Research Article |
Corresponding author: Pilar Rodriguez ( pilar.rodriguez@ehu.es ) Academic editor: Samuel James
© 2014 Pilar Rodriguez, Steven Fend, David Lenat.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Rodriguez P, Fend S, Lenat D (2014) Sylphella puccoon gen. n., sp. n. and two additional new species of aquatic oligochaetes (Lumbriculidae, Clitellata) from poorly-known lotic habitats in North Carolina (USA). ZooKeys 451: 1-32. https://doi.org/10.3897/zookeys.451.7304
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Three new species of Lumbriculidae were collected from floodplain seeps and small streams in southeastern North America. Some of these habitats are naturally acidic. Sylphella puccoon gen. n., sp. n. has prosoporous male ducts in X–XI, and spermathecae in XII–XIII. Muscular, spherical atrial ampullae and acuminate penial sheaths distinguish this monotypic new genus from other lumbriculid genera having similar arrangements of reproductive organs. Cookidrilus pocosinus sp. n. resembles its two subterranean, Palearctic congeners in the arrangement of reproductive organs, but is easily distinguished by the position of the spermathecal pores in front of the chaetae in X–XIII. Stylodrilus coreyi sp. n. differs from congeners having simple-pointed chaetae and elongate atria primarily by the structure of the male duct and the large clusters of prostate cells. Streams and wetlands of Southeastern USA have a remarkably high diversity of endemic lumbriculids, and these poorly-known invertebrates should be considered in conservation efforts.
Lumbriculids, biodiversity, acidic waters, pocosin soils, North America
In contrast to larger streams and rivers, aquatic habitats such as wetlands, small headwater tributaries or springs have received little attention. As these habitats are not directly connected to each other by flow, and their physical structure can vary greatly from one location to another, they may be expected to support a distinct invertebrate fauna, demonstrate greater variation in taxonomic composition, and have patterns of taxa richness and assemblage variation that do not correlate with adjacent main stream habitats. Riverine wetlands studies in North America indicate high macroinvertebrate taxonomic richness, and greater assemblage variation compared to nearby riffle communities (
Biological assessment of swamp streams in the southeastern USA has been particularly difficult, especially in naturally acidic areas, since the unusual conditions result in a distinctive fauna with relatively low diversity and abundance of taxa commonly used to indicate excellent water quality (e.g., Ephemeroptera, Plecoptera, Trichoptera – EPT). The North Carolina Division of Environmental Management has struggled with ratings for swamp streams in North Carolina for many years, and for some regions of the state there is still insufficient information to assign water quality ratings (
The southeastern region of North America has revealed a great degree of endemicity in the oligochaete family Lumbriculidae. Recent collections from the Sandhills and Coastal Plain ecoregions of North Carolina have resulted in the description of new, and probably endemic, lumbriculid species and genera (
Oligochaetes were usually collected by disturbing the substrate and then sweeping through this area with a 300 μm mesh net. Samples were elutriated to remove the heavier sediments. Most collections were live-picked at the sample site, but some material was fixed whole in 10% buffered formalin and brought back to the laboratory for sorting. Field-picked specimens were relaxed by the addition of small amounts of alcohol, and then they were fixed in formalin and/or Bouin’s solution. Formalin-preserved specimens were transferred to 70% alcohol after one day, for long term storage.
Most worms were whole-mounted or longitudinally dissected, stained with Harris’ hematoxylin or borax carmine, dehydrated through an alcohol series, transferred to methyl salicylate and slide mounted in Canada balsam. A few specimens were sagitally sectioned at 7 μm, slide mounted, and stained in hematoxylin and eosin Y.
Drawings of the reproductive system and chaetae were made using a camera lucida. In the descriptions of the male duct and spermatheca, the term ental indicates a position that is inner or deep within the body, as opposed to ectal for an outer or near-surface position. In the descriptions of chaetae, proximal is used to describe a position near the symmetry axis of the body, as opposed to distal. Segment numbers are shown in Roman numerals; intersegments are given as Arabic numerals; e.g., “9/10” to represent the intersegment of IX and X. Holotype and paratype specimens are deposited in the U.S. National Museum of Natural History, Smithsonian Institution (USNM), Washington D.C., USA; California Academy of Sciences (CASIZ), San Francisco, California, USA; and Museo Nacional de Ciencias Naturales (MNCN), Madrid, Spain. Non-type specimens are in the authors’ collections.
a: atrium, aa: atrial ampulla, ad: atrial duct, ae: atrial epithelium, am: atrial muscle layer, b: brain, bv: blood vessel, cc: chloragogen cells, cg: chaetal gland, ch: chaeta, dv: dorsal blood vessel, e: efferent duct of nephridium, ff: female funnel, fp: female pore, g: gut, i: intestine, mp: male pore, o: ovary, oc: oocytes, pg: pharyngeal glands, ph: pharynx, pr: prostate, prj: prostate junction, p: penis, ps: penis cuticular sheath, pt: prostomium, sa: spermathecal ampulla, sd: spermathecal duct, sf: sperm funnel, siv: supraintestinal blood vessel, sp: spermatheca, spp: spermathecal pores, t: testis, vd: vas deferens.
