With Notes on Its Distribution and Ecology

AMAZONIANA XV (1/2): st - 66 Kiel, Dezember 1998

Description of Tøulidesmella tabatínga n.sp. (Diplopoda, Polydesmidao Pyrgodesmidae) from Amazon River floodplains, with notes on its distribution and ecology

S.I. Golovatch & J. Adis

Dr. Sergei I. Golovatch, Institute for Problems of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky prospekt, ll707l Moscow V-71, Russia. Priv.-Doz. Dr. Joachim Adis, Max-Planck-Institute for Limnology, Postfach 165, D-24302 Plön, Germany, in cooperation with National Institute for Amazonian Research (INPA), Manaus, Brazil (Accepted for publication: October, 1998).

Abstract

A new pyrgodesmid, Taulidesmella tabatinga n.sp., is described from near lquitos, Peru, from near Tabatinga (an area at the border between Brazil, Peru and Colombia), from the environs of Manaus and from Rio Madeira, Brazil, all these localities lying along the Solimões/Amazon River. T. tabatinga is only a second congener distinct from the type-species T. chanchamayo KRAUS, 1959, from Peru, chiefly by the much larger body size, l2-lobed collum, somewhat differently lobulated paraterga and simpler gonopods. This species, apparently widespread in Amazonian floodplains, represents a "terricolous migrant" which passes the aquatic phase on tree trunks above the water-level and has a low flood lolerance (l < l6 hs).

Keywords: Diplopoda, Pyrgodesmidae, Taulidesmella' cerotegument, plastron, floodplains' Amazon, Neotropics,

Resumo

Um novo pirgodesmídeo, Taulidesmella tabatinga n. sp., é descrito proveniente perto de lquitos, Peru, de Tabatinga (uma área na fronteira entre Brasil, Peru e Colombia), das vizinhanças de Manaus, e do Rio Madeira, Brasil, com todas estas localidades situadas ao longo do Rio Solimões/Amazonas. T. tabatinga é somente o segundo congênera distinguindo-se da espécie-tipo T. chanchamayo KRAUS, 1959, do Peru, principalmente pelo tamanho bem maior do corpo, a coluna l2-lobulada, uma paraterga lobulada de uma forma diferente e gonópodos mais simples. Esta espécie, aparentemente com uma ampla distribuição na Amazônia, representa um "migrante terrícola" o qual passa a fase aquática nos troncos, acima da linha d'água, e mostra uma baixa tolerância de submersão (l < l6 hs).

ISSN 0065-6755/199810571 O MPI für Limnologie, AG Tropenökologie, Plön; INPA, Manaus

