Rickia gigas Santam., Enghoff, & Reboleira, 2016

Santamaria, Sergi, Enghoff, Henrik & Reboleira, Ana Sofia P. S., 2016, Hidden biodiversity revealed by collections-based research-Laboulbeniales in millipedes: genus Rickia, Phytotaxa 243 (2), pp. 101-127 : 109-111

Rickia gigas Santam., Enghoff, & Reboleira , sp. nov. ( Figs 16–23 , 61–65 )

Mycobank MB 815404

Diagnosis:—Receptacle triseriate, a: 3–4, m: 2–3, p: 3–4 (+ 8–14 of lateral branch). Very large species, often exceeding 2000 μm in length. Posterior series extending in a free, lateral branch of 8–14 cells. Antheridia solitary or in pairs scattered on the thallus. Perithecial apex bearing two protuberant lobes and two short lips.

Type: — TANZANIA. Tanga, just outside Amboni Caves, on Archispirostreptus gigas (Peters 1855) ( Spirostreptida , Spirostreptidae ), 7

August 1974, I. B. & H. Enghoff leg., C-F-95086, C-F!, holotype designated here; BCB-SS · E576 ad, f, BCB!, isotypes designated here .

Etymology:— gigas , a Latin noun in apposition meaning “giant”, referring to the large size of the species and its main host.

Thallus hyaline except for the dark brown foot, the trichogyne scar, the septa separating the appendiculate cells from appendages and antheridia, and the antheridial efferent necks. Total length (379–)657–2189 μm. Receptacle triseriate. Basal cell cylindrical, slightly broadened at the distal end, usually very elongated, up to 13 times as long as broad, reaching up to 734 μm of total length, straight to variably curved ( Figs 16, 23 , I), showing a slight geniculation next to the darkened foot ( Fig. 16 , arrowhead).

Anterior series consisting of 3–4 superposed, slightly outwardly inflated, and variably shaped cells ( Fig. 16 ).

Median series consisting of 2–3 cells ( Fig. 20 , m), arising below cells a 2 and p 2, each with a distal appendiculate cell and secondary appendages, which are difficult to distinguish in mature specimens, each consisting of a brown base and a deteriorate apex, mostly similar to the remaining secondary appendages in the thallus.

Posterior series consisting of a basal part with 3–4 cells similar to those of the anterior series, and a free lateral flat branch (110–)245–325 μm long, which consists of a basal large, isodiametric cell, and (7–)10–13 superposed, flattened cells, 2–3 times as broad as long cells ( Figs 20 , 63 ). This branch is broadest near its midlength; each cell on both sides with appendiculate cells, which randomly support appendages or antheridia above constricted and brown septa ( Fig. 17 ), except for the outer side of the 2–5 lower cells, which bear neither antheridia nor appendages. Sometimes this free branch appears strongly tinged with brown, may be by deterioration ( Fig. 23 , arrowhead).

Antheridia 16–19 × 5–7 μm, above a trapezoidal to squarish stalk cell, with outwardly curved, more or less brownish, efferent necks. By pairs ( Fig. 64 ) or isolated, vertically superposed on the outer sides of lower cells of the marginal series, including the free branch of the posterior series ( Figs 17, 19 ).

Secondary appendages 34–63 μm, hyaline except for the diffuse brown base, above the constricted septum, which separates them from the appendiculate cells ( Fig. 17 , arrow). Short, with parallel margins and rounded distally when young, quickly deteriorating, disorganizing and becoming dirty with maturation and ageing of the thallus. Following the same pattern of distribution on the thallus as the antheridia, except that they are absent from cells of the anterior series.

Perithecia 166–292 × 50–89 μm, up to five on the same thallus ( Fig. 23 ), formed primarily from the anterior series, but also from the posterior and even, but rarely, from the median series ( Fig. 16 ). Ovoid, with maximum breadth near 1/3 of its height ( Fig. 65 ), gradually tapering towards an abruptly distinguished neck and, when seen in front view, a symmetrical tip showing two large outer lobes ( Fig. 18 ), each having small rounded apical papillae ( Fig. 21 , arrowheads), and two inner rather short lips ( Fig. 62 ). Persistent trichogyne brown scar at upper outer margin of neck ( Figs. 21 , 62 , trs). Perithecial basal cells very flattened and inconspicuous. Perithecial stalk cell ( VI) usually very elongate (up to 1087 μm), up to 22 times as long as broad, more or less flexuous, with parallel sides, inflated at the two ends ( Fig. 16 ), especially under the perithecium, sometimes deeply pigmented with brown at the base, when ageing. Ascospores 70–103 μm.

Position on host: —Thalli grow mostly on the legs, but can also be found on the dorsal parts of the first body rings.

