Microdrile Oligochaeta in bromeliad pools of a Honduran cloud forest.

Zootaxa 3947 (4): 508–526 www.mapress.com /zootaxa / Copyright © 2015 Magnolia Press

Article

ISSN 1175-5326 (print edition)

ZOOTAXA

ISSN 1175-5334 (online edition)

http://dx.doi.org/10.11646/zootaxa.3947.4.3 http://zoobank.org/urn:lsid:zoobank.org:pub:2EA27694-0D0E-40D5-A0F1-EC053A622594

Microdrile Oligochaeta in bromeliad pools of a Honduran cloud forest RÜDIGER M. SCHMELZ1,2, MERLIJN JOCQUE3, 4, 5 & RUT COLLADO2 1

ECT Oekotoxikologie GmbH, Böttgerstr. 2–14, 65439 Flörsheim. E-mail: [email protected] Universidade da Coruña, Fac. Ciencias, Dep. de Bioloxía Animal, Biol. Vexetal y Ecoloxía, Alejandro da Sota, 10; E-15008 A Coruña, Spain 3 Jessica Ware Lab, Rutgers, The State University of New Jersey, 195 University Avenue, Newark, NJ 07102, USA 4 Koninklijk Belgisch Instituut voor Natuurwetenschappen (KBIN), Vautierstraat 29; 1000 Brussels, Belgium 5 Operation Wallacea, Hope House, Old Bolingbroke, Lincolnshire, UK 2

Abstract Phytotelmata, or plant-held water bodies, often house complex aquatic invertebrate communities. Microdrile oligochaetes (Clitellata, Annelida) are known to be part of that community, but specimens are rarely identified to species level. Here we report three species of Enchytraeidae and three species of Naididae from a collection sampled in phytotelms of bromeliads in Cusuco National Park, Honduras. Two species of enchytraeids are new to science. Bryodrilus hondurensis sp. nov. is distinguished from other members of the genus by the high number of ventral chaetae, up to 11 per bundle. The genus is Holarctic and this is the southernmost record so far of a Bryodrilus species. Hemienchytraeus phytotelmatus sp. nov. is distinguished by a combination of characters, among which the huge spermathecae and seminal vesicles are most conspicuous. The genus is common in tropical and subtropical soils around the world. A third species of enchytraeids in the collection, Cernosvitoviella atrata (Bretscher), is redescribed, together with three known species of Naididae, Pristina jenkinae (Stephenson), Pristina osborni (Walton) and Pristina terrena Collado & Schmelz. Presence of ingested debris and humus in the intestine of most specimens suggests that the collected animals live and reproduce in the phytotelms. We provide a list of oligochaete species recorded so far from bromeliad pools in Central and South America. Key words: Clitellata, Enchytraeidae, Naididae, phytotelmata, Cusuco National Park, new species

Introduction In the Neotropics, numerous species of bromeliads are able to hold water in their central tube- or funnel-shaped tanks of tightly overlapping leaves and their lateral leaf axils. These compartments, named phytotelmata (Varga 1928), are plant delineated water bodies, typically filled with water and decaying plant matter. They are developed also in other plant taxa, in Asia for example mostly in the carnivorous pitcher plants (Nepenthes spp.). Phytotelmata frequently house complex aquatic animal communities, ranging from protozoans to vertebrates (Picado 1913; Frank & Lounibos 1983; Frank et al. 2004). These small aquatic habitats have been studied for their specialised fauna and as a brooding site for mosquitoes as vectors of human pathogens. Recently they have received renewed interest due to their potential as model systems to address ecological questions in small but natural ecosystems (Srivastava et al. 2004). There are several overviews of the insect fauna in these habitats (e.g. Frank & Lounibos 1983); a more comprehensive overview of inhabitants in pitcher plants was published by Adlassnig et al. (2011). Less information is available on the non-insect fauna in phytotelmata, but see the overview of Crustacea in phytotelmata (Jocque et al. 2013). Oligochaetes are often recorded from these habitats (Picado 1913; Laessle 1961; Paoletti et al. 1991; Richardson et al. 2000; Carrias et al. 2001; Ospina-Bautista et al. 2004; Jocque et al. 2010), but after the seminal monograph of Picado (1913), they were rarely identified to species level. Both megadrile and microdrile oligochaetes have been found. Four earthworm species belonging to two families were recorded in Picado (1913) from bromeliads in Costa Rica, all identified or described by W. Michaelsen (1912). From 1995 on, a more directed search for earthworms in bromeliad tanks revealed the presence of more species (Righi 1995;

508 Accepted by B. Sket: 26 Mar. 2015; published: 17 Apr. 2015

James 1996, 2004; Csuzdi & Pavliček 2009; Sherlock et al. 2011; Sherlock & Csuzdi 2013). Today some 25 earthworm species from Central and South America are recorded from bromeliad water tanks (Table 1) with several more awaiting description (James & Brown 2006). Microdrile oligochaetes occurring in phytotelmata are much less studied. The taxa recorded belong to Naididae and Enchytraeidae. Well-known in Central American bromeliads is the naidid Aulophorus superterrenus (Michaelsen, 1912) (=Dero superterrena), recorded repeatedly and almost exclusively from bromeliad tanks (Picado 1913; Marcus 1943; Christoffersen 2007). Other finds of microdrile oligochaetes are sporadic and rarely identified to species. Marcus (1943) identified Naidium roseum Piguet in one of the bromeliads investigated in São Paulo. His record was later transferred to Pristina jenkinae (Stephenson) by Sperber (1948). Harman et al. (1988) identified specimens from a bromeliad in Peru as Pristinella (= Pristina) acuminata (Liang). Céréghino et al. (2011) list Pristina menoni (Aiyer), P. notopora Černosvitov and P. osborni (Walton) from bromeliad tanks in French Guiana, identified by N. Giani. As to enchytraeids, we found only one species recorded from bromeliads, Fridericia striata (Levinsen) (Michaelsen 1912; Picado 1913). This record however has been questioned (Schmelz 2003: 329), as reinvestigated reference specimens did not belong to this species. (F. striata is a litter species in European temperate deciduous forests.) B. Healy examined enchytraeid material collected in the studies of Richardson (1999) and Richardson et al. (2000, 2006) and distinguished three morphospecies of the genus Hemienchytraeus. Other papers mention “Nais-like forms" (Laessle 1961), “Enchytraeidae” (Paoletti et al. 1991), or “Haplotaxidae” (Ospina-Bautista et al. 2004). Recently a new species of Pristina was described from the digestive fluid of epiphytic pitcher plants in Borneo (Schenkova & Čermák 2013). In a study of the aquatic communities in bromeliads in Cusuco National Park of Honduras several microdrile oligochaete worms were collected in two sampling campaigns. Results of the morphological investigations are presented in this paper.

FIGURE 1. Map to show the location of the study site.

Material and methods Study site. The samples for this study were collected on two expeditions to Cusuco National Park (CNP), the first in July-August 2006, the second in June-August 2013. CNP is situated in north-western Honduras, within the Merendon Mountain Range (Fig. 1). The core zone of the park consists of lower montane tropical rainforest (a mix of primary and secondary forest), with patches of primary cloud forest and upper montane rain forest that are

OLIGOCHAETA IN HONDURAN BROMELIADS

Zootaxa 3947 (4) © 2015 Magnolia Press ·

509

characterized by high densities of bromeliads. The altitude in the park ranges from 20 to 2244 m asl. Most of the sampling sites were in the core zone of the park, above 1500 m. Here the annual mean temperature is about 14.5°C, average annual precipitation is c. 1800 mm (www.worldclim.org). Sampling and investigation. Animals were collected from bromeliads (Tillandsia guatemalensis and Catopsis spp.). Bromeliads were destructively sampled and rinsed with filtered (64 micrometer) water; animals were picked out alive with a pipette and preserved in 70% ethanol. For a more detailed description of the used methodologies see Jocque et al. (2010). Preserved worms were passed through an ethanol-xylol dehydration series, whole-mounted in Canada balsam between two coverslips, and investigated with a light-microscope equipped with interference contrast optics and a drawing tube. For further details see Schmelz & Collado (2010). Styles of description follow Schmelz (2003) and Schmelz and Römbke (2005). Types and some of the non-type reference material are deposited at the Royal Belgian Institute for Natural Sciences (RBINS) (collective accession number IG 327183). Further non-type reference material remains in the personal collections of R.M. Schmelz and R. Collado. For nomenclatural purposes, the names of the two new species are ascribed to one author (Schmelz). Geographical locations are given in decimal degrees and in square brackets. Paired reproductive organs are described in the singular.

Results The eight species found belong to the genera Bryodrilus, Hemienchytraeus, Cernosvitoviella (Enchytraeidae) and Pristina (Naididae). Included are four known species: Cernosvitoviella atrata (Bretscher), Pristina jenkinae (Stephenson), Pristina osborni (Walton) and Pristina terrena Collado & Schmelz, the latter being the first record after the original description. Two species, one of Hemienchytraeus and one of Pristina, remain unnamed. Two species of enchytraeids are new to science and are described in the following.

Taxonomy Family Enchytraeidae Vejdovský, 1879 Genus Bryodrilus Ude, 1892 Type species: Bryodrilus ehlersi Ude, 1892 (by monotypy)

Bryodrilus hondurensis Schmelz, sp. nov. (Figure 2) Material examined. Holotype. IG 327183-01, adult specimen, unstained whole mount. Honduras, Cusuco National Park, Napacu [15.50834 -88.23274], 2057 m asl, bromeliad tank on the ground. M. Jocque 18/08/2006. Paratypes. IG 327183-02 to IG 327183-04, three adult specimens, unstained whole mounts, same plant and collection data as holotype. Holotype and three paratype specimens strongly contracted, segments 4–6x as wide as long, one paratype specimen less contracted, slightly macerated. Etymology. Named after the country where it was found. Description. Body cylindrical, slightly tapering anteriorly, strongly tapering posteriorly in hindmost 4–5 segments. Holotype 9 mm long and 0.8 mm wide, contracted paratypes 6.5, 8.8 mm long and 0.65, 0.9 mm wide at XII, macerated paratype 15 mm long and 1.0 mm wide at XII. Segment number 53 (holotype), 53, 48 (paratypes), 40 segments in a paratype specimen with regenerated posterior body end. Chaetae distinctly sigmoid, without nodulus, distally pointed and bent, proximally rounded, bend weaker. Chaetae in a bundle arranged in asymmetric fan, chaetae of unequal size, those towards dorsal and ventral midlines of body gradually smaller; largest ventral chaetae c. 70 by 6 μm in II, 90 by 6.5 μm in XI, 100–110 by 6–6.5 μm in caudal segments; maximum number per bundle 10 (3 spms) or 11 (1 spm); chaetal formula 5-8-8-2 : 5-10,(11) -10-3,(2). Chaetae absent at XII; in lateral preclitellar bundles mostly 7 chaetae, in lateral postclitellar bundles mostly 6–7 chaetae, in ventral preclitellar

510 · Zootaxa 3947 (4) © 2015 Magnolia Press

SCHMELZ

bundles mostly 9–10, or 10–11 chaetae, in ventral postclitellar bundles mostly 9–10 chaetae; numbers decreasing in all rows towards posterior end, in lateral bundles from 7 or 8 down to 2, in ventral bundles from 10 or 11 down to 2 or 3. Epidermal gland cells inconspicuous in posterior body half; in preclitellar segments 4–5 rows per segment, density increasing towards anterior end; anterior 4–5 segments completely covered with gland cells except at intersegmental furrows. Dorsal pore at 0/I, a transverse slit.