56 51 Introduction Description: Length ca. 13 (cr") ro l4-15 mm (9), \,vidrh Ll-1.2 and 3.3-3.4 (cr), and 1.3-1.4 and 3.7- 3'8 mm (9) on midbody pro- and metazona, respectively. Coloration in alcohol generally dark grey-brown, This study continues our assessment of the millipede fauna and ecology of Amazo- variegated with abundant bläckish markings dorsally and laterally; legs and sterna light pinkish-brown. nia, this time being restricted to a new species obviously showing some adaptations to Metaterga mottled spotty, on sides brownish, in vivo with a coating of green algae, beneath yellow-pinkish life in inundation forests. V/ith this remarkable form, a whole guild of millipede species like venter or legs. Vertex blackish, occiput and labrum yellowish, frons and antennae dark brown, latter can be assumed to exist in the floodplain forests of Amazonia, apparently both within almost blackish distally but whitish apically. Distal podomeres increasingly brownish distally. Body with Brazil and Peru, which can be characterized as "terricolous migrants" (cf. ADIS 1997). 20 segments (d, 9). Vertigial region roughly granulorugose, elevated; antennae moderately strongly A number of distribution patterns ranging from the upper Solimões/Amazon River clavate, geniculate between joints 3 and 4; joint 5 much longer and a bit thicker than 6th (Figs. l-2). Collum usual, flabellate, entirely concealing head from above, with l2 lobes at elevated and downstream at least to the Manaus region, central Amazonia, have already been a slightly explanate fore edge, granose throughout and without evident tuberculations; each of caudalmost lobe of observed in millipedes, Pycnoropis tida (cHAMBERLIN l94l) being perhaps the fore margin incomplete, only half as wide as any other in between (Figs. l, 2, 5). Surface superficially hitherto best-known example (GoLovATCH et al. 1997; GoLovATCH et al. 1998). inegularly microgranulate to microtuberculate, dull; micropilosity untraceable obviously due to coating The holotype and the bulk of paratypes of the new species have been deposited in with a cerotegument (see below). Surface of subsequent prozona and ventrolateral parts of metazona the Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus, Brazil, while a few microporose/microalveolate, shagreened, of highly characteristic fine structure (Fig. ). Like collum, paratypes have been retained for the collections of the Museo Historia Natural de la subsequent metaterga basically extremely delicately and densely microgranulate to microtuberculate, more universidad Nacional Mayor de San Marcos, Lima (MHNL), Zoological Museum of the or less strongly tuberculate, with usual three transverse rows ofrounded, relatively low tubercles dorsally State University of Moscow (ZMUM), Senckenberg Museum, Frankfurt a.M. (SMF), and a number of grains/microtubercles both in between and more laterally; dorsal tuberculation pattern Zoologisk Museum, University of Copenhagen (ZMUC), Muséum d'Histoire naturelle, usual, expressed mainly like 2+2 longitudinal rows of somewhat higher tubercles, on somite 19 already Geneva (MHNG), Museo de Zoologia da Universidade de São Paulo (MZSp), and J. like 3+3 rows of even higher tubercles (Figs. 5, 6). Suture between pro- and metazona microalveolate ADrS (CA). almost like on metazona beneath. Dorsum quite convex; paraterga declivent but remaining somewhat higher than level ofventer (Fig. 3), very prominent, with three (on segments l-15, rarely also on segment l6) or four (on segments l6-19, rarely only on segments 17-19) distinct marginal lobes laterally, with Taxonomy gradually reduced (from five to two) distofrontal crenulations and four (of which 2nd from side almost always double) distocaudal crenulations on each side in front of respective lateralmost larger tubercle (Figs. 5, 6). Front and caudal corners ofparaterga invariably rather broadly rounded, caudal corners more Tøulídesmella tabatínga n.sp. (Figs. 1-9) narrowly so, only on somite l9 a little projecting caudad beyond tergal contour (Fig. 7). Caudal tergal limbus with a comb ofvery dense, small, flattened but evident bacilli (Fig.3). Ozopores absent. Epiproct Holotype c," (INPA), Brazil, Edo. Amazônas, near