The new species were collected at five North Carolina locations: one site in the central Piedmont region (UT Pokeberry Creek), two sites in the eastern Coastal Plain (Pettiford Creek and Lake Run) and two sites in the Sandhills (Drowning Creek and Anderson Creek). The Sandhills area is located between the Piedmont and Coastal Plain regions, in the southeastern part of North Carolina. The Coastal Plain and Sandhills sites are humic (“brown-water”) systems. Coordinates for sampling sites are given in WGS84.
The unnamed tributary (UT) to Pokeberry Creek was sampled near the town of Pittsboro in Chatham County, N35.8267, W79.1013. This is part of a floodplain complex of seeps and pools that have surface water only during fall, winter and spring months. The clay soils in the Pokeberry Creek catchment produce small streams (seeps) with a limited hyporheic zone and reduced groundwater storage, causing them to go dry during summer months. These shallow seeps are about 0.5 m wide, with a substrate of clay and decomposing leaves. They originate at the base of a steep hill, largely fed by groundwater, and flow for about 200 m into Pokeberry Creek, within a totally forested area. There were no water chemistry samples from the Pokeberry seeps, but samples from nearby streams suggest pH values close to 7.
Pettiford Creek drains a pocosin area (nutrient-poor, forested or shrub wetland) of the Croatan National Forest in Carteret County. The sampling site (N34.7471, W77.0221) was both upstream and downstream of Forest Service Road 128, also known as Millis Road. Pettiford Creek is about 5 m wide in constricted areas (bridges), but has a much wider braided channel elsewhere (>100 m). The substrate is mostly detritus over a fine sand base. This stream has been frequently used as a reference location by the North Carolina Division of Water Quality. Water pH values from this stream were 3.6 in 2004 and 3.4 in 2010, and conductivity was low (50–85 μS/cm) (
Lake Run drains Little Singletary Lake in Bladen County; samples were collected at State Road (SR) 1325, N34.7773, W78.6646. This stream was sampled for benthic macroinvertebrates in 1981, as part of a study of naturally acidic streams (Lenat, unpublished). At that time, the pH was found to be consistently less than 3.8, with a substrate of fine sand and clay overlain by leaves and woody debris. Stream width was 2–4 m, with a maximum depth of 1.2 m. Conductivity was low, with a range of 45–56 μS/cm. Lake Run also supported 11 EPT species usually considered to be intolerant (Lenat, unpublished data from 1981). In addition to the Cookidrilus species described here, the present collection included the lumbriculids A. lenati and M. arenosus.
Drowning Creek was sampled at SR 1004 on the Richmond County/Moore County border, N35.0662, W79.5496. A NCDWQ collection in July 2006 recorded a pH of 5.6, and conductivity was 26 μS/cm in the main channel. This site is about 2.5 km upstream of a reach classified as Outstanding Resource Water (
Anderson Creek is a small tributary to the Lower Little River at SR 2031 in Harnett County, N35.2661, W78.8192. Based on earlier studies, conductivity is low (49 μS /cm) and pH slightly acidic (5.0–5.9); the stream has a sand-gravel substrate and is classified as “Good” based on a moderate EPT species richness (
Simple-pointed chaetae. Two pairs of testes and one pair of ovaries. Ovaries in first segment behind testes. Male pores paired in X and XI, female pores paired in the intersegment 12/13. Male ducts prosoporous. Atrial duct forms a penis within a penial sac, distally covered by a cuticular sheath. Two pairs of spermathecae, beginning in the ovarian segment.
Sylphella puccoon sp. n.
USNM 1251692: a dissected worm, stained in Harris’ hematoxylin, mounted in Canada balsam (collected 23 Jan 2009).
all from the type locality. USNM 1251693-1251698: 7 Jan 2009, 1 whole mount; 23 Jan 2009, 3 dissected; 30 Jan 2009, 2 sectioned (1 sagittal, 1 transverse). MNCN 16.03/3083: 14 Jan 2009, 2 dissected. CASIZ 197898: 23 Jan 2009, 3 dissected.
An unnamed, very small tributary (seep) to Pokeberry Creek, Chatham Co., North Carolina, USA.
The genus name refers to Sylph, the Latin name of an elemental spirit of the air that suggests the Latin silva, for woodland, followed by the Latin diminutive -ella. The specific name puccoon is the Algonquian Indian word which means pokeberry (Phylolacca species).
7 Jan 2009, 2 whole mounts. 14 Jan 2009, 3 dissected and 3 whole mounts; 11 in alcohol. 23 Jan 2009, 9 dissected and 1 whole mount; 3 in alcohol. 30 Jan 2009, 2 sectioned for histological study. All specimens (including the type series) collected by D.R. Lenat from the type locality.
(based on mated specimens). Number of segments 65–83. Length of fixed worms 15–25 mm. Diameter of the body from 14 unmounted worms in lateral aspect (measured to 0.01 mm): 0.44–0.66 mm in VIII (mean 0.51 mm), 0.45–0.68 mm at clitellum (mean 0.54 mm), and 0.50–0.76 mm (mean 0.61 mm) at mid-body.
Prostomium rounded-conical, 270–400 μm long, width about the same as length. Secondary annulation (narrow ring in anterior part of segment) from segment V; present but weak in post-clitellar segments (Fig.
Drawings of Sylphella puccoon gen. n., sp. n. A Anterior part of the body showing secondary annulations, clitellum and position of genital pores B chaetae of segment II and clitellar region C schematic drawing of reproductive organs (female funnel obscured by ovary) D detail of atrium E posterior lateral blood vessels.
