Research Article |
Corresponding author: Fahri Fahri ( fahribadjeber11@gmail.com ) Corresponding author: Anh D. Nguyen ( ducanh410@yahoo.com ) Academic editor: Samuel James
© 2018 Fahri Fahri, Rizki Amaliah, Bambang Suryobroto, Tri Atmowidi, Anh D. Nguyen.
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:
Fahri F, Amaliah R, Suryobroto B, Atmowidi T, Nguyen AD (2018) Three new “caecate” earthworm species from Sulawesi, Indonesia (Oligochaeta, Megascolecidae). ZooKeys 805: 1-14. https://doi.org/10.3897/zookeys.805.24834
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Three new earthworm species are described from Sulawesi, Indonesia. Two belong to the genus Pithemera Sims & Easton, 1972, namely P. suwastikai Fahri, Amaliah & Atmowidi, sp. n. and P. tadulako Fahri, Amaliah & Atmowidi, sp. n. The new species, P. suwastikai sp. n. is distinguished by a medium size (135–165 mm long, 4.5–6.5 mm diameter), four pairs of spermathecal pores in 5/6/7/8/9, 7–12 setae between male pores, no genital markings, holandry, and simple intestinal caeca. Pithemera tadulako sp. n. is recognized by a large size (217–340 mm long, 13–15 mm diameter), two pairs of spermathecal pores in 7/8/9, no setae between male pores, no genital markings, holandry, and simple intestinal caeca. Another new species, Metaphire rusydii Fahri, Amaliah & Nguyen, sp. n., is diagnosed by its large size (250–280 mm long,12–16 mm diameter), two pairs of spermathecal pores in 7/8/9, no setae between male porophores, presence of genital markings in the male region, holandry, and complex intestinal caeca. Additionally, an identification key to “caecate” species is provided to the Sulawesi’s fauna.
Caecate earthworms, Indonesia, Metaphire , new species, Pithemera , Sulawesi
Earthworms with intestinal caeca consists of four genera belonging to family Megascolecidae, namely Pithemera Sims & Easton, 1972, Amynthas Kinberg, 1867, Pheretima Kinberg, 1867, and Metaphire Sims & Easton, 1972. This group is distributed in the Oriental to Australian region (
Earthworms from Sulawesi have been reported by
Fresh specimens were collected from yards at Lomba village (00°53'05.9"S, 123°17'50.0"E), Banggai district, 26 March 2016 and Puncak Jiti near Lore Lindu National Park (01°29'18.94"S, 120°02'09.28"E), Toro village, South Kulawi sub–district, Sigi district, Central Sulawesi, Indonesia, 28 May 2017. Hiking trail 1 (01°25'18.44"S, 119°55'00.14"E) 25 November 2017 and hiking trail No.2 (01°25'17.54"S, 119°53'53.4"E) 24 November 2017, natural forest of Mt. Torompupu, Quarlesi Mountain, Salua village, Kulawi sub–district, Sigi district, Central Sulawesi, Indonesia (Fig.
The earthworms were killed in formalin 2%, transferred to 4% formalin for fixation for approximately 24 hours, and then transferred to fresh 4% formalin for long–term preservation and morphological studies. Specimens were dissected from the dorsal side for internal observation. Both external and internal morphology were observed under a Nikon type 104 C-LEDS stereo microscope. Holotypes and paratypes are deposited in Museum of Zoology in Bogor (
Perichaeta bicincta Perrier, 1875, by original designation.
Pithemera members are easily recognized by the origin of intestinal caeca at xxii. Sims & Easton (1972) divided Pithemera into three groups: P. sedgwicki group with intestinal caeca characters being single in mid-ventral, P. bicincta group with intestinal caeca being paired laterally and first spermathecal pores in 4/5, and P. pacifica group with intestinal caeca being paired laterally, first spermathecal pores in 5/6 and four thecal segments. Currently, the genus consists of 26 nominal species distributed mainly in New Guinea, and the Philippines (http://taxo.drilobase.org).
