae. Ventral tube with Figure 3. Triacanthella madiba sp. n., details of granulation types on dorsal side of the body. A amiboid primary granule area on Th. III B triangular primary granule area on Abd. III C triangular primary granule area on Abd. II, surrounded by smaller secondary granules D detail of the lateral plate of smaller secondary granules on head e axial area of Abd. V, with larger secondary granules between axial chaetae F linear arrangement of secondary granules on the manubrium. Scales: 30 µm. 9-11 + 9-11 latero-distal chaetae, and 1-2 chaetae on each side of the sternite of Abd. I. Tenaculum with 3 + 3 teeth. Dens without ventro-apical lobe, bearing 10-15 chaetae dorsally with fine granulation (secondary granules smaller than chaetal sockets); the basal macrochaeta of the dens is about 2.3 the length of the nearest mesochaeta; well developed mucro with a large lamella and a very distinct dorso-basal heel (Figs 6E-F).
Discussion. Triacanthella madiba sp. n. shares numerous characters with T. vogeli Weiner & Najt, 1997, described from southern Chile. It differs mainly by the ocelli G and H being equal in size to the other ocelli and the absence of rosette-shape tubercles on Abd. VI. It is also morphologically close to T. andina Cassagnau & Rapoport, 1962 from Argentina, but macrochaetae are less numerous on Abd. I-III "(333 versus 444). In addition, the lamellae of the maxilla are shorter and the papillae bearing the anal spines are not as strong in T. madiba sp. n., as in T. andina. Overall, these three species are extremely similar morphologically in spite of being very remote geographically. Triacanthella madiba sp. n. differs from Australian and New-Zealand species by characters pointed out in the key. An additional important character is the chaetotaxy of the distal part of the labial palp, which is similar to that described by Fjellberg for an unidentified species of Australia (Fjellberg 1999), being strongly reduced compared to that of T. biroi, Stach 1924 from Europe (Fjellberg 1999).
Distribution and ecology. Triacanthella madiba sp. n. is recorded in bat guano in a cave of Table Mountain National Park. This is the first record of the genus Triacanthella in a guano habitat and the first record of the genus for Africa. None of the Triacanthella species recorded so far are found in tropical regions. They are all restricted to temperate zones, where they occur in a large range of habitats in Europe (from xeric Mediterranean to permanently cold), while they are limited to humid and cool litter or surface soil layers in the southern hemisphere (Australia, New Zealand, Chile and Argentina, Weiner and Najt 1997). Its presence underground in a cool, nutrient rich and permanently humid habitat, and its absence in the remnant forest patches of Table  Mountain that we sampled extensively is surprising. The only subterranean records of the genus Triacanthella, include the record of T. copelandi in a cave in Tennessee (USA), without anymore detail, and a single specimen collected in a small shallow cave of oriental Pyrenees in France, that was described as T. proxima Delamare 1951, and later synonymised with T. perfecta. In the area around this last cave, T. perfecta is actually common in beech forest litter (unpublished observations), and its presence underground as a single specimen is obviously accidental. Conversely, T. madiba sp. n. occurs abundantly in the guano microhabitat of Wynberg cave and was not found outside in Table Mountain. The species can therefore be considered troglophilic in this area. Actually, T. madiba sp. n. may have been already recorded as Schaefferia (Typhlogastrura) sp. in Sharratt et al. (2000), collected from guano material during a cave fauna survey in Table Mountain.
Although the labial palp of T. madiba sp. n. is similar to the unidentified Australian species (Fjellberg 1999), it also shares some characters with certain South American species, making its placement in the phylogeny based on morphological characters problematic. If the new species is more closely related to the Australian and New-Zealand species, it would follow a classical transantarctic gondwanian pattern (Brundin 1965(Brundin , 1966Sanmartín and Ronquist 2004). Alternatively, it could be that T. madiba sp. n. is more closely related to South American species based on the characters pointed out in the key provided. Thus, T. madiba sp. n. could be the result of dispersal from South America (e.g. Allwood et al. 2010), associated with a significant shift in its ecological requirements. On-going molecular and morphological studies on this basal genus will hopefully resolve their intriguing biogeographic pattern.
Name derivation. We dedicate this species to Madiba, former President of South Africa, Nelson Rolihlahla Mandela, who celebrated his 20 years of freedom on 11 February 2010.