Sylphella puccoon gen. n., sp. n. A Anterior part of the worm, showing prostomium B clitellar epidermis C chaeta in XII D egg sac containing oocytes and some blood vessels E dorsal vessel showing the cardiac cells and supra-intestinal vessel, dorsal to the intestine in segment XVII F reproductive segments, showing two atria, with their respective sperm funnels, and spermathecae of an unmated specimen G sperm funnel on the septum behind the atrium H atrial ampulla with sperm in the lumen, showing the several layers of musculature I prostatic cells forming small clusters over the atrial ampulla J cross-hatched muscular fibers shown at the surface of the atrial ampulla K Spermathecal ampulla with loose sperm in the lumen L spermathecal duct M penis within the penial sac, with conical penial sheath. For comparison N penis with tubular cuticular sheath in Styloscolex japonicus, and O penis with a soft cuticular layer in Lumbriculus japonicus. D, E, G–O histological sections of reproductive organs, other photographs from stained whole mounts or dissected specimens.
Length (μm) of chaetae in Sylphella puccoon gen. n., sp. n. (measurements on one whole-mounted specimen from Pokeberry Cr., North Carolina, USA 14 Jan 2009).
Segment | II | III | IV | V | VI | VII | VIII | IX | X | Posterior |
---|---|---|---|---|---|---|---|---|---|---|
Dorsal | 63 | – | 88 | 90 | 103 | 94 | 118 | 120 | 120 | 99–121 |
Ventral | 167 | 141 | 140 | 141 | 162 | 154 | 140 | 141 | 132 | 95–124 |
Ventral/dorsal length | 2.6 | – | 1.6 | 1.6 | 1.6 | 1.6 | 1.2 | 1.2 | 1.1 | 1.0 |
Transverse, oval male pores are in line of ventral chaetae of segment X and XI, about midway between chaetae and posterior septum (Fig.
Pharynx developed mainly dorsally and laterally, in segments II and III. Pharyngeal glands well developed dorsally and ventrally in IV–VI, usually extending ventrally into VII. Chloragogenous tissue well developed from VII backwards. A supra-intestinal vessel may appear differentiated from the perivisceral sinus (Fig.
Two pairs small testes, in segments X and XI; one pair elongate ovaries in XII, extending through XIII. Female funnels large, attached to the septum and opening in intersegment 12/13. Two pairs spermathecae, the first in the post-atrial segment (typically XII), and the second in the post-ovarian segment (typically XIII) (Figs
A single vas deferens per atrium (prosoporous condition), sperm funnels located on the septa of intersegments 10/11 and 11/12 (posterior septa of atrial segments), but folded back into the next segment. Vasa deferentia long (about 700 μm), penetrating the posterior septa, and forming a long, convoluted loop within each post-atrial segment (Fig.
The spermathecae have a narrow duct and an irregular, sacciform ampulla. Spermathecal duct fusiform, (30–45 μm maximum diameter), formed by columnar epithelium, a thin (about 2 μm) muscle layer, and with a wide lumen except at the pore; ental end of the duct prolonged into a narrow neck (12–20 μm diameter) which joins the ampulla (Figs
Two specimens had the entire sequence of reproductive organs in segments VII–X, with the clitellum in VII–XI instead of the usual X–XIV; apparently an anterior shift of three segments. These aberrant worms appeared normal in other respects, except that nephridia were not present in VII and VIII.
The combination of multiple atrial segments, prosopore male ducts in the testicular segments (GI and GII, see
Taxonomic characters of the reproductive system that distinguish Lumbriculus tetraporophorus Popchenko, 1976 from Sylphella puccoon gen. n., sp. n.
Characters | Lumbriculus tetraporophorus | Sylphella puccoon |
---|---|---|
Male porophores | 2 pairs, prominent, conical (210 μm high), formed by concentric muscle ridges | Absent |
Atrial ampulla | Pear-shaped (250×510 μm) | Nearly spherical (140–210 μm Ø) |
Atrial duct | 170 μm long, wider in the middle | Cylindrical (90–110 μm long). Penial sac 120–130 μm |
Atrial musculature | 48–51 μm, in 2 orthogonal layers, circular muscle 34 μm thick | 40–50 μm intercrossing fibers in many indistinct layers |
Penis | 140–170 μm long, with tapered end (probably typical Lumbriculus type of extrudable lining cells in the atrial duct) | 90–110 μm long, tapered end of atrial duct sharply acuminate, ectally covered by cuticle |
Prostatic cells | Diffuse (rykhlym) | In petiolate clusters of cells |
Vas deferens | Prosoporous, 18–20 μm Ø, joining entally, barely penetrating next segment | Prosoporous, (12–16 μm Ø, joining ectally, forming a loop in next segment |
Female pores | ventral | lateral |
The tetrathecate condition, with paired spermathecae in the first two postatrial segments, is a feature shared with some species in the semiprosoporous lumbriculid genera Trichodrilus Claparède, 1862 and Eremidrilus Fend & Rodriguez, 2003. However, the presence of two pairs of prosoporous atria in Sylphella suggests that a close phylogenetic relationship with these genera is improbable.