Notes on hosts:— Archispirosteptus gigas is one of the World’s largest millipedes, reaching 260 mm in length and 19 mm in diameter. It is widespread in eastern tropical Africa ( Mwabvu et al. 2010). ‘ Spirostreptus’ hamatus is a moderate-sized spirostreptid, up to 10 cm long and 5 mm diameter, it occurs in the Tanzanian Eastern Arc mountains (Enghoff et al. in press). The genus name is cited among inverted commas because the name Spirostreptus has been re-interpreted ( Hoffman et al. 2001) to apply to a different group of species, and no other genus name is currently available for hamatus and several other species.

Discussion:— The number of appendiculate cells vary from one to three on the cells of lateral series, each bearing one secondary appendage, a solitary antheridium or one group with paired antheridia ( Fig. 19 ). Thalli found on Spirostreptus hamatus Demange 1970 (BCB-SS·E578ac) are smaller than those on Archispirostreptus gigas that we regard as the typical, representing what may be considered a varietal extreme of the species in relation to measurements and number of cells. The receptacle cells show conspicuous and numerous pores connecting them, which is exceptional and never previously described for any of the Laboulbeniales ( Fig. 22 ). It is interesting also to remember that, with the exception of dimorphic yeasts, all filamentous ascomycetes show a simple pore between cells according to scholarly mycological textbooks (e.g., Webster & Weber 2007: 227). Also it is worth mentioning that our SEM studies show no evidence of a haustorium penetration below the foot attachment after removal of the thallus ( Fig. 61 ). So far it seems incomprehensible how these fungi can acquire nourishment and grow without a haustorium, essential for a biotrophic fungi, as the Laboulbeniales are known to be. The apparent absence of a penetration into the host constitute a huge challenge in the interpretation of the entire biology of Laboulbeniales and their interaction with the host. Ongoing studies on this matter will clarify this discussion.

Archispirostreptus gigas is commonly kept as a pet and goes under the name of “African Giant Black” (AGB). Rickia gigas may infect A. gigas kept in terraria which has long been reported as an aesthetic problem at internet forums and wikis of enthusiasts. The identification of the culprit as a laboulbenial fungus was previously made (Hughes pers. comm.).

Rickia gigas is among the world’s largest Laboulbeniales with thalli surpassing 2 mm in length. Only two species seem to be significantly larger: the largest is Laboulbenia kunkelii (Giard) Thaxt. reaching 4 mm ( Giard 1892) followed by Rhachomyces mattiroloi Colla (= R. longissimus Thaxt. ) with 3.5 mm ( Thaxter 1931). In the same size class as R. gigas we find Rhizomyces canzonerii W. Rossi with 2.1 mm ( Rossi 1990), Rhachomyces giachinoi W. Rossi with 1.9 mm ( Rossi 2006), Trianomyces hollowayanus W. Rossi & A. Weir with 1.85 mm ( Rossi & Weir 1998), Tettigomyces gracilis with 1.5 mm ( Thaxter 1926), Stigmatomyces limnophorae Thaxt. with 1.43 mm ( Rossi et al. 2013), and Filariomyces forficulae Shanor with 1.2 mm ( Shanor 1952). The number of species approaching 1 mm of length is relatively big in the genus Rickia : R. apiculifera Thaxt. , R. biseriata Thaxt. , R. coelostomatis Thaxt. , R. passalina Thaxt. , etc. ( Thaxter 1926).

Additional collections examined: — TANZANIA. E Usambara Mts. Amani, 1000 m, on ‘ Spirostreptus ’ hamatus Demange 1970 ( Spirostreptida , Spirostreptidae ), 1 August 1979, M. Stoltze leg., BCB-SS·E578ac (BCB!), C-F-92242 (C-F!). From pet trade, no further information, on Archispirostreptus gigas , C-F-92226 (C-F!). Pwani region, Kisarawe District, Ruvu South Forest Reserve, on A. gigas (no date and collector information), C-F-95117 (C-F!). Rubeho Mts, forest 5 km SW Madizini, on ‘ S. ’ hamatus , 10–24 September 1993, M. Andersen leg., C-F-95118 (C-F!).

Rickia laboulbenioides De Kesel in De Kesel et al. ( Figs 54–55 )

Described from Cylindroiulus latestriatus (Curtis 1845) ( Julida , Julidae ) from The Netherlands and Belgium ( De Kesel et al. 2013), R. laboulbenioides is very different from any other known species of the genus parasitizing millipedes. It was compared with R. uncigeri in the protologue. The specific epithet seems very appropriate because of the overall resemblance with Laboulbenia , particularly concerning the enlarged terminal portion of median and posterior series of cells of the receptacle, and the greatly elongated primary appendage and supporting cell.