Holotype. 1 mature (
Medium size, length 135–165 mm, diameter 4.5–5.5 mm at x and 4.5–6.5mm at xx, segments 110–127. Prostomium epilobous. First dorsal pore in 12/13. Setae 27–38 in v, 33–49 in vii, 38–54 in viii and 64–74 in xxv, and 7–12 between male porophores in xviii. Spermathecal pores arranged in four pairs, 5/6–8/9. Male pores paired, discharging directly onto surface of xviii. Genital markings absent. Holandric. Intestinal caeca originating from xxii, paired laterally.
The species is named after Dr I Nengah Suwastika, head of the Biology Department of Tadulako University for his kind support of our study on Sulawesi earthworms.
External characters. Body generally cylindrical. Medium size, length 135–165 mm, diameter 4.5–5.5 mm at x and 4.5–6.5mm at xx, segments 110–127. Brownish red on dorsum, dark brown around clitellum and yellowish white on ventrum, especially in living specimens (Fig.
Pithemera suwastikai sp. n., holotype. A Living specimen (dorsal view); B Spermathecal pore; C Spermathecae, right side on intrasegmental 5/6/7/8/9 (am = ampulla; dv = diverticulum); D Prostate gland; E Male pore region (mp = male pore); F Intestinal caecum. Scale bars: 50 mm (A), 1 mm (B–F).
Prostomium epilobous. First dorsal pore in 12/13. Setae regularly distributed around segmental equators: 27–38 in v, 33–49 in vii (Table
Character | P. donvictorianoi Aspe & James, 2015 | P. pacifica (Beddard, 1899) | P. dahli (Ude, 1905) | P. suwastikai sp. n. |
---|---|---|---|---|
Length (mm) | 41–58 | 56 | 70 | 135–165 |
Diameter (mm) | 2.5–3.0 | - | 2.5 | 4.5–5.5 |
Segment number | 85–100 | 90 | 120 | 110–127 |
Clitellum | xiv to xv | xiv–xvi/ xiv–xv* | xvi–xvi | xiv–xvi |
Female pore | single | paired* | single | single |
Spermathecae pore | 5/6–8/9 (inconspicuous) | 5/6–8/9 | 5/6–8/9 | 5/6–8/9 |
Dorsal pore | 12/13 | - | 12/13 | 12/13 |
Copulatory pouches | absent | absent | absent | absent |
Genital marking | absent | present in xii–xiii, xvii–xviii, xx–xxii | present in x, xi, xvii–xxi | absent |
Setae on vii or viii | 42–48 (vii) | 47 (viii) | 70 (viii) | 33–49 (vii) |
Setae bet. male pore | 8 | 10 | - | 10–12 |
Septa | 8/9 absent | 8/9 present, thin | 9/10 absent | 8/9 absent |
Intestinal caeca | xxii to xxi | - | - | simple (xxii–xx) |
Last hearts | xiii | xii | xiii | xiii |
Testis | holandric | metandric | metandric | holandric |
Prostate gland | xvi to xix | xvii–xix | xvi–xxii | xvi–xx, xvii |
Spermathecal pores small, slightly rounded, lateroventrally paired in 5/6–8/9 (Fig.
The openings of male pores small, on the setal ring of xviii, paired and discharging directly onto surface of xviii (Fig.
Internal characters. Septa 3/4/5/6/7/8 thick, 8/9 absent, 9/10/11/12/13 thin. Gizzard round within viii-x. Last hearts in xiii. Intestine origin at xv; caeca originating at xxii, extending anteriorly to xx, simple and paired laterally (Fig.
Four pairs of spermathecae paired in vi–ix. Ampulla round; duct enlarged, stout, approx. 1/4–1/2 as long as ampulla; no nephridia on spermathecal ducts. Diverticulum cylindrical, longer than ampulla, attached to base of ducts (Fig.
Holandric. Testes sacs paired in x–xi, small, separated, ventral, yellowish. Seminal vesicles in xi–xii. Ovaries paired on xiii. Prostate gland racemose paired within xvi–xx or xvii–xx. Prostatic ducts long and U–shaped (Fig.