The general form of the atria bears a slight resemblance to some Palearctic species of the genus Trichodrilus having petiolate atria, spherical and very muscular atrial ampullae, and two pairs of spermathecae (e.g., T. aporophorus Popchenko, 1976b, T. claparedei Hrabě, 1937). Bichaeta sanguinea Bretscher, 1990 also has a spherical and very muscular atrium, but lacks an atrial duct. In contrast, genera resembling Sylphella in the arrangement of reproductive organs (Lamprodrilus, Lamprortus, Wsewolodus and Lumbriculus) tend to have elongate atria.
The atrial musculature in Sylphella consists of many small, cross-hatched layers, similar to some other lumbriculids, such as Trichodrilus longipenis Giani & Rodriguez, 1994. Details of atrial musculature are usually not given in lumbriculid diagnoses, but where described, the atrial muscle fibers show a simpler organization (parallel or two opposing layers) in the related genera. The Sylphella arrangement of atrial muscles should be distinguished from the simple crossed musculature in Lumbriculus species, which consists of only two perpendicular layers; however, it bears some resemblance to the many diagonally arranged layers in some Eclipidrilus Eisen species (
The penis in Sylphella puccoon is similar to that described for Styloscolex japonicus Yamaguchi, 1937 in its basic structure, as well as in the presence of a smooth, rigid cuticular layer (sheath) on the ectal end (Fig.
Lamprortus and most Lamprodrilus species also have a type-1 penis (i.e., an extension of the atrial duct within a fold of the ventral body wall, see
Enlarged ventral chaetae in anterior segments occur to some degree in many lumbriculids, but the difference is well marked in several Trichodrilus species (see
Sylphella puccoon gen. n., sp. n. has only been collected during winter months from a single, small seep that is a tributary of Pokeberry Creek, North Carolina. A large number of similar seeps were investigated by one of the authors (D. Lenat) adjacent to Pokeberry Creek, but Sylphella was limited to a 10-m reach of the largest seep (1 meter wide). The small streams in this area go completely dry during summer months, due a combination of clay soils and seasonal rainfall patterns. The dominant macroinvertebrates in these seeps were the isopod Caecidotea forbesi (William), the amphipod Crangonyx sp. Bate, and chironomids. The mayfly genera Callibaetis Eaton and Leptophlebia Westwood can be abundant, but other EPT taxa were sparse. Other oligochaetes at this site include Rhynchelmis bolinensis Fend & Lenat (the type locality), Eclipidrilus cf. fontanus, Rhyacodrilus propiporus Rodriguez & Fend, and an undescribed lumbriculid of unknown generic attribution.
USNM 1251699: a dissected specimen, stained in Harris’ hematoxylin and mounted in Canada balsam (collected 4 March 2011).
USNM 1251700-1251702: from the type locality, 22 Feb 2011, 1 dissected; 4 Mar 2011, 1 whole-mounted; Pettiford Creek, at Millis Road, Carteret County, North Carolina, USA, 15 Mar 2007, 1 whole mount. MNCN 16.03/3084: from the type locality, 22 February 2011, 1 dissected, stained in Harris’ hematoxylin and mounted in Canada balsam, and 1 histologically sectioned, stained with hematoxylin-eosin. CASIZ 197899: Pettiford Creek, 15 Mar 2007, 1 whole mount.
Lake Run, outlet stream draining Little Singletary Lake at SR 1325, in Bladen County, North Carolina, USA.
The specific name refers to pocosin, “swamp-on-a-hill” in the Algonquin Indian language. Most specimens were collected in two sites draining pocosin areas.
From the type locality, 22 Feb 2011, 4 whole mounts, 1 dissected, 1 sagittally sectioned. Pettiford Creek, at Millis Road, Carteret County, North Carolina, USA, 22 Apr 2008, 1 whole mount; 5 Apr 2010, 2 dissected. Drowning Creek at State Road 1004, Moore County, North Carolina, 12 Jan 2009, 1 whole mount. Anderson Creek at SR 2031, Harnett County, North Carolina, 27 Jun 2011, 1 whole mount. All specimens (including the type series) collected by D.R. Lenat.
Number of segments 53–71. Diameter of the body 279–342 µm in segment VIII and 360–441 µm at the clitellum. Prostomium round, 120–154 µm long. Brain back to intersegment 2/3. Secondary annulation (narrow ring in anterior part of segment) well marked from segment VI to IX, not always visible in the postclitellar region, but evident in the caudal region of the body (Figs
Cookidrilus pocosinus sp. n. A Anterior region of the body B caudal region with pygidium C chaetae D chaetal gland behind ventral bundle of chaetae E clitellum F spermathecal and male pores in front of and behind ventral chaetae of segment X G atrium H atrial ampulla showing apical junction of vasa deferentia I atrial ampulla showing junction of prostatic cell clusters J basal junction of vas deferens to atrial ampulla K detail of atrial duct and protruded penis L third spermatheca behind the female segment. A, D, J, K, L histological sections, other photographs from stained whole mounts or dissected specimens.
Pharynx developed mainly dorsally, in segments II and III. Pharyngeal glands in last part of IV, and well developed in V and VI, dorsally and laterally. Chloragogenous tissue starting in the hind part of VI and well developed from VII backwards. Nephridia present on at least one side in VII in some specimens; most specimens have at least one nephridium in XIII, and in a few posterior segments. Nephridiopores inconspicuous, without vesicles; nephridial duct very thin and transparent. Sperm sac extends forward to VIII, and backward to XII–XV. Egg sac back to XIII–XVII.
