Metaphire agrestis (Goto & Hatai, 1899)

Figs 2, 3

Perichaeta agrestis Goto & Hatai, 1899: 17, 24.

Pheretima agrestis — Michaelsen 1900: 313; Yamaguchi 1930: 51; 1962: 25; Kobayashi 1938: 141; Hatai 1930: 651; Howell 1939: 231. Gates 1953: 5; 1954: 224; 1958: 1, 31; 1963: 11; 1982: 38.

Amynthas agrestis — Beddard 1900: 637; Sims and Easton 1972: 235. Reynolds 1978: 119, 127; 2010: 143; 2011: 269; 2014: 116; 2022: 110. Easton 1981: 51. Reynolds and Wetzel 2004: 88; 2008: 179. Hong and Kim 2005: 130; 2009: 137. Blakemore 2010: 429; 2013 a: 56, 57; Chang et al. 2016: 503. Minamiya 2017: 14; Shekhovtsov et al. 2018: 11. Schall et al. 2023: 58.

Metaphire agrestis — Blakemore 2003: 7, 28 (syn. striata). Uchida and Ihara 2003: 34. Uchida and Kaneko 2004: 37. Iki and Ohba 2022: 42. Sato et al. 2023: 5, 6, 8.

Pheretima hataii — Ohfuchi, 1937: 13; Ohfuchi, 1938: 178.

Metaphire hataii — Sims and Easton 1972: 238. Easton, 1981: 58. Blakemore, 2007 a: 46; 2008: 113; 2010 a: 19; 2012: 19.

Material examined.

• 5 clitellates (533 R 71_02, 533 R 72_03, 533 R 74_01, 533 R 74_02, and 533 R 75_02) from Jinjiangshan Park, Dandong Prefecture, Liaoning (40.1312°N, 124.3746°E, 40 m elev.), collected by Huifeng Zhao, Shixiong Ma, Yanmeng Bi, and Yufeng Zhang, 2023-07-26. All other specimens have been deposited in C-HLU.

Diagnosis (modified from Reynolds 2022).

Size 70–200 mm length by 5–8 mm (clitellum width). Segment numbers 63–110. Spermathecal pores three pairs in 5 / 6 / 7 / 8. Pre-clitellar genital markings present or absent; when present, ventral, areas of slight epidermal modification on VII and / or VIII, occasionally on VI and IX, unpaired and median or symmetrically paired, forming setal gaps, epidermis finely wrinkled or crosshatched, sometimes darker in color in live specimens. Male pores usually absent; when present, small, transversely slit-like. Post-clitellar genital markings usually absent; when present, single, large circular pad, pre-setal on XVIII, just median to male pores, with a concave center surrounded by a narrow but distinct, raised rim, reaching posteriorly slightly behind the setal line on XVIII and anteriorly to the setal line on XVII. Spermathecae present or absent; when fully present, three pairs in VI – VIII, duct shorter than ampulla; diverticulum longer than the main pouch. Prostate glands present or absent; when present, extending through some or all of XVI – XXIII, ducts in XVIII. Accessory gland mostly absent, when present, large and paired in front of the setal line on segment XVIII. Intestinal caeca paired in XXVII extending anteriorly to XX, digitate.

Description of Chinese specimens in this study.

External characters. Length 80–94 mm by width 5.0–8.0 mm (n = 5). Color of live specimens reddish-brown. Color of preserved specimens may vary in shades because of the duration of preservation but generally brownish-yellow (with blackish highlights) throughout with milk gray clitellum. Number of segments 100–108. Prostomium epilobous (Fig. 2 A). First dorsal pore on 12 / 13. Clitellum annular at XIV – XVI; setae or dorsal pores and intersegmental furrow absent. Setal arrangement perichaetine; setae number 36–40 (V), 52–65 (VII), and 55–72 (VIII). Female pore single in medio-ventral at XIV (Fig. 2 B). Spermathecal pores three pairs, 5 / 6–7 / 8, ventro-lateral, 0.28–0.30 C apart ventrally. Pre-clitellar genital markings absent (Fig. 2 D). Male pores and post-clitellar genital markings absent.

Internal characters. Septa 4 / 5 / 6 quite thickened, 6 / 7 / 8 thin and fibrous, 8 / 9 / 10 absent, 10 / 11 / 12 / 13 thin. Gizzard within VIII – IX (Fig. 2 C). Intestine enlarged from XIV. Intestinal caeca manicate with five finger-like sacs, originating in XXVII and extending anteriorly to XX (Fig. 3 H). Last pair of hearts in XIII.