FIGURE 2. Bryodrilus hondurensis sp. nov. A. Anterior body region. oa, oesophageal appendages; pp, pharyngeal pad, in upright position here due to strong contraction of animal; st, spermatheca; in, intestine in VIII, widened. B. Ventral chaeta from X. C. Spermatheca. Right: Crown of ectal glands. D. Nephridium at 9/10. All drawings from unstained whole mounts.



511

Body wall varying in thickness, dorsally ca. 40 µm, ventrally ca. 80 µm; cuticle thin, 1 µm thick or less; longitudinal muscle layer well-developed. Brain strongly compressed, probably triangular in shape with rounded edges and truncate posterior end. Pharyngeal glands 3 pairs in IV–VI, all with primary ventral lobes, glands in VI largest. Dorsal connection of dorsal lobes not ascertained. Oesophageal appendages in VI, four rounded bodies attached to oesophagus, one pair dorsal, one pair ventral; canals or cavities not ascertained. Nephridia 7 preclitellar pairs, from 4/5 to 10/11; anteseptale elongate, consisting of funnel and parts of nephridial body, tapering towards septum, length c. 50–80 µm, postseptale distinctly larger than anteseptale, exact shape not ascertained; medial rise of efferent duct. First postclitellar nephridia at 13/14. Coelomocytes nucleate, small, broadly oval, about 26 µm long and 21 µm wide, finely granulated, numerous but not filling coelom completely. Gut in contracted specimens widening abruptly in VII or over VII and VIII, lumen filled with dark plant debris from XII, XIII, or XV on. Dorsal blood vessel from XI. Pars tumida of midgut (ventrally inflated gut epithelium) not distinguished. Chloragocytes from VI, as a flat layer, cell height usually below 20 µm, occasionally up to 40 µm; cells conspicuous in preclitellar segments by numerous and minute strong-brown vesicles; cells pale in postclitellar segments. Clitellum from XII–1/2 XIII, extending to level of chaetae of XIII, girdle-shaped, cells in reticulate pattern; hyalocytes absent mid-ventrally, here only granulocytes. Thickness up to 50 µm dorsally, c. 20 µm ventrally, probably less in non-contracted specimens. Hyalocyte diameter c. 10 µm, granulocyte diameter c. 5–6 µm. Seminal vesicle absent, developing sperm dorsally in XI. Mature spermatozoa aligned on top of sperm funnel, ca. 110 µm long, heads ca. 40 µm long. Sperm funnel small, ca. 140 µm long and 90 µm wide, collar about half as wide as funnel body. Vas deferens densely coiled ventrally in XII, between sperm funnel and male glandular bulb. Bursal slit longitudinal, male glandular bulb spherical, diameter ca. 80–85 µm, pierced centrally by vas deferens. Subneural glands absent. Spermathecae. Ectal pore a transverse slit laterally at 4/5, slightly below longitudinal line of lateral chaetal bundles. Ectal glands as a crown of ca. 8 glands, diameter of crown 1.2–1.5x ectal duct diameter. Ectal duct short and thick, diameter 40 µm, c. 2.5x as long as wide, thick-walled, surrounded by musculature; duct canal narrow, gradually widening into ampullar lumen; ampulla not or only slightly wider than ectal duct, with thin epithelium, spherical or ellispoid, continued into narrow, elongate, thin-walled ental duct that extends towards body center dorsally of oesophagus. Communication of ental ducts and dorsal attachment to oesophagus not ascertained. Remarks. All visible details comply with the genus diagnosis of Bryodrilus: head pore at 0/I, chaetae sigmoid without nodulus, pharyngeal glands without secondary glands, nephridial anteseptale short, and above all, two pairs of compact oesophageal appendages in VI. The sudden gut enlargement disagrees with the genus diagnosis but is most likely a fixation artefact. Within the genus Bryodrilus, B. hondurensis sp. nov. is most easily distinguished by (1) the high number of chaetae per bundle. The majority of the other 15 Bryodrilus species described so far have a maximum of 4, 5 or 6, rarely 7 or 8, chaetae per bundle, not 10 or 11 as B. hondurensis. All other diagnostic characters occur in other species of the genus as well, but not in such a combination: (2) Seven pairs of preclitellar nephridia, from 4/5 to 10/ 11, (3) nephridial anteseptale elongate, (4) seminal vesicle absent, (5) spermatheca with large crown of ectal glands, (6) short ectal duct, and (7) ampulla without diverticula. The number of preclitellar nephridia (7 pairs, from 4/5 to 10/11) is unusually high but shared by B. fuscistriatus Chen & Xie, 2006 from northeastern China and the boreal-temperate holarctic B. ehlersi Ude, 1892 (see redescription in Cech et al. 2012). Some differences of these species from B. hondurensis, apart from the chaetae, are as follows. B. fuscistriatus: spermathecae with two diverticula, seminal vesicle large, extending over 3 segments. B. ehlersi: nephridial anteseptale short, consisting almost of funnel only, spermathecal ectal gland small, not circumferal, ectal duct elongate. Xie et al. (2000) describe seven pairs of preclitellar nephridia in specimens from north-eastern China identified as Bryodrilus parvus Nurminen, 1970. According to Dózsa-Farkas et al. (2012), B. parvus has 5 preclitellar pairs, from 6/7 to 10/11, therefore the species in Xie et al. (2000) is a different, probably new, species. Dózsa-Farkas et al. (2012) reinvestigated types of B. parvus, and they recognized the species as a junior synonym of B. librus (Nielsen & Christensen, 1959), based on morphological and DNA data. B. parvus sensu Xie et al. (2000) differs from B. hondurensis in smaller body size (3.5–4.7 mm), fewer segments (32–38) and chaetae (up to 6 per bundle), among other characters. Several details remain unknown or incompletely known and require further investigation from living or properly fixed material: Colour and texture in vivo of coelomocytes and epidermal gland cells, shape of brain, details of pharyngeal glands and postclitellar nephridia, presence/absence of lumina in the oesophageal


SCHMELZ

appendages. There is probably a mid-dorsal connection of the spermathecae as in all other species of the genus (except in Bryodrilus librus, where blind-ending spermathecae occur, see Dózsa-Farkas et al. 2012 for a recent review), but this remains to be confirmed. Other peculiarities are likely fixation artefacts: The sudden gut enlargement at VII or VIII is probably caused by the strong contraction of the animals and not present in vivo. Piper et al. (1982) and Christensen & DózsaFarkas (1999) observed the same in preserved specimens of other Bryodrilus species. A gradual gut enlargement is part of the genus diagnosis of Bryodrilus and one of the characters that separate it from Henlea, a genus with abrupt gut enlargement. Furthermore, the spermathecal ectal pore, a transverse slit in our specimens, may be rounded and widened in living material. Spermathecae may be more slender than seen here; the ectal duct is coated with musculature and most probably maximally contracted. And of course, body dimensions of living specimens will be different: we expect an adult live body length of about 20 mm and a diameter of 0.5 mm. The gut of all specimens is filled with dark-brown, amorphous, humic organic matter, interspersed by fragments of sclerotized plant remains such as tissue walls, spines, twiglets or rootlets. No algal remains (e.g. diatom shells) were found. The worms appear to feed on the humus accumulating on the bottom of the phytotelmata. This is the southernmost record of a Bryodrilus species. The genus is most diverse in arctic to subarctic regions of Siberia, Alaska, Canada and Greenland. Only one species, B. ehlersi Ude is widely distributed in temperate regions. Three species are described from north-eastern China (B. longifistulatus Xie, Liang & Wang, 2000, B. macrotheca Xie, Liang & Wang, 2000, B. fuscistriatus Chen & Xie, 2006). Up to now the most southern record of a Bryodrilus species was from western Florida by Healy (1996) (B. novaescotiae Bell, 1962, originally described from Nova Scotia, Canada).

Genus Hemienchytraeus Černosvitov, 1934 Type species: Enchytraeus stephensoni Cognetti, 1927 (nom. nov. pro Enchytraeus cavicola Stephenson, 1924 non E. cavicola Joseph, 1880)

Hemienchytraeus phytotelmatus Schmelz, sp. nov. (Figure 3) Material examined. Holotype. IG 327183-05, adult specimen, unstained whole mount. Honduras, Cusuco National Park, Napacu [15.50834 -88.23274], 2057 m asl, bromeliad tank on the ground, M. Jocque 18/08/2006. Paratypes all from same locality, all unstained whole mounts: IG 327183-06 to IG 327183-10, 5 adult specimens, same data and same plant as holotype. IG 327183-11 to IG 327183-15, 4 adult specimens, 1 subadult, [15.50541 88.23648], 2025 m asl, bromeliad tank on the ground, M. Jocque 13/08/2006. IG 327183-16 to IG 327183-20, 5 adult specimens [15.50723 -88.23363], 2061 m asl, M. Jocque 11/08/2006. Further non-type material, in the 1st author's collection: 40 specimens, unstained whole mounts, 20 adult, 8 subadult, 2 juvenile, complete or posteriorly incomplete, same location as types series, M. Jocque 06–18/08/2006; 5 specimens, 3 adults, 1 subadult, 1 juvenile, [15.505813 -88.21473], 2061 m asl, M. Jocque 29/06/2013. Etymology. Named after the habitat where the species was found. Description. Animals strongly contracted and bent inward, some specimens bent into a circle. Body length 9.5–12 mm, diameter 0.4–0.5 mm. Segment number of adults with complete posterior end 44–66 (n = 17); 12 specimens with 51–57 segments. Chaetae 2 per bundle (occasionally 3, 1, or 0), absent at XII, lateral chaetae smaller than ventral chaetae in a segment. Anterior chaetae straight distally and with proximal hook, posterior chaetae straight proximally and with distal bend. Chaetae in caudal segments almost twice as large as preclitellar chaetae. Ventral preclitellar chaetae c. 50 µm long and 5 µm thick, ventral caudal chaetae 80–90 µm long and 8 µm thick. Chaetae smallest immediately behind clitellum (30 : 3 µm laterally, 40 : 4 µm ventrally), gradually increasing in size posteriad; from about XXX on distinctly larger than preclitellar chaetae. Head pore on prostomium mid-dorsally. Epidermal gland cells one row per segment, at chaetal level; from VIII on towards anterior end increasingly more glands per segment; peristomium and posterior half of prostomium completely covered with gland cells. OLIGOCHAETA IN HONDURAN BROMELIADS


513

FIGURE 3. Hemienchytraeus phytotelmatus sp. nov. A. Anterior body region, anterior 16 segments, lateral view, schematic. er, ental reservoir of spermatheca; oo, oocytes; pp, pharyngeal pad; sl, secondary pharyngeal gland lobes in V and VI; sv, seminal vesicle. B. Nephridia at 6/7, 7/8. C. Ventral chaetae, from a caudal segment (left) and from V (right). D. Male efferent apparatus with sperm funnel, vas deferens and male copulatory organ. E. Ectal part of spermatheca. ct, connecting tube; eb, ectal bulb of ampulla; tr, transition from connecting tube to ental reservoir. All drawings from unstained whole mounts.