Two pairs testes, in segments IX and X, and one pair ovaries in segment XI. Two vasa deferentia per atrium (semiprosoporous condition), originating in sperm funnels located in the septa of intersegment 9/10 and 10/11, respectively. Posterior vas deferens not entering segment XI. Vasa deferentia very narrow (8–14 µm diameter), joining the atrium in the ectal (or basal) part of the ampulla, and running through the atrial musculature to the apical part of the atrium, where they open to the atrial lumen (Figs
Female funnels large, attached to the septum and opening in intersegment 11/12 (Fig.
Cookidrilus pocosinus sp. n. has been ascribed to the genus Cookidrilus Rodriguez & Giani, 1987 based on the main diagnostic characters of the genus: 2 pair testes and one pair ovaries, two (anterior and posterior) vasa deferentia joining each atrium, one pair spermathecae in the atrial segment, and subsequent pairs of spermathecae in postatrial segments (
In Table
Morphological characters of the three known species of the genus Cookidrilus Rodriguez & Giani, 1987.
Cookidrilus | speluncaeus | ruffoi | pocosinus sp. n. |
---|---|---|---|
Body diameter | 350 µm at clitellum | 583–633 µm | 360–441 µm at clitellum |
Double annulation begins | In III | – | In VI |
Prostomium form and length | Round, 76–83 µm | Often wrinkled, 305–400 µm | Round, 120–154 µm |
Clitellum | X–XII | Poorly developed, in X–XII | X–XII |
Pharynx | Dorsal and ventrally well developed, in II–IV | Dorsal and ventrally well developed, back to VII, VIII | Typical dorsal pad, in II–III |
Pharyngeal glands | IV–VIII | III–VII (VIII) | IV (posterior)–VI |
Chaetae, length | 73–82 µm in ante-clitellar region | 105–112 µm in II, 174–236 µm in anterior to middle region | 56–62 µm in II, 68–82 µm in anterior to middle region |
Posterior body region | Not modified | Evaginable tube | Not modified |
Spermathecae, number and position of pores | 3 pairs, pores behind ventral chaetae | 2 pairs, pores behind ventral chaetae | 3 pairs, pores in front of ventral chaetae |
Spermathecal ducts, form and length | Tubular, short ducts 44–76 µm | Bottle shaped, 115–143 µm | Bottle shaped, short ducts, 34–86 µm |
Spermathecal ampulla | The first is small, the third penetrates XIII | Do not penetrate other segments | The first smaller. Do not penetrate other segments |
Atrium | In X | In X | In X |
Atrial ampulla, shape and size | Pyriform, 71 µm long, 48 µm Ø | Pyriform, 207 µm long, 161 µm Ø | Tubular, 86–110 µm long, 26–30 µm Ø |
Atrial duct length | 29 µm | 84 µm | 34–40 µm |
Penis | Simple pore | Protrusible penis | Protrusible penis |
Prostate layer | Dense, diffuse layer | 3–4 clusters of cells | 8–10 clusters of cells |
Atrial muscular layer | 4 µm thick | 16–20 µm thick | 2–3 µm thick |
Vas deferens diameter / junction to the atrium | 11 µm / apical | 15–20 µm / lateral | 8–14 µm / at the base of the ampulla (opening apically) |
Posterior vas deferens | Penetrates 10/11 | Penetrates 10/11 | Does not penetrate 10/11 |
In the original description of the genus,
The presence of penis may be a common generic character in Cookidrilus, since it is only absent in the type species, C. speluncaeus. On the other hand, C. ruffoi differs in the number of spermathecae. The analysis of lumbriculid genera performed by
The position of spermathecal pores in front of the ventral chaetae is an unusual feature of the new Cookidrilus species. Spermathecal pores in lumbriculids are usually placed behind the chaetae of the corresponding segment, and in the other 2 species of Cookidrilus, even the first spermatheca opens in the narrow space between the ventral chaetae and the male pores. This character is shared with several Nearctic lumbriculids: K. hexatheca (for the first pair of spermathecae), some Rhynchelmis species (in
Cookidrilus pocosinus sp. n. appears to have a life cycle adapted to seasonal drying of surface flow. This is the first record of Cookidrilus in North America, and it is also the first report of the genus in a non-subterranean habitat. This species has been found so far in four North Carolina streams, but almost all specimens were from Lake Run and Pettiford Creek. These streams are both located in the southern Coastal Plain, in relatively undisturbed watersheds, and drain pocosin areas with peat soils. Both streams have extremely low pH values (often less than 4.0), very low conductivity, and dry up completely during summer droughts. In Lake Run, most specimens were found in shaded sections, in midstream areas with both good flow and a fine sand substrate. In Pettiford Creek, the substrate consisted of fine sand covered by a layer of organic debris. These data indicate that C. pocosinus is usually associated with very low pH, although single specimens were collected from a seasonally inundated side channel of Drowning Creek, and from the main channel of Anderson Creek. Both of those streams have average pH values near 5.5.