border between Brazil, Peru and Colombia, above (Fig. 7) rather short, trilobated and fully exposed in dorsal view, directed ventrocaudally, surmounted by Tabatinga (4'16'5, 69'56'W), left bank of Amazon/Solimões River, above water-level ot a Cecropia tree a bundle of setae. Subanal scale low and broad, subtriangular, with 1+l strong, rather widely separated, trunk (Cecropiaceae) in whitewater inundation forest during high-water, 16.04.1997, leg. J. ADIS. paramedian setae at caudal comers. Paratypes: 27 ðõ, 15 99 flNPA), I c,', I I (MZSP), I c,., I I (MHNL), I ð, 2 ?? (MHNG), Legs mostly invisible from above, unmodified, relatively long and slender, tarsi only a little longer and 1d,2 ?? (SMF), I ð,2 ?? (ZMUC), 2 ðð,2 99 (ZMUM), 2 ðð,4 99 (CA), same place, date slenderer than femora. Sterna narrow, only between d coxae 3-7 with a paramedian pair of small but and collector, together with holotype; I d, I I (ZMUM), Brazil, Edo. Amazônas, 5 km upstream from evident, setose tubercles. Tabatinga in channel ("furo") of mixedwater inundation forest, on tree trunks above water-level during Gonopods (Figs. 8, 9) in situ either crossing or hÞld subparallel to each other. Coxite relatively large, high-water, 19.03.1998, leg. J. ADIS & S. GOLOVATCH;2 dd,2 CC (MHNL), peru, Depto. Lorero, subglobose, mostly very finely granulate and microsetose, rather densely setose distally. Telopodite environs oflquitos, Rio Nanay (3'42'3, 73'16'W), Padre Cocha, blackish mixedwater inundation forst, on suberect, almost twice as high as coxite, strongly exposed distally, with a relatively large and strongly tree trunks above water-level, 19.04.1997,Ieg. J. ADIS & A. MÁRMOL;2 ðð (MHNL), environs of setose prefemur. Acropodite slender, distinctly and deeply bipartite, with a caudomesal, slightly sinuate Iquitos (3"46'5, 73"15'W), Rio Itaya, Moena Caño, whitewater inundation forest, on tree trunks, solenomerite (sl) only a little shorter and slenderer that a stronger front branch (a). 30.01.1994, leg. e. UÁnMOL; 1 d (INPA), Brazil, environs of Manaus, Lago Janauarí (3'20'5, Epigynal lamina behind I coxae 2 inconspicuous (Fig. l). 60"27'W), mixedwater inundation forest, on tree trunk, 24.0"1.1996: I d (INPA), same locality, in litter, Remarks: The allocation of tabatinga n.sp. in Taulidesmel/a KRAUS, 1959, monotypic, with the 06.03.1997;6 ðè,7 9f [NPA), same locality, on tree trunks, 07.07.1997;40 ðõ,44 9e (INPA), Peruvian T. chanchamayo KRAUS, 1959 as the sole hitherto known congener, is warranted at least for the environs of Manaus, Ilha do Careiro (3'10'S, 59'44'W), whitewater (várzea) inundation forest, on tree time being, as the entire generic classification ofthe Pyrgodesmidae is too badly confused. Indeed, this is trunk, 09.07.1997; I ð, I I QNPA), environs of Manaus, Paraná de Capitarí at Ilha de Curarí (03" l5'S, apparently the only pyrgodesmid genus which is characterized by the ozopores totally wanting combined 59"49'W), várzea inundation forest, on tree trunk, 20.05.199"1; I d (INPA), environs of Manaus, Paraná with 20 body segments, the rather typical pyrgodesmid appearance and, especially, the simple, deeply de Pratarí at Ilha de Pratarí (03"35,60"53'), várzea inundation forest, on tree trunk,07.08.1996; I c,. bipartite, suberect gonopod telopodite (cf. KRAUS 1959). By these features, tabatinga n.sp. is a doubtless (INPA), Brazil, Rio Madeira, Borba (4'24'5, 59"35'W), várzea inundarion forest, on rree rrunks, Taulidesmella. However, the new species differs strongly from T. chanchamayo by the much larger body 31.05.199.1, all leg. K. VOHLAND. size and dissimilar patterns ofboth metatergal tuberculation and lobes. In addition, tabatínga n.sp. displays Name: The specific name emphasizes the type locality. a few, relatively minor, deviations in gonopod structure, e.g. the distally setose coxite, the more simple Diagnosis: Distinguishable fromT. chancharrayo KRAUS, 1959, the type, and only known species, branch a devoid ofadditional outgrowths, the somewhat shorter and slenderer solenomerite, etc. from Peru, by the much larger body size, flatter body, l2-lobed collum, somewhat differently lobed paraterga, simpler gonopods, etc. (see discussion below).