Body wall thickness varying between 12 µm (dorsally, hindmost segments) and 50 µm (ventrally, foremost segments); thickness mostly ca. 20 µm; cuticle very thin, less than 1 µm, longitudinal muscle layer always welldeveloped. Brain deeply incised anteriorly, slightly concave or almost straight posteriorly, about as long as wide (c.


SCHMELZ

80–100 µm) when tip of anterior incision is taken as reference. Ventral nerve cord apparently medullar. Oesophageal appendage with at least 4–5 terminal branches on each side. Pharyngeal glands with secondary ventral lobes in V and VI, lobes equally large and spherical. Dorsal lobes united in IV–VI, separate in IV or VI in single specimens. Preclitellar nephridia 4 pairs, from 6/7 to 9/10; anteseptale and postseptale rounded, length ratio 3 : 4, constriction at septum; subterminal rise of efferent duct, no terminal vesicle seen. First postclitellar nephridium from 13/14. Dorsal blood vessel origin not seen in most specimens; origin in XII in one submature specimen. Pars tumida of midgut (ventrally inflated gut epithelium) in XXVIII–XXXVI, extending over 4 to 5 segments. Clitellum short, in XII and anterior parts of XIII, not reaching chaetae of XIII; girdle-shaped, mid-ventrally only granulocytes in indefinite rows; hyalocytes and granulocytes alternating dorsally and laterally down to level of bursal slits, pattern reticulate (dense rows in one specimen). Border cells with an outer ring of granular cells and an inner ring of hyaline cells. Seminal vesicle very large, extending over 3 to 7 segments in adults, behind clitellum down to XVI (XVII), in preclitellar segments from IX, X or XI, occupying much coelomic space in these segments. Spermatozoa ca. 200 µm long, heads ca. 15 µm long. Sperm funnel convoluted, about as long as body diameter, tapering distad, proximally c. 80–100 µm wide; collar wider and with flap-like extensions to which spermatozoa are attached. Vas deferens in XII ventrally, coiled into dense isodiametric spirals. Male copulatory organ: Bursal slit longitudinal, outer margin like an elongate E. Male glandular bulb spherical, diameter c. 80 µm. Dorso-ventral copulatory muscles conspicuous, strands present in all of XII, anterior and posterior strands inserting ventrally in body wall, central strands penetrating male glandular bulb. No subneural glands or other epidermal modifications. One to four eggs mature at a time, in various positions, seen from XI to XVIII, in one or two consecutive segments, in same segments as seminal vesicle or behind. Spermatheca. No ectal gland. Ectal duct c. 120–150 µm long, 10–14 µm wide distally and 16–18 µm wide proximally, canal narrow, diameter c. 1.5 µm; ampullar ectal bulb inconspicuous, c. 25–26 µm wide, thick-walled, with few spermatozoa present. Connecting tube extending into VIII or IX, narrower than ectal bulb, length c. 350– 400 μm, widening towards ental reservoir, and with meandering, often sperm-filled canal widening entad as well. Ental reservoir thin-walled, very large, extending over 2–4 segments, present in VII to X, mostly VIII–IX, and with diameter up to 2/3 body diameter, sperm arranged in distinct but loose packages with smooth and wavy outline. Remarks. Hemienchytraeus phytotelmatus sp. nov. is recognized by the following combination of characters: (1) huge spermathecae and seminal vesicles, (2) pharyngeal glands with secondary lobes in V and VI, (3) oesophageal appendages with 4–5 terminal branches, (4) 4 pairs of preclitellar nephridia, from 6/7 to 9/10, (5) clitellum girdle-shaped, (6) male glandular ("penial") bulb present, small. Most conspicuous are the huge masses of sperm accumulated in 10–11 segments of the anterior body region, first allosperm of the spermathecae, followed by mature or developing sperm in the seminal vesicles. Five out of the 23 currently accepted species of Hemienchytraeus (Schmelz & Collado 2012) share the most conspicuous traits of H. phytotelmatus, the huge spermathecae and seminal vesicles: H. loksai Dózsa-Farkas, 1989 from Ecuador and Peru, the two Brazilian species H. cipoensis Righi, 1973a and H. makusi Righi, 1988, and the two Central African species H. africanus Černosvitov, 1938 and H. shirensis Bell, 1954. The differences of these species from H. phytotelmatus are as follows: H. loksai is densely covered with epidermal gland cells, there are 5 preclitellar pairs of nephridia, from 5/ 6 to 9/10, and 3 secondary pharyngeal gland lobes, in V, VI, and VII (Dózsa-Farkas 1989; Schmelz & Collado 2007). H. cipoensis has short and simple oesophageal appendages without secondary or tertiary tubes, the clitellum is saddle-shaped, and male glandular bulbs are absent (Righi 1973a). H. makusi is without epidermal gland cells, secondary pharyngeal gland lobes are absent, and sperm in the ental reservoir of the spermathecal ampulla is arranged in numerous discrete and digitiform packages (Righi 1988). The dorsal blood vessel originates in XV, but this trait was not well-distinguished in our specimens. H. africanus is larger (up to 17 mm in fixed state), with more segments (up to 72), chaetae are smaller posteriorly than anteriorly, and there are two large accessory male glands in front of and behind a small male glandular bulb (Černosvitov 1938). H. shirensis has a very thick body wall (1/4 worm diameter), a clitellum extending over 2 segments (from the chaetae of XI to the chaetae of XIII), and nephridia with very small anteseptale and large and bilobed postseptale (Bell 1954). Knowledge of several characters in the new species is unsatisfactory, due to the fact that only ethanolpreserved material was available. Especially important is form and branching pattern of the oesophageal appendage, one of the main diagnostic characters at the genus and species level. In specimens that have not been anaesthetized prior to fixation, these delicate tubes are usually too much compressed and convoluted to be observed



515

and described properly. In one specimen of the type series the following was distinguished: Unpaired trunk, elongate primary branches, longer than trunk, c. 3x as long as wide (80–90 μm long, 23–29 μm wide), and 4–5 terminal branches on each side, narrower than primary branches (14–17 μm wide). Terminal branches appear to be tertiary, i.e. branching off short bifurcated stump-like secondary branches. One subadult specimen has a regenerating anterior end. From segment VIII on anteriad, 5 segments are being regenerated. Body diameter is smaller here, and organs are not yet fully developed. The ental reservoir of the spermathecae is present in VIII and IX, but the ectal part is missing, and there is no connection of the organ with the exterior. It seems that the worm's anterior end was bitten off when fully mature, and then regenerated.—In juvenile specimens the size difference between anterior and posterior ventral chaetae is less marked, e.g. 50 : 4.5 μm vs. 60 : 5 μm.—The gut of all specimens is filled with plants remnants in decomposition and small amounts of amorphous humus. Healy (in litt.) distinguished three unnamed species of Hemienchytraeus collected in bromeliads of Puerto Rico together with Aulophorus superterrenus (Richardson et al. 2000). In one of them the described details agree with H. phytotelmatus : "54–56 segments … large spermatheca with simple duct, large, flared, sperm funnel, large seminal vesicle extending back for several segments and smallish penial bulb" (Healy in litt.).

Hemienchytraeus sp. 1 Material examined. IG 327183-21, juvenile specimen, Honduras, Cusuco National Park [15.506299 -88.23704], 1457 m asl, M. Jocque 07/07/2013. Description. Length 1.5 mm, diameter 0.12 mm at V, 0.15 mm at XIII; 21 segments. Two chaetae per bundle, distally straight; chaetae slightly enlarged in caudal segments, ventrally c. 45 : 4 μm in caudal segments, max. c. 35–40 : 3.5 μm in anterior segments. Ventral chaetae thicker than lateral ones, length of laterals not measurable. Epidermal glands inconspicuous, one row of pale enlarged cells at level of chaetae. Oesophageal appendages bifurcating twice, with two elongate secondary branches on each side. Pharyngeal glands 3 pairs in IV–VI, all connected dorsally, a pair of small secondary ventral lobes in V. Dorsal blood vessel from IX, midgut pars tumida in XV–XVI. Five pairs of preclitellar nephridia, from 5/6 to 9/10, anteseptale as large as postseptale, c. 25 μm long. Coeolomocytes very scarce, small, length c. 10 μm. Remarks. This juvenile specimen cannot be identified to species, but by virtue of the oesophageal appendages, the pharyngeal glands and the preclitellar nephridia it belongs to a species different from H. phytotelmatus sp. nov.

Genus Cernosvitoviella Nielsen & Christensen, 1959 Type species: Marionina atrata Bretscher, 1903

Cernosvitoviella atrata (Bretscher, 1903) Marionina atrata Bretscher, 1903: 17. Enchytraeoides atratus (Bretscher). Černosvitov 1928: 14–16, text fig. 3, pl. 1 figs 8, 9. Cernosvitoviella atrata (Bretscher). Nielsen & Christensen 1959: 38–39, figs 15–18. Chalupský 1992: 140–141, fig. 7. Rota & Healy 1999: 31. Timm 2009: 148–149. Schmelz & Collado 2010: 57, 62.

