First elucidation of a blood fluke (Electrovermis zappum n. gen., n. sp.) life cycle including a chondrichthyan or bivalve

Abstract

We describe a new fish blood fluke (Digenea: Aporocotylidae: Electrovermis zappum n. gen., n. sp.) and its life cycle in the intertidal zone adjacent to Mobile Bay (north-central Gulf of Mexico). This is the first elucidated aporocotylid life cycle that includes a chondrichthyan definitive host or a bivalve intermediate host. The new species undergoes asexual reproduction within the gonad of the variable coquina clam before maturing in the heart of the lesser electric ray. These adults and cercariae had identical 28S, 18S, and ITS2 nucleotide sequences. The new genus is similar to Ogawaia Cutmor et al., 2018 by having an inverse U-shaped intestine, a looping testis, and a uterus having distinct ascending and descending segments. It differs by having a body that is ≥ 30 × longer than wide, a testis with >30 curves, an obvious cirrus sac enveloping an extremely elongate cirrus, an ovary anterior to the seminal vesicle, and a post-gonadal uterus. The new species further differs from the type species of Ogawaia (Ogawaia glaucostegi Cutmore et al., 2018) by having a massive seminal vesicle (>10% of body length), a cirrus sac enveloping an extremely elongate cirrus, and a slightly sinuous uterus. Histology confirmed gametogenesis in an infected coquina clam but no discernible cellular response to infection was observed. We also i) characterize a second morphologically and genetically distinct cercaria (perhaps representing an innominate chondrichthyan aporocotylid) infecting the green jackknife clam in Mississippi Sound (north-central Gulf of Mexico), ii) compare all known aporocotylid cercariae infecting estuarine and marine mollusks and polychaetes and iii) provide a key to identify those cercariae. A phylogenetic analysis including nucleotide sequences from adult and cercarial specimens of the newly collected fish blood flukes further supports the notion that chondrichthyan aporocotylids are monophyletic and use bivalves as the first intermediate host; perhaps unlike any other blood fluke lineage.

Molecular data reshape our understanding of the life cycles of three digeneans (Monorchiidae and Gymnophallidae) infecting the bivalve, Donax variabilis: it’s just a facultative host!

“…In particular, D. variabilis Say, 1822 is common on the southeastern US Atlantic coast (south of Chesapeake Bay to mid-east Florida) and throughout the Gulf of Mexico from southwest Florida, USA to Campeche State, Mexico [ 2 , 66 ]. It has been reported as host to a variety of parasites [in 4 , 32 ] including several digenean larvae [ 29 , 30 , 38 , 62 , 63 ]. However, because these clams live in sympatry with congeneric cryptic species [ 1 , 2 ], such host reports are questionable.…”

Fish blood flukes (Digenea: Aporocotylidae) from Indonesia: Two new genera and species infecting the banded eagle ray, Aetomylaeus nichofii (Bloch and Schneider, 1801) Capapé and Desoutter, 1979 (Myliobatiformes: Myliobatidae) from Borneo

“…bulbosus and A . kirstenjensenae ) by the combination of having an aspinous, diminutive anterior sucker, an asymmetrical inverse U-shaped intestine, a curving testis, and a post-caecal common genital pore as well as by lacking any spine along the lateral tegument ( Madhavi and Hanumantha Rao, 1970 ; Bullard and Jensen, 2008 ; Cutmore et al, 2018 ; Warren and Bullard, 2019 ; Warren et al, 2020 ). It differs from M. richardheardi by the combination of having >30 testicular curves (vs. 9–10), a vas deferens that is >70% of the seminal vesicle length, a seminal vesicle that curves 6 times (vs. 9–10), and a uterus that extends anteriad beyond the level of the seminal vesicle (KEY) ( Bullard and Jensen, 2008 ).…”

“… Parasite Host Site of infection Locality Reference Aetohemecus kirstenjensenae n. sp., n. gen. banded eagle ray, Aetomylaeus nichofii (Bloch and Schneider, 1801) Capapé and Desoutter, 1979 heart Makassar Strait, (01°12′55.20″S, 116°58′27.50″E), off Manggar, East Kalimantan, Borneo, Indonesia present study Achorovermis testisinuosus Warren and Bullard, 2020 smalltooth sawfish, Pristis pectinata Latham, 1796 heart Eastern Gulf of Mexico, off Naples, Florida, USA Warren et al (2020) Chimaerohemecus trondheimensis Van der land, 1967 rabbit fish, Chimaera monstrosa Linnaeus, 1758 dorsal aorta NE Atlantic, off Bergen, Norway Van der Land (1967) ; Lockyer et al, 2003b spook fish, Hydrolagus mitsukurii (Jordan and Snyder, 1904) Nakaya, 1984 dorsal aorta and postcardinal vein around kidney Saruga Bay, Japan Kamegai et al, 2002 Electrovermis zappum Warren and Bullard, 2019 lesser electric ray, Narcine bancroftii (Griffith and Smith, 1834) Carvalho, 2001 heart Gulf of Mexico, off Fort Morgan, Alabama, USA Warren and Bullard (2019) Gymnurahemecus bulbosus Warren, Ruiz, Whelan, Kritsky, and Bullard, 2019 smooth butterfly ray, Gymnura micrura (Bloch and Schneider, 1801) Uyeno, 1983 heart Gulf of Mexico, off Mobile, Alabama, USA Warren et al (2019) Homestios janinecairae n. sp., n. gen. banded eagle ray, Aetomylaeus nichofii (Bloch and Schneider, 1801) Capapé and Desoutter, 1979 heart Java Sea, (03°52′28.00″S, 114°36′37.00″E), off Takisung, South Kalimantan, Borneo, Indonesia present study …”

“…The aporocotylids that infect chondrichthyans comprise 11 spp. of nine genera ( Table 1 ) and have large C-shaped tegumental spines (infecting sharks, a ray, and a chimaera) or lack spines (infecting batoids [except Gymnurahemecus bulbosus Warren, Ruiz, Whelan, Kritsky, and Bullard, 2019]) ( Short, 1954 ; Van der Land, 1967 ; Madhavi and Hanumantha Rao, 1970 ; Maillard and Ktari, 1978 ; Bullard et al, 2006 ; Bullard and Jensen, 2008 , Orélis-Ribeiro et al, 2013 ; Cutmore et al, 2018 ; Warren et al, 2019 , 2020 ; Warren and Bullard, 2019 ). Further, aporocotylids infecting batoids (except G. bulbosus ) have a curving testis ( Madhavi and Hanumantha Rao, 1970 ; Bullard and Jensen, 2008 ; Cutmore et al, 2018 ; Warren and Bullard, 2019 ; Warren et al, 2020 ).…”

“…Species of Plehniella infect the body cavity of catfishes, lack spines, and have a star-shaped intestine ( Truong and Bullard, 2013 ; Orélis-Ribeiro and Bullard, 2015 ). The current separation of these two morphologically distinct lineages of fish blood flukes is further represented in nucleotide-based phylogenetic studies using the large subunit of ribosomal DNA ( 28S rDNA ) ( Warren et al, 2019 ; Warren and Bullard, 2019 ).…”