Specimens were collected in yards at Lomba village, Banggai district, Central Sulawesi, Indonesia at 5 m a.s.l. The species was found in sandy soils at depths of 0–10 cm, around the roots of banana trees planted 1–2 m away from houses. No other specimens were collected despite continued collecting effort. The specimens were collected at an elevation of 50 meters above sea level. When collected, earthworms were moving actively on the ground.
This new species belongs to the Pithemera pacifica group characterized by having the first spermathecal pores in 5/6 and four thecal segments (
The new species has similar characters to P. donvictorianoi Aspe & James, 2015, e.g., in the number of spermathecal pores, but different in clitellum (xiv–xvi vs. xiv–xv), setae on vii (33–49 vs. 42–48). P. suwastikai sp. n. also has different length with P. donvictorianoi (135–165 mm vs. 41–58 mm) and diameter (4.5–5.5 mm vs. 2.5–3.0 mm). In addition, P. donvictorianoi is a white worm, with small, narrow, oval spermathecal ampulla; ducts short, slender; diverticulum stalk short, attached to ducts, terminating in short ovate receptacle. In contrast, P. suwastikai sp. n. has brownish red pigment on dorsum, dark brown around clitellum and yellowish white on ventrum; ampulla rounded; ducts enlarged, approx. 1/4–1/2 as long as ampulla; diverticulum cylindrical, longer than ampulla, attached to base of ducts.
This new species is also similar to P. dahli (Ude, 1905) by having spermathecal pores in 5/6–8/9 and dorsal pore in 12/13. However, it differs from P. dahli in larger size (length: 135–165 mm vs. 70 mm; diameter 4.5–6.5 mm vs. 2.5 mm), absence of genital markings (vs. genital markings in x, xi, xvii–xxi), holandric (vs. metandric), and prostate glands in xvi–xx or xvii–xx (vs. in xvi–xxii). P. suwastikai sp. n. has also similar characters to P. pacifica (Beddard, 1899) in spermathecal pores (5/6–8/9) and dorsal pore (12/13), but it is totally different in absence of genital markings (vs. present in x, xi, xvii–xxi) and holandric (vs. metandric). The comparison of the four species is presented in Table
Holotype.1 mature (
Large size, length 217–340 mm, diameter 13–15 mm, segments 120–123; darkish blue on dorsum, purplish brown around clitellum and yellowish white on ventrum. Prostomium epilobous. First dorsal pore in 12/13. Setae 42–56 in v, 48–65 in vii, 44–69 in viii and 55 in xxv, and no setae between male porophores in xviii. Spermathecal pores lateroventrally paired in 7/8/9. Male pores paired, discharging directly onto surface of xviii. Genital markings absent. Holandric.
The species is named after the well–known Tadulako University in central Sulawesi. ‘Tadulako’ means a ‘leader’ in indigenous culture of central Sulawesi.
External characters. Body generally cylindrical; large size, length 217–340 mm, diameter 13–14 mm at x and 15 mm at xx, segments 120–123. Darkish blue on dorsum, purplish brown around clitellum and yellowish white on ventrum, especially for living specimens (Fig.
Prostomium epilobous. First dorsal pore in 12/13. Setae 42–56 in v, 48–65 in vii, 44–69 in viii and 55 at xxv, no setae between male porophores in xviii; setae distance aa=1–1.2ab, zz=1–2zy. Clitellum annular, xiv–xvi, smooth without setae and dorsal pores. Female pore single, mid-ventral in xiv.
Spermathecal pores small, lateroventrally paired in 7/8/9 (Fig.
Male pores small, forming vertical lines, paired and discharging directly onto surface of xviii (Fig.
Internal characters. Septa 3/4/5/6/7/8 thick, 8/9 absent, 9/10/11/12/13 thin. Pharyngeal gizzard within viii–x. Last hearts in xiii. Intestine originating at xv; caeca originating at xxii, extending anteriorly to xx, simple (Fig.
Two pairs of large spermathecae in viii–ix. Spermathecal ampulla oval; duct stout and very short; no nephridia on spermathecal ducts. Diverticulum claviform, much shorter than ampulla, attached to ducts (Fig.