Material examined. IG 327183-22, one adult specimen, unstained whole mount. Honduras, Cusuco National Park [15.505813 -88.21473], 2061 m asl, M. Jocque 29/06/2013. Description. Length 1.8 mm, diameter at V 0.12 mm, 0.17 at XII, 0.1 mm at XX, 23 segments. Chaetae sigmoid with nodulus, formula 4,5-4,3 : 5,6-4,3. Length c. 25 μm, diameter c. 1.5 μm in caudal segments, chaetae appear smaller in anterior segments, length not measurable. Lateral chaetae slightly shifted dorsally, bundles completely in dorsal body half; distance of dorsal bundles to lateral line about half of that of ventral bundles (c. 17 vs. 33 μm). Epidermal gland cells not seen, circumferal epidermis somewhat rugose at chaetal level. Body wall 4 μm thick dorsally, up to 6 μm ventrally. Prostomium 60 μm high at base, 45 μm long, hollow, very


SCHMELZ

few transverse muscles inside, no papillae or protrusions, inner epithelial surface slightly wavy. Prostomium separated from peristomium by a medial dorsal-ventral ligament (musculature?). Dorsal and ventral chaetal bundles of one side in a segment interconnected with two transverse intracoelomic ligaments, possibly retractor muscles. Brain deeply incised posteriorly, 95 μm long, width not measured. No oesophageal appendages, no intestinal diverticula. Four pairs pharyngeal glands, two primary pairs in IV, V, broadly attached to dorso-anterior face of respective septa, two ventral secondary pairs in V, VI, larger than primary glands, immediately behind but not attached to septa. Chloragocytes from V, dense coverage from VIII, cell diameter c. 10 μm. Dorsal blood vessel from XIII, anterior bifurcation prostomial. Midgut pars tumida not distinguished. Ventral nerve cord medullar, with promiment segmental lateral swellings in IV–VI, swellings continuing in VII f., but gradually fading out. Preclitellar nephridia unpaired at 6/7 and 8/9 to the left, at 8/9 to the right. Anteseptale an elongate funnel, postseptale covering entire segment length, lobed, loops of canals visible. Coelomocytes few in number, different anteriorly and posteriorly; in anterior segments small and inconspicuous, oval to rhomboid, with fine irregular vesicles, length c. 12 μm; in hindmost 4 segments an aggregation of larger cells, length 16–19 μm, with conspicuous large vesicles of equal size at periphery; both types nucleated. Clitellum absent ventrally and dorsally, in XII–XIII, 2 complete segment lengths, beginning 1 epidermal cell row behind chaetae of XI, ending 1 cell row behind chaetae of XIII, consisting of c. 31 transverse rows. Seminal vesicle absent, few cysts free dorsally in XI. Sperm funnel funnel-shaped, 2x as long as wide, c. 30 μm long, tapering from 15 μm entally to 8 μm near septum; vas deferens thin-walled, widened to 6–8 μm diameter behind septum 11/12, narrowing ectally to 3.5 μm diameter near ectal pore. Male pores on body surface, with irregular glandular mass (diameter c. 16 μm) surrounding most distal part of vas deferens. One mature egg. Spermathecae not attached to oesophagus, a simple tube c. 4x as long as wide, with ectal duct 8–10 μm wide and elongate ampulla 10–12 μm wide; no glands or other modifications near ectal pore. Remarks. Cernosvitoviella is a Holarctic aquatic genus, common in temperate and boreal sediments of limnic and river habitats, and in moist soil. Its presence in phytotelmata of a tropical cloud forest is surprising from a biogeographical point of view but not in contradiction with the known habitat requirements. There are few records of the genus outside the Holarctic. Botea (1983) identified a single specimen from groundwater habitats in Cuba as "Cernosvitoviella sp." but the illustrations (Botea 1983, fig. 18A,B) show a specimen with only two chaetae per bundle, which suggests that the specimen was misidentified. Reference material is no longer available (V. Pop. pers. com.). Cernosvitoviella has further been recorded from rain forest soil in Papua New Guinea (Standen 1988). Recently it was also found in peat soil on mountain peaks of the Mata Atlântica in Paraná, Brazil (R. Schmelz, C. Niva, unpublished). We consider our find as the first record of the genus from Central America. The single specimen is well-preserved and allows investigation of all relevant characters except presence/ absence of dark coelomocyte granules, seen only in living specimens. Our identification of specimens as C. atrata is mainly based on the shape of the spermatheca and the male efferent apparatus, the latter matching closely the redescription in Nielsen & Christensen (1959, Fig. 18, reproduced in Schmelz & Collado 2010). Further characters also fit the species diagnosis: coelomocytes differing in shape anteriorly and posteriorly, clitellum open ventrally and dorsally (Schmelz pers. obs.), 2+2 pattern of pharyngeal glands. C. atrata is highly variable and probably a species complex (Timm 2009, Schmelz & Collado 2010). Several forms which may be separate species have been distinguished, based on body size, coelomocyte variations and size of spermathecae (Nielsen & Christensen 1959, Chalupský 1992), but none of the forms are well-described; furthermore the original description (Bretscher 1903) is poor and there are no types. Therefore it remains undecided whether this Honduras specimen belongs to one of the microspecies within C. atrata as known from the northern hemisphere, which would suggest a cosmopolitan distribution, or whether it is a species of its own. Nevertheless, referring to current taxonomic knowledge, this specimen belongs to C. atrata.

Familiy Naididae Ehrenberg, 1828 Subfamily Pristininae Lastočkin, 1924 Genus Pristina Ehrenberg, 1828 Type species: Pristina longiseta Ehrenberg, 1828



517

Pristina terrena Collado & Schmelz, 2000 Pristina terrena Collado & Schmelz, 2000: 513–514, figs 8, 9.

Material examined. Five specimens, sexually immature, IG 327183-23 to IG 327183-27; one specimen with budding zone and primordial testes in VIII and primordial ovaries in IX. Cusuco National Park, Honduras, [15.505813 -88.21473, 15.506299 -88.23704, 15.522537 -88.27598, 15.513245 -88.28807, 15.526152 -88.27662], respectively 2061 m, 1457 m, 1558 m, 1468 m and 1587 m asl, M. Jocque 07/07/2013 to 06/08/2013. Further 6 specimens in the 3rd author's collection, [15.52425 -88.28853, 15.50731 -88.29428], respectively 1659 m, 1347 m asl, M. Jocque 07/08/2006. Description. Body length 1–2 mm, diameter 0.1–0.14 mm. Segment number of complete specimens 17–24 (17, 17, 19, 20, 24). Budding zone present in two specimens, between chaetae of XVII and XVIII (specimen with 24 segments) or XIV and XV (specimen with 20 segments). Posterior zooids with 6 or 7 segments. Dorsal bundles with 1 or 2 elongate, serrate hairs and 1 or 2 simple-pointed needles; more often just one hair and one needle per bundle. Hairs up to or more than three times as long as body diameter, increasing from II to VII to maximum length. From VII on, hair length 240–340 μm, varying among bundles, segments and specimens. Hair length slightly reduced in hindmost 2 segments, not as much as in foremost segments. Hairs c. 2 μm thick at base, tapering continuously ectad, less than 1 μm thick at tip; serration distinct at x250 magnification on convex side of bent chaeta, serration 'teeth' > 1 μm apart, distance between teeth wider at base than towards the tip. Needles tightly attached to proximal hair shaft and not always well-distinguished, c. 40 μm long, straight without nodulus, about 1.5 μm thick in ental 4/5, strongly thinning out in ectal 1/5, bent backwards towards hair, ectal tip parallel to hair shaft. Tip simple-pointed at x1000 magnification but somewhat widened. Chaetal follicle conspicuous, diameter c. 15 μm. Ventral chaetae all alike, 37–40 μm long, bifid, nodulus as a faint swelling at c. 2/5 from distal tip, teeth short, about 1.5 μm long, upper tooth minutely shorter and thinner than lower; chaetae straight distally, only teeth bent here; proximal third of chaetae bent in opposite direction of teeth; in II 6–9 chaetae per bundle, varying among specimens, 5–7 in II–XI, in posterior body half 3–5 per bundle, decreasing posteriad from 5 to 4 or from 4 to 3. Prostomium without proboscis, rounded, longer than wide in one specimen, wider than long in all others (c. 50–70 μm long and 70–80 μm wide). Prostomial epithelium with several bilateral-symmetrical protuberances projecting entad into prostomial lumen, protuberances larger ventrally near mouth opening than dorsally, absent mid-ventrally. Epidermal gland cells seen in some specimens, laterally of and level to dorsal chaetal bundles. Pharyngeal pad with tenuous protractor and retractor muscles. Pharyngeal glands in separate packages at 3/4, 4/5, and 5/6, enclosing septa. Gut diameter abruptly widened behind septum 6/7, from c. 80 to 180 μm, not constricted in following segment (i.e. no stomach distinguishable), no cells with intracellular 'stomachal' canals distinguished. Dorsal blood vessel large in VI (and V), not seen posteriorly. Three simple and unbranched commissural vessels observed near 2/3, 3/4, 4/5. Pars tumida of midgut present. First nephridium in VII, unpaired. Most of following nephridia unpaired as well, on alternating sides, 10 nephridia counted altogether in a specimen with 20 segments. Nephrostome present, on anterior face of 6/7 ventro-laterally; wide and densely packed loops in all of VII, dorsally and ventrally. Nephropores ventral, anterior to ventral chaetal bundles. Coelomocytes spherical, diameter 6–10 μm, with glassy irregular texture, vesicles not distinguished. Remarks. Our specimens agree in all diagnostic details with Pristina terrena Collado & Schmelz, 2000. Noteworthy are the long serrate hairs that increase in length from II to VII and vary in length from VIII on, seemingly simple-pointed needles without nodulus and a tapering distal fifth bent towards the hair, and ventral chaetae that differ very little in size and shape between anterior and posterior bundles, with short and more or less equal-sized teeth. Further similiarities of P. terrena extend to body size, segment number, blood vessels, blood commissurals, and location of the first nephridium. The only difference of possible taxonomic importance is the widening of the intestine, described as gradual in P. terrena and abrupt in our specimens. However, the latter is a fixation artefact due to strong contraction of the animals when fixed in ethanol. We reinvestigated non-type ethanol-preserved reference specimens of the original series from Collado's personal collection (see Collado & Schmelz 2000), and there the intestine shows an abrupt widening as well. A stomach was not seen in the Honduras material and is absent in P. terrena as originally described. The coelomocyte granulation, conspicuous in living specimens, is no longer seen in ethanol-preserved material, but the non-type reference material (see above) has the same irregular glassy texture without distinct vesicle; such a pattern can be indicative of coarse refractile granules as seen in live P. terrena. The same correspondence has been observed in enchytraeids (comp. Rota 2013).