58 59 Distribution and ecology fresh potatoes and flakes of dry frsh ("Tetramin")). Females mostly deposited up to 60 eggs in an egg chamber (cf. HOPKIN & READ 1992),witha "chimney" for ventilation, This appears a diplopod widespread at least in the upper and central parts of Amazo- constructed of clay material and a diameter of about 3 mm. The first juvenile stage (n > nia, where apparently restricted to various kinds of inundation forest. Hence T. taba- 500; body length l.0l t 0.04 mm) hatched and left the egg chamber after one week in tinga n.sp.joins the relatively few examples of millipede species of trans-Amazonian or perforating its wall. The fourth developmental stage was attained about eight weeks similarly vast distribution. Among the Pyrgodesmidae, only Muyudesmus obliteratus thereafter. Due to the somewhat modified mouthparts in T. tabatinga (see above), we KRAUS, 1960, has been reported from near lquitos, Peru down to Belém, Brazil, i.e. suspect that the development of advanced juvenile stages depends, at least in part, on virtually all along the Amazon River, whence it might have been introduced to Europe- the presence of algae in their diet, which was not the case in the laboratory cultures. an hothouses. In white- and mixedwater inundation forests along the Amazon River, between

Tabatinga and Manaus, the aquatic phase lasts 5-7 months. Adults of the tenicolous ?n Acknowledgments tabatinga temporarily climb tree trunks prior to inundation. Here they spend the period of flooding, representing "terricolous migrants" (cf. ADIS 1997). During the day, they We are very grateful to Prof. Dr. Andrés Mármol (Universidad Nacional de la Amazonia Peruana aggregate in groups of up to 200 animals on the bark surface l-2 m above the water- (UNAP), Iquitos, Peru) and Dipl.- Biol. Katrin Vohland (Tropical Ecology Working Group at the Max- level. They blend in well with their background, due to a coating of green algae on the Planck-lnstitute for Limnology (MPIL), Plön, Germany) for having entrusted their material to us for dorsal surface of their cuticula and the generally dark grey-brown colour of their treatment. Prof. Dr. R.L. Hoffman (Virginia Museum of Natural History, Martinsville, USA) and Prof. Dr. William A. Shear (Hampden-Sydney College, Hampden-Sydney/Va., USA) are thanked for valuable mottled spotty metaterga. At night, the adults forage. Their guts contained bark and comments on the manuscript. Dr. Manfred Grasshoff (Senckenberg Museum, Frankfurt, Germany) kindly green plant material, including algae, lichens and moss. During the aquatic phase, adults sent us for revision the holotype oî T. chanchamayo KRAUS, 1959, under his care. ln addition, technical are also found inside termite nests of the trunk/canopy region (K. VOHLAND, pers. assistance of Berit Hansen (MPIL'Plön, Germany) in taking photographs, SEM micrographs and rearing obs.). animals is deeply appreciated. Brigitte Albrecht kindly made the SEM prints and Stephanie Krohn (both The mouthparts (Figs. 10-13) seem to be modified, in showing highly elongate rod- MPIL Plön) helped during the diving experiments. shaped teeth ofthe pectinate lamellae. These are heavily coated by green algae (cf. Figs. 12, 13) which possibly represent a substantial diet, as reported for the pyrgodesmid Gonographis adisi HOFFMAN, 1985, from blackwater inundation forests near Manaus References (cr. ADIS & MESSNER 1997). However, food requirements of juveniles and adults during the terrestrial period are still unknown. ADIS, J. (1997): Tenest¡ial invertebrates: Survival strategies, group spectrum, dominance and activity In the laboratory, adults. of T. tabatinga (9 da,l0 99 from Tabatinga) showed a patterns. - In: JUNK, W.J. (ed.): The Centrâl Amazon floodplain. Ecology of a pulsing system: 299- flood tolerance of I < 16 hs when being submerged in nonaerated water at 22-24 "C 317. Ecological Studies 126, Springer, Berlin: 525 pp. (4.4-6.5 mg Orll) in strainers of metal gauze (width of mesh 0.6 mm). The complete ADIS, J. & B. MESSNER (1997): Adaptations to life under water: Tiger beetles and millipedes. - ln: secretion layer (cerotegument) on the dorsal cuticula, which is supported by small JIJNK, W.J. (ed.): The Central Amazon floodplain. Ecology of a pulsing system: 3 l8-330. Ecological secretion pillars (Figs. 14, l5), does not extend into the coxal region of the sternites, Studies 12ó, Springer, Berlin: 525 pp. ADIS, J., GOLOVATCH, S.I., HOFFMAN, R.L., HALES, D.F. & F.J. BURROWS (1998): Morphotogical where it is incomplete and the spiracles remain uncovered (Figs. 16-19). For this reason, adaptations of the semiaquatic millipede lporodesminus wøllacei SILVESTRI 1904 with notes plastron respiration by means of an air casing held in the cavity between the cerotegu- on the taxonomy, distribution, habitats and ecology ofthis and a related species (Pyrgodesmidae Polydesmida ment and the cuticula is not possible (cf. Gonographis adisi in ADIS & MESSNER Diplopoda). - Tropical Zoology : ll(2): 37 l -387. 1997), as the thin layer of air does not reach the spiracles. The atrium wall of the GOLOVATCH, S.t., HOFFMAN, R.L., ADIS, J., VOHLAND, K. & A. MÁRMOL (1997): On the identity deepened and carries piston-like microtrichia (Fig. However, the outer spiracle is l7). of further two millipede species (Diplopoda) from the environs of Manaus, Central Amazonia,Brazil. - spiracle wall is funnel-shaped deepened, not hemispherically vaulted, and the atrium Amazoniana l4(3 l4): 30 I -309. wall has no cuticular lattice, as found in other polydesmidans inhabiting wetlands (ADIS GOLOVATCH, S.I., VOHLAND, K., HOFFMAN, R.L,, ADIS, J., BACHMANN, L., MÁRMOL, A. & J. & MESSNER 1997). ln adults of T. tabatinga, a small air bubble covering the spiracle TOMIUK (1998): Review of the Neotropical millipede genus Pycnotrop¡r CARL, l9l4 (Diplopoda, opening after submergence dissappeared within 2 hs, thus excluding plastron respiration Polydesmida, Aphelidesmidae). - Amazoniana l5(l/2): 67-102. over a longer period of time. If functional, both piston-like microtrichia and cerotegu- HOPKIN, S.P. & H. READ (1992): The biology of millipedes. - Oxford Univ. Press, Oxford: 233 pp. ment permit a flood resistance due to plastron respiration from several weeks up to KRAUS, O. (1959): Myriapoden aus Peru, VIII. - Senckenberg. biol. 40(516):263-28t. months in polydesmidan species inhabiting wetlands of different climatic zones (ADIS KRAUS, O. (1960): Myriapoden aus Peru, IX. - Senckenberg. biol. 4l(3/4):241-264. & MESSNER 1997; ADIS et al. 1996, 1998). MESSNER,8., ADIS, J. & K.P. ZULKA (1996): Stigmale Plastronstrukturen, die einigen Diplopoden- In the laboratory, T. tabatinga could only be reared up to the fourth developmental Arten eine submerse Lebensweis in kaltem und in fließendem Wasser ermöglichen. - Rev. suisse Zool. 103(3):613-622. stage (15 body segments; offspring of 30 dd & 30 ç9 from Tabatinga; animals kept on bark chips admixed with moist clay at 21127 'C (nighlday) and fed with slices of