Holandric. Testes sacs paired in x–xi, large, separated, ventral, yellowish. Seminal vesicles in xi–xii. Ovaries paired on xiii. Prostate glands racemose, paired in xvii–xix (Fig.
Specimens were collected in Puncak Jiti, Toro village, South Kulawi sub-district, Sigi district at 1,370 m a.s.l. and near Kalimpa’a Lake, Lore Lindu National Park at 1,600 m a.s.l. This species was found on the surface of soils after rains that contains a lot of leaf litter.
The new species is totally different from species groups divided by
The new species is somewhat similar to P. viengthongensis Hong &James, 2008 from Laos by having spermathecal pores in 7/8/9 and absence of genital markings. However, P. tadulako sp. n. is long (217–340 mm), and has more setae on vii (48–65), spermathecal ampulla being oval, ducts enlarged, short and stout; diverticulum cylindrical, shorter than ampulla. In contrast, P. viengthongensis is short (39 mm), has fewer setae on vii (37), spermathecal ampulla being ovate, smooth surface, duct short, thick; diverticulum stalk long and slender, chamber and chili-shaped. Moreover, two species are also distinguished by ventral distance between male porophores (0.02x body circumference in P. tadulako vs. 0.31x in P. viengthongensis).
Rhodopis javanica Kinberg, 1867, by monotypy.
This genus currently contains approximately 198 species widely distributed in the Oriental regions from Japan southwards through the Indo-Australasian archipelago to the rain forests of Australasia eastwards through Oceania (http://taxo.drilobase.org/index.php?title=Metaphire).
Holotype. 1 mature (
Large size, length 250–280 mm, diameter 12–16 mm, segments 117–119; purplish blue on dorsum, and paler on ventrum. Prostomium 1/3 epilobous. First dorsal pore in 11/12. Setae 36–51 in v, 45–54 in vii, 41–59 in viii and 43–51 in xxv, and no setae between male porophores in xviii. Male pores located in xviii, within copulatory pouches. Genital markings present only in the male region. Spermathecal pores lateroventrally paired in 7/8/9. Holandric. Intestinal caeca complex or lobed mesially.
The species is named after Dr H M Rusydi Hasanuddin, Dean of Faculty of Sciences at Tadulako University, for his kind support to the authors for this research.
External characters. Body generally cylindrical. Large size, length 250–280 mm, diameter 12–16 mm at x and 13–15 mm at xx, segments 117–119. Purplish blue on dorsum through the lateral region, clitellum purplish brown on dorsum through the lateral region and paler on ventrum, especially for living specimens (Fig.
Metaphire rusydii sp. n., holotype. A Living specimen (dorsal view); B Living specimen (ventral view of male pore region); C Preserved specimen (dorsal view); D Spermathecal pore; E Spermathecae, right side on intrasegmental 7/8/9 (am = ampulla; dv = diverticulum); F Prostate gland; G Male pore region (cp = opening copulatory pouch); H Intestinal caecum. Scale bars: 50 mm (A), 1 mm (C–H).
Prostomium 1/3 epilobous. First dorsal pore in 11/12. Setae regularly distributed around segmental equators, 36–51 in v, 45–54 in vii, 41–59 in viii and 43–51 in xxv, no setae between male porophores in xviii; setae distance aa=ab, zz=1–1.2zy. Clitellum annular, within xiv–xvi, smooth without setae and dorsal pores. Female pore single, mid-ventral in xiv.
Spermathecal pores obviously visible, horizontally elongated, jagged, or small, ventrally paired in 7/8/9 (Fig.
Male pores deeply located inside copulatory pouches in the setal ring of xviii. The openings of copulatory pouches horizontally elongated, with swollen edges; ventral distance between male porophores 0.02x body circumference (Fig.
Internal characters. Septa 3/4/5/6/7/8 and 10/11/12/13 thick, 8/9 membranous and 9/10 absent. Gizzard in viii. Last hearts in xiii. Intestine beginning in xv; caeca laterally paired, complex or lobed mesially, originating at xxvii, then extending anteriorly to xxii (Fig.
