Paraharmotrema karinganiense n. gen., n. sp. (Digenea: Liolopidae) infecting the intestine of serrated hinged terrapin (Pelusios sinuatus), east African black mud turtle (Pelusios subniger), and South African helmeted turtle (Pelomedusa galeata) and a phylogenetic hypothesis for liolopid genera

Abstract

We herein describe Paraharmotrema karinganiense n. gen., n. sp. Dutton & Bullard (Liolopidae Dollfus, 1934) from specimens infecting the intestine of the serrated hinged terrapin (Pelusios sinuatus), east African black mud turtle (Pelusios subniger) (both Nwanedzi River, Mozambique), and South African helmeted terrapin (Pelomedusa galeata) (North-western Zululand, KwaZulu-Natal Province, South Africa). The new genus can be easily differentiated from the other accepted liolopid genera (Liolope Cohn, 1902; Helicotrema Odhner, 1912; Harmotrema Nicoll, 1914; Dracovermis Brooks & Overstreet, 1978) by the combination of having a linguliform body approximately 6-9 × longer than wide, tegumental spines/scales, a minute ventral sucker located in the anterior 1/7-1/8 of the body, deeply lobed testes that are transverse and abut the caeca (spanning the intercaecal space), a uterus that is lateral to the anterior testis (not ventral to the anterior testis), a lobed ovary that is dextral and nearest the posterior testis, and a vitellarium that does not extend anteriad to the level of the ventral sucker and that does not fill the intercaecal space. Nucleotide sequences of large subunit ribosomal DNA (28S) and internal transcribed space region (ITS2) from all analyzed specimens of the new species were identical, respectively; the 28S sequences differed from that of Liolope copulans Cohn, 1902 and from that of Harmotrema laticaudae Yamaguti, 1933 by 103 (8%) and 105 (8%) nucleotides, respectively. The 28S phylogenetic analysis recovered the new genus sister to a clade comprising L. copulans and H. laticaudae. A key to liolopid genera is provided herein. The present study comprises the first nucleotide-based phylogenetic placement of Harmotrema and first record of a liolopid from South Africa or Mozambique. It is the first proposal of a new liolopid genus in 43 yrs, and it documents a second liolopid genus from P. subniger while tripling the number of liolopid turtle hosts reported from the continent of Africa.

Keywords: Parasite; Pelomedusidae; Pleurodira; Systematics; Taxonomy.

Graphical abstract

Figs. 1–2

Paraharmotrema karinganiense Dutton & Bullard n. sp. (Digenea: Liolopidae). (1) Body of adult (holotype, USNM No. 1659278) from intestine of serrated hinged terrapin, Pelusios sinuatus (Smith 1838) (Pleurodira: Pelomedusidae), ventral view. (2) Body of juvenile (paratype, USNM No. 1659285) from intestine of east African black mud turtle, Pelusios subniger (Bonnaterre, 1789) (Pleurodira: Pelomedusidae), dorsal view. Oral sucker (os), pharynx (ph), nerve commissure (nc), excretory system (es), sinistral caecum (sc), ventral sucker (vs), vitellarium (vr), cirrus sac (cs), metraterm (m), vas deferens (vd), anterior vas efferens (ave), anterior testis (at), uterus (u), posterior vas efferens (pve), ovary (o), posterior testis (pt), and excretory pore (ep).

Figs. 3–4

Paraharmotrema karinganiense Dutton & Bullard n. sp. (Digenea: Liolopidae) from intestine of serrated hinged terrapin, Pelusios sinuatus (Smith 1838) (Pleurodira: Pelomedusidae). (3) Female genitalia (holotype, USNM No. 1659278), ventral view. (4) Male genitalia (holotype, USNM No. 1659278), ventral view. Egg (e), ovary (o), oviduct (ov), ootype (oo), uterus (u), primary vitelline reservoir (pvr), dextral caecum (dc), transverse vitelline duct (tvd), sinistral caecum (sc), dextral excretory branch (deb), posterior vas efferens (pve), sinistral excretory branch (seb), posterior testis (pt), cirrus sac (cs), pars prostatica (pp), secondary bipartite internal seminal vesicle (sbisv), cirrus (c), initial bipartite internal seminal vesicle (ibisv), common genital pore (cgp), metraterm (m), vitellarium (vr), and vas deferens (vd).

Figs. 5–6

Paraharmotrema karinganiense Dutton & Bullard n. sp. (Digenea: Liolopidae) from intestine of serrated hinged terrapin, Pelusios sinuatus (Smith 1838) (Pleurodira: Pelomedusidae). (5) Ventral sucker, ventral view, scanning electron micrograph. (6) Ventral sucker, ventral view, light micrograph.

Figs. 7–9

Paraharmotrema karinganiense Dutton & Bullard n. sp. (Digenea: Liolopidae) from the intestine of the intestine of the serrated hinged terrapin, Pelusios sinuatus (Smith 1838) (Pleurodira: Pelomedusidae). (7) Tegumental scales in antero-dextral ventral body surface, ventral view, light micrograph. (8) Tegumental scales on ventral body surface posterior to oral sucker, ventral view, light micrograph. (9) Tegumental scales in same position as in Fig. 8 (showing exposed tips of scales only), ventral view, scanning electron micrograph.

Fig. 10

Large subunit ribosomal DNA (28S) Bayesian phylogeny. Values aside nodes are posterior probability. Scale bar is in substitutions per site. GenBank numbers in parentheses following each taxon.