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. 2020 Dec;147(14):1765-1773.
doi: 10.1017/S0031182020001729. Epub 2020 Sep 18.

Host-parasite relationships between seabirds and the haemadipsid leech Chtonobdella palmyrae (Annelida: Clitellata) inhabiting oceanic islands in the Pacific Ocean

Takafumi Nakano  1 , Hajime Suzuki  2   3 , Naoko Suzuki  2 , Yuichi Kimura  4 , Tatsuo Sato  5 , Hiromi Kamigaichi  6 , Naoki Tomita  7 , Takeshi Yamasaki  7
Affiliations

Host-parasite relationships between seabirds and the haemadipsid leech Chtonobdella palmyrae (Annelida: Clitellata) inhabiting oceanic islands in the Pacific Ocean

Takafumi Nakano et al. Parasitology. 2020 Dec.

Abstract

The duognathous haemadipsid leeches of the genus Chtonobdella show a trans-oceanic distribution throughout the Indo-Pacific region. Although passive long-distance dispersal (LDD) of Chtonobdella leeches by birds has been suggested, little is known about the host-parasite relationships between avian hosts and Chtonobdella leeches. In the current study, we investigated Chtonobdella leech infestations of the eyes and other mucus membranes of migratory procellariiform seabirds, Pterodroma hypoleuca and Oceanodroma tristrami, captured at six locations in the Bonin Islands, Honshu and Okinawa Island, Japan. Analyses of the partial sequences of 18S rRNA, 28S rRNA, and mitochondrial cytochrome c oxidase subunit I (COI) and morphological examination of the specimens demonstrated that the Chtonobdella leeches belonged to Chtonobdella palmyrae, which is indigenous to Palmyra Atoll in the Northern Line Islands. A dominant COI sequence type was observed in samples from all six sites; therefore, C. palmyrae almost surely dispersed approximately 1000 km by infesting the eyes and mucus membranes of procellariiform seabirds. The host-parasite relationships between procellariiform seabirds and C. palmyrae provide explicit evidence of the LDD of duognathous haemadipsid leeches. The taxonomic status of Haemadipsa zeylanica ivosimae from the Volcano Islands is also briefly discussed.

Keywords: Avian host; Haemadipsidae; Hirudiniformes; blood-feeding; migration; overseas dispersal.

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Conflict of interest statement

None.

Figures

Fig. 1.
Fig. 1.
Map showing sampling localities for Chtonobdella palmyrae (Richardson) infesting seabirds from Japan; the white star denotes the type locality of the species.
Fig. 2.
Fig. 2.
Heavy infestation of C. palmyrae (Richardson) in the eyes of a petrel, Oceanodroma tristrami Salvin (KUZ B491), from Anijima Island, Bonin Islands; arrow heads indicate respective leeches.
Fig. 3.
Fig. 3.
Molecular phylogenetic position and haplotype networks of C. palmyrae (Richardson) infesting seabirds in Japan. (A) BI tree for 5172 bp alignment positions of nuclear 18S rRNA, 28S rRNA and mitochondrial COI markers; numbers on nodes indicate bootstrap values for ML and Bayesian PPs. Statistical parsimony networks of (B) the 985 bp COI haplotypes of Japanese (Jpn) leeches and C. palmyrae from Palmyra Atoll, and (C) the 1271 bp COI haplotypes only between the Japanese leeches; filled circles indicate missing haplotypes; each numeral in parentheses denotes the sample size of the respective haplotype.
Fig. 4.
Fig. 4.
Preserved specimen of C. palmyrae (Richardson) (KUZ Z1636) infesting O. tristrami Salvin (KUZ B491) from Anijima Island, Bonin Islands: (A) dorsal and (B) ventral views. Scale bar: 2 mm.
Fig. 5.
Fig. 5.
Drawings of C. palmyrae (Richardson) (KUZ Z1636) infesting O. tristrami Salvin (KUZ B491) from Anijima Island, Bonin Islands. (A) Dorsal, (B) lateral and (C) ventral views of somites I–X, (D) ventral view of somites XI and XII, (E) dorsal, (F) lateral and (G) ventral views of somites XXI–XXVII and caudal sucker and (H) dorsal view of median reproductive systems, including positions of ganglia XI–XIII. at, atrium; fg, female gonopore; fr, friction ray; mg, male gonopore; np, nephridiopore; phl, prehensile lobe; ra, respiratory auricle; vd, vaginal duct; and vs, vaginal sac. Scale bars: (A–G) 0.5 mm and (H) 0.1 mm.
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