Spermathecae paired in viii and ix. Spermathecal ampulla large, oval shaped; ducts stout and short, 1/5 as long as ampulla. Diverticulum cylindrical, much shorter than ampulla, attached to ducts; distal part enlarged to a rounded seminal chamber (Fig.
Holandric. Testes sacs paired in x–xi, large, separated, ventral, yellowish. The copulatory pouches hidden inside body wall. Seminal vesicles in xi–xii. Ovaries paired on xiii, oviduct and ovisac developing in xiii. Prostate glands racemose, paired in xvii–xix (Fig.
Specimens were collected in Mt. Torompupu (Quarlessi Mountain), natural forest at 1,120 m a.s.l. and 1,360 m a.s.l. This species was found on soil surface in piles of leaf litter after rains. According to local hunters in Mt. Torompupu, the species can be mostly found after rains and usually observed on old trails in the forest. We did not find this species at an altitude of less than 1,000 m a.s.l.; presumably, the species may be distributed in an altitude of more than 1,000 m a.s.l.
The new species, Metaphire rusydii sp. n., belongs to the schmardae-group, which is characterized by two thecal segments, holandry, and having structure multiple/complex of intestinal caeca (
To date, a total of 17 earthworm species has been recorded from Sulawesi (
1 | Intestinal caecum, origin at xxii | 2 |
– | Intestinal caecum, origin at xxvii | 3 |
2 | Spermathecal pores in 5/6–8/9 | Pithemera suwastikai sp.n. |
– | Spermathecal pores in 7/8/9 | Pithemera tadulako sp.n. |
3 | Copulatory pouches absent; one to six pairs of spermathecal pores | 4 |
– | Copulatory pouches present; two or five pairs of spermathecal pores | 9 |
4 | Spermathecal pores from 7/8 | 5 |
– | Spermathecal pores absent or in3/4/5/6/7/8/9 | 8 |
5 | One pair of spermathecal pores in 7/8 | Amynthas zebrus |
– | Two pairs of spermathecal pores in 7/8/9 | 6 |
6 | Genital marking absent; the base with 12 secondary caeca | 7 |
– | Genital markings present | Amynthas purpurus |
7 | Dark olive-green. Ampulla with globular sac, with narrow (undulating) diverticulum, expanded terminally | Amynthas jampeanus |
– | Stone-grey to French-grey posteriorly. Ampulla with pyriform sac, long duct, receiving an undulating diverticulum, terminally dilated | Amynthas digitatus |
8 | Spermathecal pores absent | Amynthas bonthainensis |
– | Six pairs of spermathecal pores in 3/4/5/6/7/8/9 | Amynthas hexathecus |
9 | Spermathecal ducts with micronephridia. Three to five pairs of spermathecal pores in 4/5/6/7/8/9 | Pheretima darnleiensis |
– | Spermathecal ducts without micronephridia. Two two pairs of spermathecal pores in 7/8/9 | Metaphire rusydii sp. n. |
We thank our colleagues, Mihwan Sataral, Sofyan Ladjatang, and Endang Prasetyawati Wahyunigsih, Mus’af, Donny Aprilyanto, Evans Madiyono, Sucipto Suherman, and Pa Sahlan, for their assistance during fieldwork. Thanks are also due to Anna J. Holmquest, Jackie Childers, and Pa Sarino for their help in collecting Metaphire rusydii in Mt Torompupu. We would like to thank Dr Alexander L. Stubbs from University of California Berkeley for kindly correcting the English and invaluable comments to improve our manuscript. We would like to thank reviewers for the great comments and suggestions.
The research was partially supported by National Science Foundaton (NSF grant DEB 1457845) awarded to Professor Jimmy A. McGuire, entitle “A Biotic Inventory of Terrestrial Vertebrates, Arthropods, and Haemoporidium Parasities of Sulawesi, Indonesia” in Mt Torompupu. Also thank to Dr Anang Setiawan Achmadi for the opportunity to participate in the research. The paper is supported by the project “Penelitian Kerja Sama Antar PerguruanTinggi” between Tadulako University and Bogor Agricultural University 2017–2018, funded by Ministry of Research, Technology and Higher Education Indonesia.