SCHMELZ

This is the first record of P. terrena after the original description from rain forest soils near Manaus, Brazil. The distance of approx. 3500 km between the two localities may suggest an extremely good dispersal ability of the species, but P. terrena may also be common and widespread in Central and South America. Records of Pristina in Central and South America are scarce and mostly restricted to limnic, river and groundwater habitats, where this soil-dwelling species may not occur. Pristina species were regularly found in a non-flooded ("terra firme") primary forest plot of Amazonia, with six species described or recorded so far (Collado & Schmelz 2000, 2001, 2002; Augustsson 2001) and also in the Mata Atlântica of the Brazilian State Paraná (Römbke et al. 2005).

Pristina jenkinae (Stephenson, 1931) Naidium jenkinae Stephenson, 1931: 39–41, text fig. 1. Naidium roseum Piguet. Marcus 1943: 130–131, pl. 25 fig. 105, pl. 26 fig. 106. Pristina jenkinae (Stephenson). Sperber 1948: 224–225. Brinkhurst 1971: 396, fig. 7.23A–B. Timm 2009: 74–75. Pristina idrensis Sperber, 1948: 220–222, fig. 23D–F, pl. 20, 21 fig. 1. Timm 2009: 74–75. Pristinella jenkinae (Stephenson). Brinkhurst 1985: 472. Kathman 1985: 1022–1026, fig. 1a–j. Pristina taita Stout, 1956: 99–101, figs 5–7. Pristina nothofagi Stout, 1958: 289–292, figs 1–6.

Material examined. Five specimens, unstained whole mounts, IG 327183-28 to IG 327183-32, [15.49735188.21247, 15.513328 -882.1247, 15.530322 -88.27633], 2070 m, 1670 m and 1608 m asl, respectively, M. Jocque 06/08/2013. Two anterior zooids, incomplete posteriorly, two posterior zooids, one specimen complete with regenerating anterior end. Description. Specimens strongly contracted, ill-preserved, diameter c. 0.24 mm. Prostomium without proboscis. Dorsally one hair and one needle per bundle, needles with parallel teeth, lower c. 2x as thick and long as upper, hair chaetae max. 20 μm long. Ventral chaetae bifid, 5–7 per bundle anteriorly. Pharyngeal glands in IV, V, discrete packages, stomach in posterior of VI and in VII. Coelomocytes spherical, diameter 6–10 μm. Remarks. This cosmopolitan freshwater species has one previous record from bromeliad tanks in Brazil (Marcus 1943: 131). Specimens were identified as Naidium roseum Piguet but later considered to be P. jenkinae (Sperber 1948). There are also several records from forest soil habitats (see below, discussion), beginning with Stout's descriptions of P. taita and P. nothofagi from New Zealand, both synonymized with P. jenkinae by Kathman (1985). Several authors (Marcus 1943; Righi & Hamoui 2002; Van Haaren & Soors 2013) consider P. jenkinae a junior synonym of P. rosea Piguet, 1906, but we prefer to follow Timm (2009) who maintains P. jenkinae as a separate species. Comparing the original descriptions (Piguet 1906; Stephenson 1931), the intestine widens in VIII in P. rosea and in VII in P. jenkinae; this seems to make a clearcut difference, apart from the much-debated differences in details of the chaetae. The taxonomy of P. jenkinae and its possible synonyms is problematic (Collado & Schmelz 2001; Righi & Hamoui 2002; Van Haaren & Soors 2013) and in need of revision. The visible details in the Honduras specimens agree with specimens from soil sites in the Brazilian Amazon (Collado & Schmelz 2001) and the Mata Atlântica (Schmelz, unpublished), studied in vivo and identified as P. jenkinae. In these specimens the stomach widens in the posterior of VI and in VII, and commissural vessels in I–III are simple, not anastomosing; both details disagree with the diagnoses of P. rosea (Piguet 1906; Sperber 1948).

Pristina osborni (Walton, 1906) Naidium osborni Walton, 1906: 703–705, fig. 12. Naidium minutum Stephenson, 1914: 327–329, figs 4, 5. Pristina minuta (Stephenson). Sperber 1948: 222–223. Pristina osborni (Walton). Brinkhurst 1971: 395, fig. 7.22N–P. Righi & Hamoui 2002: 144–145. Timm 2009: 70–71. Pristinella osborni (Walton). Brinkhurst 1985: 472.

Material examined. One juvenile specimen, not contracted, unstained whole mount, IG 327183-33 [15.512632 -88.28871], 1545 m asl, M. Jocque 06/08/2013.



519

Description. Length 0.7 mm, diameter max. 0.1 mm. 12 segments; specimen is an anterior zooid, posterior part missing. Dorsal and ventral chaetae from II, 1 hair and 1 needle per bundle dorsally, ventrally 3–4 bifids. Hairs smooth, max. length 120 μm, c. 60 μm in II, increasing in size from II to VI; needles bifid with very short equally long teeth diverging at wide angle. Ventrals with teeth equally long, length 24 μm in II, 32 μm in VII. Prostomium with slight inner protuberances, inner epithelium almost smooth; pharyngeal glands in III, IV, V and VI, distinct masses attached to anterior faces of respective septa; small in III (diameter c. 10 μm), large and of equal size in IV– VI (diameter 30–40 μm), shape roughly triangular, with one corner directing forwards. Nephridia not seen. Coelomocytes spherical, diameter 5–6 μm, nucleated, faintly vesicular. Stomach present in anterior half of VIII, onion-shaped, beginning with abrupt enlargement directly behind 7/8, epithelium with stomachal canals, stomachal lumen with elongate cilia directed backward. Behind stomach intestine narrowed, convoluted, widened abruptly again in 1/2 IX into intestine proper. Midgut pars tumida circumferal in XI. Remarks. Our specimen agrees with the original desciption of P. osborni in body size, chaetal pattern and presence of a stomach in VIII, but it differs in needle length (50 μm in P. osborni). It also agrees closely with the detailed original description of P. minuta (Stephenson, 1914). The latter is a junior synonym of P. osborni since Brinkhurst (1971); see also Righi & Hamoui (2002), Timm (2009), and Van Haaren & Soors (2013). The original description of the intestinal tract, usually neglected in species description or redescriptions of Pristina, is a neat match to the structures as found in our specimen: "The septal [=pharyngeal] glands are rather variable; they are apparently always present in segments iv and v, with the addition usually of a smaller pair in segment iii, or in segment vi, or (in one specimen) in both iii and vi [the condition seen in our specimen]. The stomach is in viii, of a pyriform shape with the broad end directed forwards; it has a somewhat streaked appearance, due apparently to the chloragogen granules being arranged more or less in rows. The alimentary tube is still narrow for some distance behind the stomach, and in contracted specimens forms here a small loop directed backwards; this is not quite straightened out even when the animal extends itself. The intestine begins in segment ix" (Stephenson 1914: 328). P. osborni is a cosmopolitan species; there is one Central American record from montane rainforest moss in Costa Rica at 2900 m asl (Harman 1982), and one record from bromeliads in French Guiana (Céréghino et al. 2011). "This limnetic species is also known from soil in Brazil" (Righi & Hamoui 2002); see this paper for further records in South America. Not all synonymies may be correct. For example, Righi's Amazonian P. minuta (Righi 1973b), synonymized with P. osborni in Righi & Hamoui (2002), has a stomach in VI and is therefore probably a different species. P. osborni should be considered as an aggregate of several species. Large variation is allowed in chaetal length, stomach location and segmental position of the budding zone (Timm 2009). It has been shown in other species of Pristina that specimens with almost identical chaetal pattern may turn out to belong to different species, once the reproductive organs are known (Erséus & Grimm 1998; Collado & Schmelz 2002). Therefore Collado & Schmelz (2002) questioned identifications and synonymizations in P. osborni based on chaetal characters alone. Since reproductive organs are rarely seen in Pristina, a genus that reproduces mainly by paratomy, other internal structures such as the intestinal tract may help to clarify taxonomic questions in this group. Sexual organs of P. osborni have been described by Erséus and Grimm (1998) but the single specimen from a freshwater creek in Northern Australia has no sudden stomachal dilatation, which makes the identification questionable.

Pristina sp. 1 Material examined. One juvenile specimen, not contracted, unstained whole mount, IG 327183-34 [15.506299 -88.23704], 1457 m asl, M. Jocque 07/07/2013. Description. Length 1.5 mm, diameter c. 0.1 mm, 20 segments. Dorsal and ventral chaetae from II, dorsally 1 hair and 1 needle per bundle, ventrally 4 bifids per bundle in II–XII, from XIII 3 per bundle. Hairs smooth, max. length 160 μm (many with distal part broken off); needles simple-pointed, 25–30 μm long. Ventrals with teeth equally long anteriorly (c. 1 μm); posteriorly lower tooth slightly longer than upper tooth; length of ventrals 26 μm in II, 28 μm in VII, posteriorly ca. 30 μm; anteriorly 4 or 5 per bundle, posteriorly mostly 3, in last 2 segments 2. Prostomium 40 μm long, 60 μm high at base, without inner protuberances, i.e. inner epithelial surface smooth. Pharyngeal glands at 4/5, 5/6, first nephridium in VIII. Gut widening gradually in VIII. Coelomocytes not seen. Body wall incrusted with numerous conspicuous bodies, probably monocystid parasites, with smooth, wavy, surface, as if with multiple cuticle, oval, slightly longer than wide (length 12–14 μm, diameter 8–10 μm), with irregular non-vesicular rugged texture. Remarks. This specimen is similar to P. terrena but differs in fewer and smaller ventral chaetae and in smooth hairs.