(amended by
Chaetae sigmoid, simple-pointed. One pair male pores in segment X (the second testis-bearing segment), behind and in line with the ventral chaetae. Two or three pairs spermathecae; first pair in the atrial segment, anterior to male pores, and one pair in the first, or in the first and second postatrial segments. Two pair testes, in IX and X. One pair atria in the second testicular segment. Semiprosoporous male duct, two vasa deferentia per atrium. Prostatic cells either in a simple diffuse layer or forming discrete clusters. One pair ovaries located in the first postatrial segment (XI).
USNM 1251703: A whole-mounted specimen in Canada balsam (collected 19 Jan 2010).
USNM 1251704-1251707: 17 Feb 2007, 1 whole mount; 19 Jan 2010, 2 whole mounts; 5 Apr 2010, 1 dissected. MNCN 16.03/3085: 19 Jan 2010, 1 dissected and 1 histologically sectioned; 5 Apr 2010, 1 whole mount, stained in borax carmine. CASIZ 197900: 16 Feb 2011, 2 dissected. All from the type locality.
Pettiford Creek at Millis Road, Carteret County, North Carolina, USA.
This species is named in honor of Jesse Edward (Ed) Corey III, an Inventory Biologist at the North Carolina Division of Parks and Recreation. We celebrate Ed’s unwavering interest in all animals and plants, including our beloved oligochaete worms.
From the type locality: 17 Feb 2007, 1 dissected. 30 Sep 2009, 7 whole mounts, 1 dissected. 19 Jan 2010, 5 whole mounts, 2 dissected, 3 sectioned (2 sagittal, 1 transverse), 2 in alcohol. 5 Apr 2010, 6 whole mounts, 2 dissected. 16 Feb 2011, 1 whole mount, 10 in alcohol. Floodplain seeps in Drowning Creek floodplain at State Road 1004, Moore County, North Carolina: 31 Dec 2008, 2 whole mounts. 12 Jan 2009, 2 whole mounts, 5 dissected. 17 Feb 2011, 1 whole mount. All specimens (including the type series) collected by D.R. Lenat.
Number of segments 53–69. In 27 unmounted specimens, body length 11.7–14.2 mm, diameter of the body in segment VIII, 240–585 µm (mean 379 µm); maximum diameter in the clitellar region to 760 µm (mean 467 µm); midbody diameter 330–630 µm (mean 429 µm). Prostomium round or conical, 142–196 µm long (Figs
Stylodrilus coreyi sp. n. A Anterior part of the body, B: simple-pointed chaeta C clitellum D nephridial efferent duct in ventral part of posterior segment (anterior part facing up) E–G consecutive histological sections of male duct H–I details of prostatic glands and connection to atrial ampulla J spermathecal ampulla K spermathecal duct L female funnel. E–L histological sections, other photographs from stained whole mounts or dissected specimens.
Chaetae simple-pointed (Fig.
One pair spermathecal pores in segment IX and one pair male pores in segment X, in line with and behind the ventral bundles of chaetae (one specimen from Drowning Creek regenerating the anterior part of the body, with spermathecal pores in VII and male pores in VIII). One pair female pores in the intersegment 11/12.
Pharyngeal pad well-developed dorsally, usually extending through IV; pharyngeal glands from the posterior part of segment IV back to VIII, dorso-lateral and ventral to the gut in segments V to VIII (Fig.
Semiprosoporous male ducts, with one anterior vas deferens attached to the sperm funnel in intersegment 9/10, and the posterior one to the funnel in 10/11, the anterior being longer (280–480 µm) than the posterior (215–300 µm). Both funnels appear deflected backward, somewhat behind their respective septa when full of sperm. Vasa deferentia (15)20–28 µm in diameter, to 34 µm close to the sperm funnel. Posterior vas deferens does not enter postatrial segment (Figs
One pair spermathecae, with ampullae typically located in segments IX and X, oval to nearly spherical (174–331 µm diameter, 205–348 µm long), containing a mass of loose sperm in the ectal part, sometimes together with amorphous material (Figs
Worms from Downing Cr are generally larger than those from Pettiford Cr (see Table
Comparison of morphological features in two study populations of Stylodrilus coreyi sp. n.
Population | No. segments | Body Ø in VIII µm | Chaetae length µm | Atrium length µm | Atrium Ø µm | Spth duct length µm | Spth ampulla length µm | Spth ampulla Ø µm |
---|---|---|---|---|---|---|---|---|
Pettiford Creek | 53–65 | 240–420 | 63–105 | 176–248 | 40–63 | c.163–225 | 205–206 | 174–179 |
Drowning Creek | 55–69 | 390–585 | 81–120 | 266–390 | 54–74 | 150–247 | 239–348 | 198–331 |
Stylodrilus coreyi sp. n. conforms to the general diagnosis of the genus Stylodrilus Claparède, 1862 (see
Stylodrilus coreyi sp. n. belongs to a group of Stylodrilus species with simple-pointed chaetae, elongate atrium, and posterior vas deferens not forming a loop in the postatrial segment (Table
Stylodrilus species with simple-pointed chaetae, elongate to tubular atrium, vas deferens not entering postatrial segment.