60 6t Figs. l-4: Taulidesmella tabatinga n.sp., I paratypes, SEM micrographs. l: anterior body part, ventral;2: head, ventral;3: midbody somite, front;4: fine structure ofventrolateral tegument showing end ofmetazonite (lefÐ, fringe of bacilli on limbus (middle), and next prozonite (right). - Scale bar 300 pm for figs. I a¡d 2.

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Figs. 5-8: Taulidesmella tabatinga n.sp., I (5-7) and d (8) pamtypes, SEM micrographs- 5: anterior body part, dorsal; 6: midbody somites, dorsal; 7: caudal body end, dorsocaudal; 8: gonopods, subventral- É

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Figs. l0-13: '' Mouthparts of Taulidesmella tabatinga n.sp., 9, SEM micrographs. l0: mouthparts opened (dorsofrontal view), showing prominent pectinate lamellae (bottom) and part of molar piece (top); 11: mouthparts semi-closed (frontal view), showing prominent pectinate lamellae (center), labrum (top) and gnathochilarium (bottom); l2 & 13: elongate rod-shaped teeth ofpectinate lamellae (frontal view), coated by algae. ffi I EE F ã 5

Figs. l4-19: Structure ofcuticular cerotegument and ofspiracle in Taulídesmella tabatinga n.sp., 9, SEM micrographs. 14 & 15: Secretion layer (cerotegument) on the dorsal cuticula (tergite 5), supported by small secretion pillars; l6 & 17: funnel-shaped deepened spiracle opening (tergite 7) with piston-like microtrichia covering the atrium wall; 18 & 19: incomplete secretion layer (cerotegument) at base oflegs (sternite 5), supported by small secretion pillars in between the sternal cones.