SCHMELZ

TABLE 1. Megadrile and microdrile Oligochaeta described or recorded from Central and South American bromeliad pools. Valid names of earthworm species follow Csuzdi (2012). Graffiona is a replacement name for Graffia (Csuzdi 2014). Acanthodrilidae, Benhamiinae Dichogaster (Diplothecodrilus) annae (Horst, 1893) (Ref.: Csuzdi & Pavlicek 2009) Dichogaster (Diplothecodrilus) bolaui (Michaelsen, 1891) (Ref.: James & Brown 2006) Dichogaster (Diplothecodrilus) tristani Cognetti, 1907 (Ref.: Michaelsen 1912; Picado 1913, as D. pitahayana Michaelsen) Eutrigaster (Eutrigaster) athena (James, 1996) Eutrigaster (Eutrigaster) bromeliocola (James, 2004) Eutrigaster (Graffiona) arborea (James, 1996) Eutrigaster (Graffiona) azul Sherlock & Csuzdi, 2011 Eutrigaster (Graffiona) basseterrensis (James, 1996) Eutrigaster (Graffiona) caesiticifusca (James, 1996) Eutrigaster (Graffiona) callaina (James, 1996) Eutrigaster (Graffiona) georgei Sherlock & Csuzdi, 2013 Eutrigaster (Graffiona) girija (James, 1996) Eutrigaster (Graffiona) johnsoni (James, 2004) Eutrigaster (Graffiona) picadoi (Michaelsen, 1912) (Ref.: Picado 1913) Eutrigaster (Graffiona) sporadonephra (Cognetti, 1905) (Ref.: Picado 1913, Fragoso & Rojas-Fernández 1996) Acanthodrilidae, Acanthodrilinae Kaxdrilus sherbutti Sherlock & Csuzdi, 2013 Megascolecidae Amynthas rodericensis (Grube, 1879) (Ref.: Csuzdi & Pavlicek 2009) Glossoscolecidae Andiodrilus biolleyi Cognetti, 1904 (Ref.: Picado 1913) Andiodrilus cabalensis Righi, 1995 (Ref.: Feijoo & Celis 2012) Andiodrilus orosiensis Michaelsen, 1912 (Ref.: Picado 1913) Andiorrhinus planaria Michaelsen, 1934 (Ref.: Adis & Righi 1989; James & Brown 2006) Andiorrhinus tarumanis Righi et al., 1976 (Ref.: Adis & Righi 1989; James & Brown 2006) Fimoscolex ohausi Michaelsen, 1900 (Ref.: James & Brown 2006) Ocnerodrilidae Kerriona limae Righi, 1980 (Ref.: James & Brown 2006) Kerriona luederwaldti Michaelsen, 1926 (Ref.: James & Brown 2006) Enchytraeidae Bryodrilus hondurensis sp. nov. Hemienchytraeus phytotelmatus sp. nov. Naididae Aulophorus superterrenus Michaelsen, 1912 (Ref.: Picado 1913, Marcus 1943, Righi 1984, Christoffersen 2007) Pristina acuminata Liang, 1958 (Ref.: Harman et al. 1988) Pristina jenkinae (Stephenson, 1914) (Ref.: Marcus 1943, as Naidium roseum Piguet) Pristina menoni (Aiyer, 1930) (Ref.: Céréghino et al. 2011) Pristina notopora Černosvitov, 1937) (Ref.: Céréghino et al. 2011) Pristina osborni (Walton, 1906) (Ref.: Céréghino et al. 2011) Pristina terrena Collado & Schmelz, 2000

Discussion Eight microdrile oligochaete species were found in the phytotelmata of Honduras, four Pristina species and four Enchytraeidae species belonging to three genera. Six species have valid names, two remain unidentified. Two enchytraeid species are new to science. These are the first species records of Enchytraeidae from phytotelmata worldwide, if the questionable record of F. striata in Picado (1913) is disregarded (Schmelz 2003). The finds represented here are preliminary and do not allow a complete overview of the diversity of microdrile oligochaetes in phytotelmata of the study site: There was a sampling bias—at the first campaign, only large specimens were picked out—the surrounding soil or tree fauna was not sampled, and the fixation procedure of specimens was not optimal. However, with some caution several conclusions can be drawn. The sexually mature specimens of enchytraeids and the presence of ingested debris and humus in the intestine of most specimens suggest that the collected animals live and reproduce in the bromeliad pools, rather than being



521

accidental finds of epiphytic or terrestrial oligochaetes living in the surrounding litter, moss or bark of the trees, and trapped in the phytotelms. A truly terrestrial enchytraeid, once submerged in water, empties the gut within one or two days and does not ingest new material (Schmelz & Collado 2010). The preserved and whole-mounted Honduras specimens have humus and plant debris often in the anterior regions of the gut (from segment XIV on), which means that the material has been ingested only a short time (less than an hour) before fixation (Schmelz, unpublished observations). Furthermore, species of Pristina and Cernosvitoviella are considered to be aquatic oligochaetes, and two species (P. jenkinae, P. osborni) have been found in bromeliad pools previously, P. jenkinae together with the specialist Aulophorus superterrenus (Marcus 1943). It might however be that these species live in a thin water film covering the vegetation. A large number of aquatic microcrustaceans in the same location are found thriving in a thin water film on the leaf litter and on vegetation and are occasionally washed in bromeliads (Jocque et al. 2013). Although nothing at all is known about enchytraeids in Honduras, extrapolations from other tropical sites suggest that the permanently moist litter and organic soil of these montane cloud forest harbours a species-rich and abundant community of enchytraeids, with Hemienchytraeus as one of the dominant genera (Schmelz et al. 2013). The affinity of oligochaetes to bromeliad pools differs greatly among species, and the same species may behave differently in different habitats. At one end of the scale are species that are only sporadically found in the pools and whose natural habitat is elsewhere, litter, soil, decaying wood, freshwater sediment, or soils; an example for the latter is Dichogaster bolaui (Michaelsen, 1891) (James & Brown 2006). At the other end of the scale are the true specialists that are mainly found in the pools and which may show adaptations for dispersal among bromeliads. Up to now the only bromeliad specialist among microdrile oligochaetes is the naidid Aulophorus superterrenus Michaelsen, 1912 (=Dero superterrena), found frequently, almost exclusively and often in high abundance in epiphytic and terrestrial bromeliads in Central and South America (Picado 1913; Marcus 1943; Righi 1984; Christoffersen 2007). Only one record so far is outside this peculiar habitat (Di Persia 1980: fluvial littoral, Argentina). These worms have the special adaptation of actively using frogs as dispersal agents by attaching to their moist skin (Lopez et al. 1999, 2005). Marcus (1943) gives a detailed account of the species' anatomy and reproduction. Among earthworms, many species of Eutrigaster are described as specialists from bromeliad pools, however these species are often found in litter or soil as well. Interestingly, the degree of affinity of Eutrigaster species to phytotelms is dependant on the geographical region and the habitat: In tropical forests of Central America these species are predominantly found in bromeliad pools, but in pine-oak forests of Costa Rica > 1000 m asl, most of the species are found in the litter (Fragoso et al. 1995). Fragoso and Rojas-Fernández (1996) present a series of interesting ecological, historical and phylogenetic hypotheses to explain this peculiar distribution pattern. Some of the microdile oligochaetes found in the Honduras bromeliad pools seem to have a large geographic distribution. Among the three species of Pristina identified here, two (P. jenkinae, P. osborni) are cosmopolitan. P. jenkinae has been recorded from terrestrial habitats in moist forest soils of the Brazilian Amazon (Collado & Schmelz 2000, 2001; Augustsson 2001) and the Mata Atlântica (Römbke et al. 2005), where it can be abundant. It seems to be a common inhabitant of moist tropical and subtropical forest soils. The same may apply to P. terrena, originally described from tropical forest soil.

Acknowledgments Thanks to Samuel James and Csaba Csuzdi for help with literature on earthworms described or recorded from bromeliad pools. Tarmo Timm and one anonymous referee made useful suggestions to improve the manuscript. Barbara Richardson kindly forwarded the letter of the late Brenda Healy with details on enchytraeid identification. Thanks also to Willem Stock for assistance with sampling in the field.

References Adis, J. & Righi, G. (1989) Mass migration and life cycle adaptation - a survival strategy of terrestrial earthworms in Central Amazonian inundation forests. Amazoniana, 11, 23–30. Adlassnig, W., Peroutka, M. & Lendi, T. (2011) Traps of carnivorous pitcher plants as a habitat: composition of the fluid,


SCHMELZ

biodiversity and mutualistic activities. Annals of Botany, 107, 181–194. http://dx.doi.org/10.1093/aob/mcq238 Augustsson, A. (2001) On enchytraeids and naidids: Life-history traits and responses to environmental stress. Doctoral thesis, Department of Animal Ecology, Lund University, Lund, 135 pp. [Sweden, ISBN 97-7105-151-1] Bell, A.W. (1954) Some enchytraeid worms (Oligochaeta) from East Africa. Transactions of the American Microscopical Society, 73, 279–311. http://dx.doi.org/10.2307/3224072 Bell, A.W. (1962) Enchytraeids (Oligochaeta) from various parts of the world. Transactions of the American Microscopical Society, 81, 158–178. http://dx.doi.org/10.2307/3223675 Botea, F. (1983) Oligochètes souterraines de Cuba. Résultats des expéditions biospéologiques cubano-roumaines à Cuba, 4, 19–38. Bretscher, K. (1903) Beobachtungen über die Oligochaeten der Schweiz, VII. Folge. Revue Suisse de Zoologie, 11, 1–21. Brinkhurst, R.O. (1971) Naididae. In: Brinkhurst, R.O. & Jamieson, B.G. (Eds.), Aquatic Oligochaeta of the World. Oliver & Boyd, Edinburg, pp. 304–443. Brinkhurst, R.O. (1985) The generic and subfamilial classification of the Naididae (Annelida: Oligochaeta). Proceedings of the Biological Society of Washington, 98, 470–475. Carrias, J.F., Cussac, M.E. & Corbara, B. (2001) A preliminary study of freshwater protozoa in tank bromeliads. Journal of Tropical Ecology, 17, 611–617. http://dx.doi.org/10.1017/S0266467401001456 Cech, G., Boros, G. & Dózsa-Farkas, K. (2012) Revision of Bryodrilus glandulosus (Dózsa-Farkas, 1990) and Mesenchytraeus kuehnelti Dózsa-Farkas, 1991 (Oligochaeta: Enchytraeidae) using morphological and molecular data. Zoologischer Anzeiger, 251, 253–262. http://dx.doi.org/10.1016/j.jcz.2011.09.005 Céréghino, R., Leroy, C., Carrias, J.-F., Pelozuelo, L., Segura, C., Bosc, C., Dejean, A., Corbara, B. (2011) Ant-plant mutualisms promote functional diversity in phytotelm communities. Functional Ecology, 25, 954–963. http://dx.doi.org/10.1111/j.1365-2435.2011.01863.x Černosvitov, L. (1928) Die Oligochaetenfauna der Karpathen. Zoologische Jahrbücher. Abteilung für Systematik, Geographie und Biologie der Tiere. Jena, 55, 1–28. Černosvitov, L. (1934) Zur Kenntnis der Enchytraeiden. II. Zoologischer Anzeiger, 105, 295–305. Černosvitov, L. (1938) Mission scientifique de l'Omo. Oligochaeta. Mémoires du Muséum National d'Histoire Naturelle, 4, 255–318. Chalupský, J. (1992) Terrestrial Enchytraeidae (Oligochaeta) and Parergodrilidae (Polychaeta) from Sweden, with description of a new enchytraeid species. Zoologica Scripta, 21, 133–150. http://dx.doi.org/10.1111/j.1463-6409.1992.tb00316.x Chen, J. & Xie, Z.C. (2006) Bryodrilus fuscistriatus, a new enchytraeid species (Oligochaeta: Enchytraeidae) from northeastern China. Proceedings of the Biological Society of Washington, 119, 195–201. http://dx.doi.org/10.2988/0006-324X(2006)119[195:BFANES]2.0.CO;2 Christensen, B. & Dózsa-Farkas, K. (1999) The enchytraeid fauna of the Palearctic tundra (Oligochaeta, Enchytraeidae). The Royal Danish Academy of Sciences and Letters, Biologiske Skrifter, 52, 1–37. Christoffersen, M.L. (2007) A catalogue of aquatic microdrile oligochaetes (Annelida: Clitellata) from South America. Acta Hydrobiologica Sinica, 31 (Supplement), 59–86. Cognetti de Martiis, L. (1927) Lumbricidi dei Carpazi. Bollettino dei Musei di Zoologia e Anatomia comparata della Reale Università di Genova, 7, 1–8. Collado, R. & Schmelz, R.M. (2000) Pristina silvicola and Pristina terrena spp. nov., two new soil-dwelling species of Naididae (Oligochaeta, Annelida) from the tropical rain forest near Manaus, Brazil, with comments on the genus Pristinella. The Journal of Zoology, London, 251, 509–516. http://dx.doi.org/10.1111/j.1469-7998.2000.tb00806.x Collado, R. & Schmelz, R.M. (2001) Descriptions of three Pristina species (Naididae, Clitellata) from Amazonian forest soils, including P. marcusi sp. nov. Hydrobiologia, 463, 1–11. http://dx.doi.org/10.1023/A:1013103100981 Collado, R. & Schmelz, R.M. (2002) Pristina trifida sp. nov., a new soil-dwelling microannelid (Oligochaeta: Naididae) from Amazonian forest soils, with comments on species recognition in the genus. Zootaxa, 118, 1–14. Csuzdi, C. (2012) Earthworm species, a searchable database. Opuscula Zoologica, Budapest, 43, 97–99. Csuzdi, C. (2014) Replacement names for Eutrigaster (Graffia) Csuzdi & Zicsi, 1991 and Dichogaster (Malawia) Csuzdi, 2010 (Oligochaeta, Acanthodrilidae). Zootaxa, 3811, 149–150. http://dx.doi.org/10.11646/zootaxa.3811.1.11 Csuzdi, C. & Pavlicek, T. (2009) New records of earthworms from Guadeloupe with description of a new species (Oligochaeta: Glossoscolecidae, Acanthodrilidae, Megascolecidae and Eudrilidae). Opuscula Zoologica Budapest, 40, 9–15. Di Persia, D.H. (1980) The aquatic Oligochaeta of Argentina: current status of knowledge. In: Brinkhurst, R.O. & Cook, D.G. (Eds.), Aquatic Oligochaete Biology. Plenum Press, New York, pp. 79–113.