According to De Kesel et al. (2013), the number of cells per series is a: 2, m: 4(–5), and p: (3–)4. If the new material studied is compared with images in the protologue there are some details of the primary appendage as well as others that deserve to be mentioned. We count six cells in the posterior series. The upper part of this series of cells may appear a little disorganized but we suggest that p 5 forms the base for the large cell which supports the primary appendage. This enlarged cell might correspond to cell p 6, located below the primary septum and the primary appendage which consists of the dome-shaped basal cell separated by a darkened and constricted septum from the terminal portion, a conspicuously and filamentous elongated cell very similar to secondary appendages ( Fig. 54 ). The filamentous terminal portion of the primary appendage was not described in the original description, and secondary appendages of our material are much longer than mentioned by De Kesel et al. (2013).

The geographical distribution of this species is extended to Portugal, Spain, Italy and Denmark, in part parasitizing other species of Cylindroiulus . See under R. dendroiuli for the correction of a record from England reported in a web page of images.

Cylindroiulus is a large genus of Julidae . Cylindroiulus punctatus and C. latestriatus are widespread in western Europe, whereas C. perforatus and C. dahli are limited to the Iberian peninsula (plus the Azores Islands for C. dahli ).

Position on host:—Mostly found in the first pair of legs and scarcely over the posterior legs, in case of high infection it is also distributed in the ventral part of the body rings.

Collections examined:— DENMARK. Western Jutland, Nørholm Skov, on Cylindroiulus punctatus (Leach 1815) and C. latestriatus (Curtis 1845) , 23 June 1988, H. Ruhberg leg. ITALY. Veneto, Montello, between Treviso and Belluno, on C. latzeli , 2 August 2010, L. Bonato et al. leg., C-F-95111 (C-F!). PORTUGAL. Algarve, Monchique, on C. perforatus (Verhoeff 1900) , 9 June 1987, P. T. Bailey leg., BCB-SS2686ae (BCB!). Algarve, Cerro da Cabeça, Moncarapacho, Olhão, on a female of Cylindroiulus sp. , 14 February 2015, S. Reboleira leg., C-F-95095 (C-F!). SPAIN. Pontevedra, Eiras, O Rosal, Finca Río Miño, on C. dahli Demange 1970 , 25 March 2004, S. T. Gregory leg., BCB-SS2687 (BCB!).

Figures

FIGURES 16–23. Rickia gigas. Fig. 16. Mature thallus with two mature perithecia; slight geniculation near the darkened foot is seen (arrowhead). Fig. 17. Detail of secondary appendages (arrow). Fig. 18. Detail of mature perithecium. Fig. 19. Detail of antheridia. Fig. 20. Lateral branch of the posterior series of cells. Fig. 21. Perithecial apex at high magnification showing rounded papillae (arrowheads). Fig. 22. Detail of receptacle cells to show the several pores connecting them (see the pointed, triangular or arrow-head sized expansions of cytoplasm in the wall cells). Fig. 23. Mature thallus with up to five perithecia, the two of the left mature, and darkening of lateral branch (arrowhead). (Figs 16, 21, 23, C-F-95086; Fig. 17, SS·E578b; Fig. 18, SS·E576d; Figs 19, 22, SS·E578c; Fig. 20, SS·E576c.) (For interpretation of abbreviations see under materials and methods.) Scale bars for Figs 16 and 23 = 100 μm; for Figs 17, 19, 21–22 = 20 μm; for Figs 18, 20 = 50 μm.

FIGURES 60–66. SEM images. Fig. 60. Rickia candelabriformis, one immature thallus and two sporelings; the arrow points to the septum between the two cells of the primary appendage. Figs 61–65. Rickia gigas; in Fig. 61 a broken foot of a thallus above the scar left by another thallus purposely removed; in Fig. 62 detail of a perithecial apex; in Fig. 63 several thalli showing the flattened appearance of the lateral branches; in Fig. 64 a row of paired antheridia; in Fig. 65 a perithecium showing the two lower tiers of wall cells. Fig. 66. Rickia siddhartha, thalli where arrows point to septa between appendiculate cells and the upper cell of secondary appendages. (For interpretation of abbreviations see under materials and methods.) Scale bars Figs 60–62, 66. = 10 μm; for Fig. 63 = 50 μm; for Fig. 64 = 25 μm; for Fig. 65 = 20 μm.

FIGURES 52–59. Species of Rickia not described in this paper. Figs 52–53. Mature thalli of Rickia dendroiuli. Arrow in Fig. 53 points to the uppermost cell of posterior series, where a diagnostic character is shown (see text). Figs 54–55.Mature thalli of Rickia laboulbenioides. Figs 56–57. Mature thalli of Rickia pachyiuli. Fig. 58. Mature thallus of Rickia siddhartha. Fig. 59. Mature thallus of Rickia uncigeri. (Figs 52–53, WR586; Fig. 54, SS2686d; Fig. 55, SS2686e; Fig. 56, SS·E582b; Fig. 57, SS·E582c; Fig. 58, SS·E601b; Fig. 59, SS·E596c.) (For interpretation of abbreviations see under materials and methods.) Scale bars = 50 μm.