Species | Atrium position (segment) | Atrial ampulla/duct size | Prostate | Vas deferens junction to atrium | Penis | Spermatheca | Spermathecal ampulla/duct size | Posterior lateral blood vessels |
---|---|---|---|---|---|---|---|---|
S. curvithecus Collado et al., 1993 | X–XI | Atrium elongate, ampulla pyriform, length > duct | Diffuse, poorly developed | At the base of the ampulla, but open subapically to atrial lumen | Conical, in a fold of the body wall, with muscular bulb and associated glands | Restricted to segment IX | Ampulla folded, length > duct | Absent |
S. glandulosus Giani & Martínez-Ansemil, 1984 | X–XI(XII) | Ampulla elongate, length ≈ duct | Diffuse | At the base of the ampulla, but open subapically to atrial lumen | Conical, in a fold of the body wall, with muscular bulb and associated glands | Restricted to segment IX | Ampulla oval, length < duct | Present (not branching) |
S. tschaunensis Morev, 1982 | X | Ampulla pyriform, length>duct | Diffuse | At the base of the ampulla, but open apically to the atrial lumen | Absent | In IX | Sac-shaped ampulla, length > duct | Present, short and slightly branching |
S. wahkeenensis Rodriguez & Coates, 1996 | IX | Atrial duct absent | Diffuse | Medially | Absent | Ampulla in VII–VIII (genitalia shifted forward) | Ampulla length > duct (both elongate) | Absent |
S. coreyi sp. n. | X–XI | Ampulla tubular, >> duct | In petiolate clusters | At the base of the ampulla, but open apically to atrial lumen | Short penis | Ampulla in IX–X | Ampulla oval, length < duct | Absent |
Among this group of species, S. wahkeenensis Rodriguez & Coates, 1996 can be distinguished from S. coreyi not only by the remarkable shape of the chaetae (proximal nodulus, hair-like in dorsal bundles, and enlarged, hook-shaped in ventral bundles of segment II), but also by the position and structure of the atrium (in segment IX, small and covered by a simple, diffuse layer of prostatic cells, with no duct or penis observed). Of the other species in that group, S. glandulosus Giani & Martínez-Ansemil, 1984 and S. curvithecus Collado et al., 1993 are separated from congeners by clear apomorphies, such as a muscular, bulbous penial sac with associated glandular complex, and a long atrial duct. Stylodrilus beattiei Cook, 1975 and S. tschaunensis Morev, 1982 also have simple-pointed chaetae and vas deferens not penetrating the postatrial segment, but they are well distinguished from this species group by the distinctly petiolate atrium with oval or pyriform ampulla, short atrial duct, and absence of a penis. Other species of the genus in which the posterior vas deferens does not penetrate the post-atrial segment are S. cernosvitovi Hrabě, 1950, S. mirandus (Hrabě, 1982), and S. aclotudi Kaygorodova & Martin, 2008, but they all have bifid chaetae.
Stylodrilus species with simple chaetae and an elongate to tubular atrium with short atrial duct include S. absoloni (Hrabě, 1970), S. lemani and S. chukotensis Sokolskaya, 1975, but in these species, the vas deferens penetrates the post-atrial segment, forming a loop. Another species in this group is S. sulci (Hrabě, 1934), distinguished from S. coreyi by the median junction of vasa deferentia to the atrium, the entrance of the posterior vas deferens into the postatrial segment, and the absence of a penis.
In North America, there are only five Stylodrilus species known so far, one of which is cosmopolitan (S. heringianus Claparède, 1862). Stylodrilus beattiei (Cook, 1975) was the first Nearctic Stylodrilus species described, from a cave in West Virginia. Subsequently, S. sovaliki (Holmquist, 1976) was described from lakes in Alaska. Later, S. californianus Rodriguez, 1996 was discovered in subterranean waters in eastern California, and S. wahkeenensis Rodriguez & Coates, 1996, was described from hyporheic waters and small streams associated with subterranean waters of Oregon and southeastern USA.
The low number of Stylodrilus species in North America may be related in part to the tendency of researchers in this area to erect new genera for those taxa with very distinct apomorphies (e.g., Spelaedrilus Cook, 1975, Phagodrilus McKey-Fender & Fender, 1988, Tenagodrilus Eckroth & Brinkhurst, 1996), despite a general arrangement of the reproductive system that fits the Stylodrilus pattern. This situation indicates the need for a sound revision of the genus, since some Stylodrilus species can in fact be closer to other genera.
Stylodrilus coreyi sp. n. has been collected from seeps and pools in humic coastal plain streams (Drowning and Pettiford Creeks), most commonly outside of the main channel. These habitats have a temporary flow regime, with seasonal drying during summer months. S. coreyi was mostly collected in detritus over a layer of fine sand. Both streams have very high water quality (
The new taxa show several characters that are interesting in the context of taxonomy of the family Lumbriculidae, and are worth a more general discussion.
In the present paper, we describe three species that differ in number and position of spermathecae. The phylogenetic analysis of the family Lumbriculidae performed by
With respect to the spermathecal pores, it is interesting to note that the most common (and thus probably ancestral) position in aquatic oligochaetes is in the anterior part of the segment, in front of the ventral chaetae or even very close to the anterior septum. This is also the most common position within the family Naididae (sensu
The organization of prostatic cells into petiolate bundles has been reported before in several lumbriculid genera, but to date this character has not been considered diagnostic for genera. Therefore, species with either diffuse or clustered prostatic cells are found within Trichodrilus (see
“Cuticular penis sheath” has been a confusing term, since different structures may be fundamentally homologous as presumably derived from ectodermal secretions of the developing penis.