523

Dózsa-Farkas, K. (1989) Neue Enchytraeiden-Arten (Oligochaeta) aus Ekuador. Acta Zoologica Hungarica, 35, 191–203. Dózsa-Farkas, K., Porco, D. & Boros, G. (2012) Are Bryodrilus parvus Nurminen, 1970 and Bryodrilus librus (Nielsen and Christensen, 1959) (Annelida: Enchytraeidae) really different species? A revision based on DNA barcodes and morphological data. Zootaxa, 3276, 38–50. Ehrenberg, G.C. (1828) Symbolae physicae seu icones et descriptiones animalium evertebratorum. Animalia evertebrata. Phytozoa. Berlin, 293 pp. Erséus, C. & Grimm, R. (1998) Pristina proboscidea and Pristinella osborni (Oligochaeta, Naididae) from a freshwater creek near Darwin, Northern Territory, Australia, with descriptions of the genital organs of both species. The Beagle, records of the museums and art galleries of the Northern Territory, 14, 149–158. Feijoo, M.A. & Celis, L.V. (2012) New species of earthworms (Oligochaeta: Glossoscolecidae) in the Amazon region of Colombia. Zootaxa, 103–119. Fragoso, C. & Rojas-Fernández, P. (1996) Earthworms inhabiting bromeliads in Mexican tropical rainforests: ecological and historical determinants. Journal of Tropical Ecology, 12, 729–734. http://dx.doi.org/10.1017/S0266467400009925 Fragoso, C., James, S.W. & Borges, S. (1995) Native earthworms of the north Neotropical region: current status and controversies. In: Hendrix, P.F. (Ed.), Earthworm ecology and biogeography in North America. Lewis, CRC Press, Boca Raton, FL, pp. 67–115. Frank, H. & Lounibos, L.P. (Eds.) (1983) Phytotelmata: Terrestrial hosts for aquatic insect communities. Plexus Publishing, Medford, NJ, 293 pp. Frank, J.H., Sreenivasan, S., Benshoff, P.J., Deyrup, M.A., Edwards, G.B., Halbert, S.E., Hamon, A.B., Lowman, M.D., Mockford, E.L., Scheffrahn, R.H., Steck, G.J., Thomas, M.C., Walker, T.J. & Welbourn, W.C. (2004) Invertebrate animals extracted from native Tillandsia (Bromeliales : Bromeliaceae) in Sarasota County, Florida. Florida entomologist, 87, 176– 185. http://dx.doi.org/10.1653/0015-4040(2004)087[0176:IAEFNT]2.0.CO;2 Harman, W.J. (1982) The aquatic Oligochaeta (Aeolosomatidea, Opistocystidae, Naididae) of Central America. The Southwestern Naturalist, 27, 287–298. http://dx.doi.org/10.2307/3670877 Harman, W.J., Brinkhurst, R.O. & Marchese, M. (1988) A contribution to the taxonomy of the aquatic Oligochaeta (Naididae) of South America. Canadian Journal of Zoology, 66, 2233–2242. http://dx.doi.org/10.1139/z88-331 Healy, B. (1996) Records of Enchytraeidae (Annelida: Oligochaeta) from west Florida, 1. Mesenchytraeus, Cognettia, Bryodrilus, Hemienchytraeus, Henlea and Buchholzia. Proceedings of the Biological Society of Washington, 109, 118– 137. James, S.W. (1996) Nine new species of Dichogaster (Oligochaeta, Megascolecidae) from Guadeloupe (French West Indies). Zoologica Scripta, 25, 21–34. http://dx.doi.org/10.1111/j.1463-6409.1996.tb00149.x James, S.W. (2004) Earthworms (Clitellata, Acanthodrilidae) of the mountains of Eastern Jamaica. Organisms, Diversity & Evolution, 4, 277–294. http://dx.doi.org/10.1016/j.ode.2004.04.003 James, S.W. & Brown, G.G. (2006) Earthworm ecology and diversity in Brazil. In: Moreira, F.M.S., Siqueira, J.O. & Brussaard, L. (Eds.), Soil biodiversity in Amazonian and other Brazilian ecosystems. CABI Publishing, Cambridge, MA, pp. 56–116. http://dx.doi.org/10.1079/9781845930325.0056 Jocque, M., Kernaham, A., Nobes, A., Williams, C. & Field, R. (2010) How effective are non-destructive sampling methods to assess aquatic invertebrate diversity in bromeliads? Hydrobiologia, 649, 293–300. Jocque, M., Fiers, F., Romero, M. & Martens, K. (2013) Crustacea in phytotelmata: a global overview. Journal of Crustacean Biology, 33, 451–460. http://dx.doi.org/10.1163/1937240X-00002161 Kathman, R.D. (1985) Synonymy of Pristinella jenkinae (Oligochaeta: Naididae). Proceedings of the Biological Society of Washington, 98, 1022–1027. Laessle, A.M. (1961) A micro-limnological study of Jamaican bromeliads. Ecology, 42, 499–517. http://dx.doi.org/10.2307/1932236 Lastočkin, D.A. (1924) New and rare Copepoda and Oligochaeta form Central Russia. Bulletin de l'Institut d'Hydrobiologie de Russe, Leningrad, 9, 5–6. Lopez, L.C.S., Filizola, B., Deiss, I. & Rios, R.I. (2005) Phoretic behaviour of bromeliad annelids (Dero) and ostracods using frogs and lizards as dispersal vectors. Hydrobiologia, 549, 15–22. http://dx.doi.org/10.1007/s10750-005-1701-4 Lopez, L.C.S., Rodrigues, P.J.F.P. & Rios, R.I. (1999) Frogs and snakes as phoretic dispersal agents of bromeliad ostracods (Limnocytheridae: Elpidium) and annelids (Naididae: Dero). Biotropica, 31, 705–708. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00421.x Marcus, E. (1943) Sôbre Naididae do Brasil. Boletins da Faculdade de Filosofia, Ciências e Letras da Universidade de São Paulo, 7, 3–247.