Spermathecae present, three pairs in VI – VIII ampulla ovate, surface flattened and wrinkled, 1.5–1.8 mm long; ampulla duct long, stout, 1.1–1.3 mm long, with a swollen basal portion; diverticulum originating from below the swollen portion of the spermathecal duct, stalk slender with a swollen long receptacle; diverticulum longer than the main pouch (Fig. 2 E). Seminal vesicles two pairs in XI and XII, well developed. Prostate glands and accessory glands absent.

Global distribution.

Cosmopolitan / Exotic. USA (Gates 1953, 1954, 1958, 1963, 1966, 1982; Davies 1954; Reynolds 1978, 2010, 2011, 2015 a, 2015 b; Callaham et al. 2002; Görres and Melnichuk 2012; Chang et al. 2016; Görres et al. 2017; Chang et al. 2021), Canada (Reynolds 2014, 2023), Japan (Kato 1972; Minamiya 2014), South Korea (Kobayashi 1935; Song and Paik 1969, 1970 a, 1970 b, 1971, 1973; Hong and Kim 2005; Hong and Kim 2009; Blakemore 2013 a, 2013 b), North Korea (Kobayashi 1935, 1938); Russia (Shekhovtsov et al. 2018), and China (this study).

Distribution in China.

Liaoning Province, northeast China.

Habitat.

Urban parks.

Biology.

Known as “jumping worms”, “snake worms”, or “crazy worms” because of their erratic thrashing behavior when disturbed.

Remarks.

Relevant literature revealed that M. agrestis (= A. agrestis) has not been previously recorded in China (Blakemore 2007 b, 2009; Xu and Xiao 2011). Metaphire agrestis is widely distributed in East Asia such as Japan (Kato 1972; Minamiya 2014), Korean Peninsula (Kobayashi 1935, 1938; Hong and Kim 2005, 2009; Blakemore 2013 a, b) and in the northern islands (Kunashiri Island and Yuri Island) of Russia (Shekhovtsov et al. 2018). It is known to be mostly dominant in Japan and Korean peninsula, where it is considered as native. Metaphire agrestis is also considered as one of the invasive pheretimoid earthworms in the USA and Canada where it is rather known as A. agrestis (Chang et al. 2016, 2021; Keller et al. 2017; Reynolds 1978, 2023).

Additional descriptions of M. agrestis (= A. agrestis) were made by Gates (1982) and Reynolds (1978). Subsequently, Pheretima hataii (= M. hataii), which was described by Ohfuchi (1937), possesses some distinguishing features (having red pre-clitellar genital markings only on VII, invariably possessing one pair of male pores and genital markings pre-setal on XVIII and having paired genital markings pre-setal on XVIII) from that of M. agrestis (having red pre-clitellar genital markings on both VII and XII, has a very low rate of species with male pores). Given these insufficient descriptions for it to be recognized as a distinct species, Uehira (1978) suggested the possibility of its synonymization to M. agrestis (Minamiya 2014). Likewise, Minamiya (pers. comm. 18 Nov 2025) considered P. hataii (= M. hataii) as a synonym of M. agrestis, stating that the distinguishing characters described in the original record for P. hataii (= M. hataii) are included within the individual variation of M. agrestis.

A summary of comparison for M. agrestis is presented in Table 4. All Chinese specimens of M. agrestis were found to have no male pores, which pertains to parthenogenetic reproduction. Meanwhile, specimens of the USA are also usually without male pores. If present, male pores are small, transversely slit-like (Chang et al. 2016), and the distance between male pores is ~ 1 / 3 of the body circumference (Kobayashi 1938; Reynolds 1978). Reynolds (1978, 2023) described the male pores as being “ minute and located on an eversible papilla, inside a transverse slit-like parietal invagination on an elevated porophore. ” It is also worth noting that Reynolds (2023) has used the same photographs of A. agrestis reported by Chang et al. (2016). Post-clitellar markings usually absent, if present, they are paired, pre-setal on the XVIII, measuring 0.8–2.2 mm.

Chang et al. (2016) provided a photograph of a specimen of A. agrestis with a single male pore and a genital marking (Fig. 3 B). This figure matches with the original illustration of the male pore and genital markings of P. hataii (= M. agrestis) (Fig. 3 A) by Ohfuchi (1937) and with a M. agrestis specimen from Japan (Fig. 3 C; photograph provided by Minamiya, pers. comm. 18 Nov 2025) although the latter two figures have paired male pores and genital markings. Meanwhile, the spermathecae of the Chinese specimens (Fig. 3 E) match their corresponding specimen counterparts from Japan (Fig. 3 D) and the USA (Fig. 3 F); whereas the intestinal caeca (Fig. 3 H) match those from the USA (Fig. 3 G).