In Lumbriculus variegatus,
Biomonitoring programs are well developed for larger streams and rivers (
The presence of lumbriculids can be particularly useful when the diversity of the macroinvertebrate community is limited by low pH (Lake Run, Pettiford Creek), lack of water during summer months (Lake Run, Pettiford Creek, Drowning Creek floodplain, UT Pokeberry Creek) or small size (UT Pokeberry Creek). UT Pokeberry Creek presents a very interesting example where the larger creek was severely affected by nonpoint source runoff, but the small seeps (which supported a variety of rare invertebrates) were shown to worthy of environmental protection (Lenat, unpublished data). The study and mapping of unusual aquatic habitats (including pools, seeps, and swamps) will bring interesting novelties to the field of biodiversity and ecology, since the range of environmental conditions and microhabitats differs from those commonly studied in rivers. Future collections from these poorly studied habitats can also give light to the fields of systematics and zoogeography. For example, springs or swamps in southeastern North America constitute the only known habitat for three recently-described, monotypic lumbriculid genera (Sylphella, Pilaridrilus, Pararhynchelmis), and have also provided dramatic range extensions for such genera as Rhynchelmis, Cookidrilus, and Altmanella.
We are grateful to Dr Akifumi Ohtaka for putting at our disposal Yamaguchi’s histological preparations of Lumbriculus japonicus, as well as a specimen of Styloscolex japonicus. We thank Mark Wetzel and Christer Erséus for valuable comments on the manuscript. This work was made possible for the first author thanks to a sabbatical permit of the University of the Basque Country (from October 2010 to September 2011), partially supported by the Basque Government research project GIU10/140, and to Cindy Brown for providing access to laboratory facilities at the US Geological Survey Menlo Park campus (CA, USA) during P. Rodriguez’s sabbatical period.
Key of the known North American Stylodrilus species
1 | Chaetae bifid, with short upper tooth (some chaetae in anterior segments can be simple-pointed) | 2 |
– | All chaetae simple-pointed | 3 |
2 | Penis long, permanently protruded, atrium oval, spermathecal duct long | S. heringianus Claparède, 1862 |
Medium size worms (0.6–1 mm diameter). Prostatic cells forming clusters, thick (to 30 μm) vasa deferentia join atrial ampulla apically, posterior vas deferens penetrates the postatrial segment. 2 pairs short, unbranched lateral blood vessels in posterior segments. Widespread in Northern USA and Canada, including the Great Lakes. | ||
– | Penis short, atrium elongate, spermathecal duct very short | S. californianus Rodriguez, 1996 |
Small worms (0.2–0.5 mm diameter). Vasa deferentia join the atral ampulla medially and open to large lumen apically after running through the atrial musculature, posterior vas deferens penetrates the postatrial segment. Ridgecrest, eastern California, phreatic waters (in a well). | ||
3 | Chaetae with markedly proximal nodulus, dorsals with very long (hair-like) distal end | S. wahkeenensis Rodriguez & Coates, 1996 |
Small worms (0.3–0.4 mm diameter). Atria in IX, tubular, posterior vas deferens not penetrating the postatrial segment, atrial duct and penis absent, spermathecal duct long and thick. Oregon, Alabama and Tennessee; hyporheic and small rivers associated with subterranean waters. | ||
– | Chaetae with distal nodulus | 4 |
4 | Atrium elongate, duct weakly separated from ampulla and of similar diameter | S. coreyi sp. n. |
Small worm (0.3–0.4 mm diameter). Posterior vas deferens not penetrating the postatrial segment. North Carolina, pocosin, acidic waters. | ||
– | Atrium pedunculate, duct clearly separated from ampulla, and much narrower | 5 |
5 | Posterior vas deferens does not enter the postatrial segment; vasa deferentia join atrial ampulla and open to the lumen basally | S. beattiei Cook, 1975 |
Medium size worm (0.7–0.9 mm diameter). Prostatic cells small and disappearing soon after mating; lateral blood vessels absent in posterior segments. Tub Cave, West Virginia. | ||
– | Posterior vas deferens penetrates the postatrial segment; vasa deferentia join atrial ampulla basally and open to the lumen medially | S. sovaliki (Holmquist, 1976) |
Medium to large size (about 1 mm diameter). Prostatic cells in bundles, posterior lateral blood vessels branched. Alaska, rivers. |
Location of study sites (all in North Carolina, USA), and species described in present paper.
Stream | Latitude | Longitude | Ecoregion | Species described |
---|---|---|---|---|
Unnamed tributary to Pokeberry Cr | N35.8267 | W79.1013 | Piedmont | Sylphella puccoon gen. n., sp. n |
Pettiford Cr | N34.7471 | W77.0221 | Coastal Plain |
Cookidrilus pocosinus sp. n. Stylodrilus coreyi sp. n. |
Lake Run | N34.7773 | W78.6646 | Coastal Plain | Cookidrilus pocosinus sp. n. |
Anderson Cr tributary to the Lower Little River | N35.2661 | W78.8192 | Sandhills | Cookidrilus pocosinus sp. n. |
Drowning Cr | N35.0662 | W79.5496 | Sandhills |
Cookidrilus pocosinus sp. n. Stylodrilus coreyi sp. n. |