SCHMELZ

Michaelsen, W. (1912) Über einige zentralamerikanische Oligochäten. Archiv für Naturgeschichte, 78A, 112–129. Nielsen, C.O. & Christensen, B. (1959) The Enchytraeidae. Critical revision and taxonomy of European species (Studies on Enchytraeidae VII). Natura Jutlandica, 8–9, 1–160. Nurminen, M. (1970) Records of Enchytraeidae (Oligochaeta) from the west coast of Greenland. Annales Zoologici Fennici, 7, 199–209. Ospina-Bautista, F., Estévez-Varón, J.V., Betancur, J. & Realpe-Rebolledo, E. (2004) Estructura y composición de la comunidad de macro invertebrados acuáticos asociados a Tillandsia turneri Baker (Bromeliaceae) en un bosque alto andino colombiano. Acta Zoologica Mexicana nueva serie, 20, 153–166. Paoletti, M.G., Taylor, R.A.J., Stinner, B.R., Stinner, D.H. & Benzing, D.H. (1991) Diversity of soil fauna in the canopy and forest floor of a Venezuelan cloud forest. Journal of Tropical Ecology, 7, 373–383. http://dx.doi.org/10.1017/S0266467400005654 Picado, C. (1913) Les broméliacées épiphytes considerées comme milieu biologique. Bulletin Scientifique de la France et de la Belgique, 47, 215–360. Piguet, E. (1906) Observations sur les Naididées et revision systématique de quelques espèces de cette famille. Imprimerie W. Kündig & Fils, Genève, 316 pp. + pls. IX–XI. Piper, S.R., MacLean, S.F. & Christensen, B. (1982) Enchytraeidae (Oligochaeta) from taiga and tundra habitats of northeastern U.S.S.R. Canadian Journal of Zoology, 60, 2594–2609. http://dx.doi.org/10.1139/z82-334 Richardson, B. (1999) The bromeliad microcosm and the assessment of faunal diversity in a neotropical forest. Biotropica, 31, 321–336. http://dx.doi.org/10.1111/j.1744-7429.1999.tb00144.x Richardson, B., Rogers, C. & Richardson, M.J. (2000) Nutrients, diversity, and community structure of two phytotelm systems in a lower montane forest, Puerto Rico. Ecological Entomology, 25, 348–356. http://dx.doi.org/10.1046/j.1365-2311.2000.00255.x Richardson, B.A., Borges, S. & Richardson, M.J. (2006) Differences between epigeic earthworm populations in tank bromeliads from Puerto Rico. Caribbean Journal of Science, 42, 380–385. Righi, G. (1973a) Sobre trés espécies Brasileiras de Enchytraeidae (Oligochaeta). Boletim de Zoologia e Biologia Marina, São Paulo, 30, 469–482. Righi, G. (1973b) On Pristina minuta (Oligochaeta, Naididae) from Brazilian Soil and its epizoic Rhabdostyla pristinis, sp. n. (Ciliata, Epistylidae). Zoologischer Anzeiger, 191, 295–299. Righi, G. (1984) Oligochaeta. In: Schaden, R. (Ed.), Manual de Identificação de Invertebrados Límnicos do Brasil, 17, pp. 1– 48. [CNPq, Conselho Nacional de Desenvolvimiento Científico e Tecnológico, Brasilia] Righi, G. (1988) Dois novos Microdrili, Oligochaeta, terrestres da Amazônia. Papéis Avulsos de Zoologia. Museu de Zoologia da Universidade de São Paulo, 36, 315–321. Righi, G. (1995) Colombian earthworms. In: Van der Hammen, T. & Dos Santos, A.G. (Eds.), Studies on Tropical Andean Ecosystems / Estudios de Ecosistemas Tropandinos. Vol. 4. Cramer, Berlin, pp. 485–607. Righi, G., Ayres, I. & Bittencourt, E. (1976) Glossoscolecidae (Oligochaeta) do Instituto Nacional de Pesquisas da Amazônia. Acta Amazonica, 6, 335–367. Righi, G. & Hamoui, V. (2002) Oligochaeta, Naididae of the West Indies and adjacent regions. Papéis Avulsos de Zoologia. Museu de Zoologia da Universidade de São Paulo, 42, 119–167. Römbke, J., Collado, R. & Schmelz, R.M. (2005) Oligochaetes (Clitellata) of the Mata Atlântica (Parana, Brazil): first results of the SOLOBIOMA project. Proceedings of the Estonian Academy of Sciences: Biology, Ecology, 54, 302–309. Rota, E. (2013) How many lookalikes has Marionina argentea (Michaelsen, 1889) (Annelida: Clitellata: Enchytraeidae)? Three new species described from morphological evidence. Zoologischer Anzeiger, 252, 123–137. http://dx.doi.org/10.1016/j.jcz.2012.05.001 Rota, E. & Healy, B. (1999) A taxonomic study of some Swedish Enchytraeidae (Oligochaeta), with descriptions of four new species and notes on the genus Fridericia. Journal of Natural History, 33, 29–64. http://dx.doi.org/10.1080/002229399300461 Schenkova, J. & Čermak, V. (2013) Description of Pristina armata n. sp (Clitellata: Naididae: Pristininae) from a carnivorous plant (Nepenthes sp.) in Borneo, Indonesia. Zootaxa, 3686 (5), 587–592. http://dx.doi.org/10.11646/zootaxa.3686.5.7 Schmelz, R.M. (2003) Taxonomy of Fridericia (Oligochaeta, Enchytraeidae). Revision of species with morphological and biochemical methods. Abhandlungen des Naturwissenschaftlichen Vereins in Hamburg (Neue Folge), 38, 1–415, figs. 1– 73. Schmelz, R.M. & Collado, R. (2012) An updated checklist of currently accepted species of Enchytraeidae (Oligochaeta). vTI Agriculture and Forestry Research, Special Issue, 357, 67–87. Schmelz, R.M. & Collado, R. (2007) Revision of Hemienchytraeus stephensoni (Cognetti, 1927) (Enchytraeidae, Oligochaeta, Annelida). Folia Facultatis scientiarum naturalium Universitatis Masarykianae Brunensis, Biologia, 110, 67–85. Schmelz, R.M. & Collado, R. (2010) A guide to European terrestrial and freshwater species of Enchytraeidae (Oligochaeta). Soil Organisms, 82, 1–176. Schmelz, R.M., Niva, C.C., Römbke, J. & Collado, R. (2013) Diversity of terrestrial Enchytraeidae (Oligochaeta) in Latin



525

America: Current knowledge and future research potential. Applied Soil Ecology, 69, 13–20. http://dx.doi.org/10.1016/j.apsoil.2012.12.012 Schmelz, R.M. & Römbke, J. (2005) Three new species of Hemienchytraeus (Enchytraeidae, Oligochaeta) from Amazonian forest soil. Journal of Natural History, 39, 2967–2986. http://dx.doi.org/10.1080/00222930500218664 Sherlock, E. & Csuzdi, C. (2013) Two new earthworm species from Belize (Oligochaeta: Acanthodrilidae). Journal of Natural History, 47, 1911–1919. http://dx.doi.org/10.1080/00222933.2013.770931 Sherlock, E., Lee, S., McPhee, S., Steer, M., Maes, J.M. & Csuzdi, C. (2011) The first earthworm collections from Nicaragua with description of two new species (Oligochaeta). Zootaxa, 2732, 49–58. Sperber, C. (1948) A taxonomic study of the Naididae. Zoologiska Bidrag från Uppsala, 28, 1–296. Srivastava, D.S., Kolasa, J., Bengtsson, J., Gonzalez, A., Lawler, S.P., Miller, T.E., Munguia, P., Romanuk, T., Schneider, D.C. & Trzcinski, M.K. (2004) Are natural microcosms useful model systems for ecology? Trends in Ecology & Evolution, 19, 379–384. Standen, V. (1988) Oligochaetes in fire climax grassland and conifer plantations in Papua New Guinea. Journal of Tropical Ecology, 5, 39–48. http://dx.doi.org/10.1017/S0266467400002480 Stephenson, J. (1914) On a collection of Oligochaeta mainly from Northern India. Records of the Indian Museum of Calcutta, 10, 321–366. Stephenson, J. (1924) Oligochaeta of the Siju Cave, Garo Hills, Assam. Records of the Indian Museum of Calcutta, 26, 127– 137. Stephenson, J. (1931) Oligochaeta from Burma, Kenya and other parts of the world. Proceedings of the Zoological Society of London, 1931, 33–92. Stout, J.D. (1956) Aquatic Oligochaetes occurring in forest litter. - I. Transactions of the Royal Society of New Zealand, 84, 97– 102. Stout, J.D. (1958) Aquatic Oligochaetes occurring in forest litter. - II. Transactions of the Royal Society of New Zealand, 85, 289–299. Timm, T. (2009) A guide to the freshwater Oligochaeta and Polychaeta of Northern and Central Europe. Lauterbornia, 66, 1– 235. Ude, H. (1892) Ein neues Enchytraeiden-Genus. Zoologischer Anzeiger, 401, 344–345. Van Haaren, T. & Soors, J. (2013) Aquatic oligochaetes of The Netherlands and Belgium. KNNV Publishing, Zeist, 302 pp. [The Netherlands] Varga, L. (1928) Ein interessanter Biotop der Biocönose von Wasserorganismen. Biologisches Zentralblatt, 48, 143–162. Vejdovský, F. (1879) Beiträge zur vergleichenden Morphologie der Anneliden. I. Monographie der Enchytraeiden. Verlag von Friedrich Tempsky, Prag, 61 pp. + 14 pls. Walton, L.B. (1906) Naididae of Cedar Point, Ohio. The American Naturalist, 40, 683–706. http://dx.doi.org/10.1086/278670 Xie, Z.C., Liang, Y.L. & Wang, H.Z. (2000) A taxonomic study of Bryodrilus (Enchytraeidae, Oligochaeta) from Changbaishan Mountain, China. Species Diversity, 5, 93–101.


SCHMELZ

A Tank Bromeliad Favors Spider Presence in a Neotropical Inundated Forest.

Belowground responses to elevation in a changing cloud forest.

Phylogeography of Liquidambar styraciflua (Altingiaceae) in Mesoamerica: survivors of a Neogene widespread temperate forest (or cloud forest) in North America?

Biology and ecology of Alchisme grossa in a cloud forest of the Bolivian Yungas.

Water relations and microclimate around the upper limit of a cloud forest in Maui, Hawai'i.

Distribution and elevated soil pools of mercury in an acidic subtropical forest of southwestern China.

Variation of biomass and carbon pools with forest type in temperate forests of Kashmir Himalaya, India.

The surrounding landscape influences the diversity of leaf-litter ants in riparian cloud forest remnants.

Bromeliad treefrogs as phoretic hosts of ostracods.

Post-fragmentation population structure in a cooperative breeding Afrotropical cloud forest bird: emergence of a source-sink population network.

Constipation and weight loss in a Honduran immigrant.

Bromeliad selection by two salamander species in a harsh environment.

Epiphyte response to drought and experimental warming in an Andean cloud forest.

Leaf spectra and weight of species in canopy, subcanopy, and understory layers in a venezuelan andean cloud forest.

Mapping the montane cloud forest of Taiwan using 12 year MODIS-derived ground fog frequency data.

Physiological Responses of Two Epiphytic Bryophytes to Nitrogen, Phosphorus and Sulfur Addition in a Subtropical Montane Cloud Forest.

Environmental controls in the water use patterns of a tropical cloud forest tree species, Drimys brasiliensis (Winteraceae).

The hydroclimatic and ecophysiological basis of cloud forest distributions under current and projected climates.

Vascular Epiphyte Diversity Differs with Host Crown Zone and Diameter, but Not Orientation in a Tropical Cloud Forest.

Circumstances surrounding deaths from the perspective of bereaved Honduran families.

A Location-Based Interactive Model of Internet of Things and Cloud (IoT-Cloud) for Mobile Cloud Computing Applications.

Interleukin-10 and soil-transmitted helminth infections in Honduran children.

Water relations and gas exchange of fan bryophytes and their adaptations to microhabitats in an Asian subtropical montane cloud forest.

Bat-fruit interactions are more specialized in shaded-coffee plantations than in tropical mountain cloud forest fragments.