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Acipensericola glacialis n. sp. (Digenea: Aporocotylidae) from heart of lake sturgeon Acipenser fulvescens Rafinesque (Acipenseriformes: Acipenseridae) in the Great Lakes Basin, Lake Winnebago System, USA

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Brett Warren at Auburn University
Brett Warren
Jackson Roberts at Louisiana State University
Jackson Roberts
Cova R Arias
Cova R Arias
Cova R Arias
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Ryan Koenigs at Wisconsin Department of Natural Resources
Ryan Koenigs
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Acipensericola glacialis n. sp. infects the heart of lake sturgeon, Acipenser fulvescens (Rafinesque), in the Lake Winnebago System and differs from its only congener, Acipensericola petersoni Bullard, Snyder, Jensen & Overstreet, 2008, by having a dendritic intestine, deeply-lobed testes, a post-ovarian oötype, and a common genital pore that is medial to the dextral caecum. Acipensericola petersoni has a non-dendritic intestine, testes that are not deeply lobed, an oötype that is at level of the ovary (ventral to the ovary), and a common genital pore that is dorsal to the dextral caecum. Comparison of the large (28S) and small (18S) sub-unit ribosomal DNA and internal transcribed spacer 2 (ITS2) regions between specimens of A. glacialis n. sp. and A. petersoni revealed 13 (of 1,621 nt; 99.2% similarity in the 28S), 8 (of 1,841 nt; 99.9% similarity in the 18S), and 11 (of 442 nt; 97.5% similarity in the ITS2) nucleotide differences. Collectively, these results comprise an unexpectedly high degree of morphological and molecular similarity given the geographical (Mississippi River Basin vs Great Lakes Basin) and phylogenetic (Polyodontidae vs Acipenseridae) separation of these hosts but seemingly did not reject a previous hypothesis concerning lake sturgeon dispersal from the Mississippi Refugium following the Wisconsin glaciation ~18,000 years ago. The new species is the first nominal blood fluke described from a sturgeon.
Acipensericola glacialis n. sp. ex heart of Acipenser fulvescens. Ventral view. A, Small adult specimen (paratype, USNM 1422364); B, Small adult specimen (paratype, USNM 1422365); C, Large adult specimen (holotype, USNM 1422361). Note that common genital pore is medial to dextral caecum; cirrus everted in illustration. Abbreviations: as, anterior sucker; cb, caecal bifurcation; ep, excretory pores, es, oesophagus; nc, nerve commissure; o, ovary; ph, pharynx; t1–t6, testes 1–6
Acipensericola glacialis n. sp. ex heart of Acipenser fulvescens. Ventral view. A, Small adult specimen (paratype, USNM 1422364); B, Small adult specimen (paratype, USNM 1422365); C, Large adult specimen (holotype, USNM 1422361). Note that common genital pore is medial to dextral caecum; cirrus everted in illustration. Abbreviations: as, anterior sucker; cb, caecal bifurcation; ep, excretory pores, es, oesophagus; nc, nerve commissure; o, ovary; ph, pharynx; t1–t6, testes 1–6
… 
Acipensericola glacialis n. sp. ex heart of Acipenser fulvescens. Ventral view. A, Small adult specimen (paratype, USNM 1422364); B, Small adult specimen (paratype, USNM 1422365); C, Large adult specimen (holotype, USNM 1422361). Abbreviations: ave, anterior trunk of vasa efferentia; ic, inverted cirrus; o, ovary; oo, oötype; ov, oviduct with sperm and serving as oviducal seminal receptacle; pve, posterior trunk of vasa efferentia; sv, seminal vesicle; t5, posteriormost testis of testicular column; t6, posteriormost testis, uterus; vd, vas deferens; vt, primary vitelline collecting duct
Acipensericola glacialis n. sp. ex heart of Acipenser fulvescens. Ventral view. A, Small adult specimen (paratype, USNM 1422364); B, Small adult specimen (paratype, USNM 1422365); C, Large adult specimen (holotype, USNM 1422361). Abbreviations: ave, anterior trunk of vasa efferentia; ic, inverted cirrus; o, ovary; oo, oötype; ov, oviduct with sperm and serving as oviducal seminal receptacle; pve, posterior trunk of vasa efferentia; sv, seminal vesicle; t5, posteriormost testis of testicular column; t6, posteriormost testis, uterus; vd, vas deferens; vt, primary vitelline collecting duct
… 
Acipensericola glacialis n. sp. ex heart of Acipenser fulvescens. Ventral view. A–C, Anterior sucker; A, Small adult specimen (paratype, USNM 1422364); B, Small adult specimen (paratype USNM 1422365); C, Large adult specimen (holotype, USNM 1422361); D, Genitalia surrounding oötype of large adult specimen (holotype, USNM 1422361). E–G, Ventrolateral transverse spine rows. E, Large adult specimen (holotype, USNM 1422361). F, Small adult specimen (paratype, USNM 1422364). G, Small adult specimen (paratype, USNM 1422365). Abbreviations: as, anterior sucker; ls, large spines; Mg, Mehlis’ gland; mo, mouth; oo, oötype; ov, oviduct; ph, pharynx; sv, seminal vesicle; u, proximal portion of uterus; vd, vas deferens; vt, vitelline duct
Acipensericola glacialis n. sp. ex heart of Acipenser fulvescens. Ventral view. A–C, Anterior sucker; A, Small adult specimen (paratype, USNM 1422364); B, Small adult specimen (paratype USNM 1422365); C, Large adult specimen (holotype, USNM 1422361); D, Genitalia surrounding oötype of large adult specimen (holotype, USNM 1422361). E–G, Ventrolateral transverse spine rows. E, Large adult specimen (holotype, USNM 1422361). F, Small adult specimen (paratype, USNM 1422364). G, Small adult specimen (paratype, USNM 1422365). Abbreviations: as, anterior sucker; ls, large spines; Mg, Mehlis’ gland; mo, mouth; oo, oötype; ov, oviduct; ph, pharynx; sv, seminal vesicle; u, proximal portion of uterus; vd, vas deferens; vt, vitelline duct
… 
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Acipensericola glacialis n. sp. (Digenea: Aporocotylidae)
from heart of lake sturgeon Acipenser fulvescens Rafinesque
(Acipenseriformes: Acipenseridae) in the Great Lakes
Basin, Lake Winnebago System, USA
Micah B. Warren .Jackson R. Roberts .Cova R. Arias .Ryan P. Koenigs .
Stephen A. Bullard
Received: 13 June 2017 / Accepted: 13 August 2017 / Published online: 8 September 2017
ÓSpringer Science+Business Media B.V. 2017
Abstract Acipensericola glacialis n. sp. infects the
heart of lake sturgeon, Acipenser fulvescens (Rafin-
esque), in the Lake Winnebago System and differs
from its only congener, Acipensericola petersoni
Bullard, Snyder, Jensen & Overstreet, 2008, by having
a dendritic intestine, deeply-lobed testes, a post-
ovarian oo
¨type, and a common genital pore that is
medial to the dextral caecum. Acipensericola peter-
soni has a non-dendritic intestine, testes that are not
deeply lobed, an oo
¨type that is at level of the ovary
(ventral to the ovary), and a common genital pore that
is dorsal to the dextral caecum. Comparison of the
large (28S) and small (18S) sub-unit ribosomal DNA
and internal transcribed spacer 2 (ITS2) regions
between specimens of A. glacialis n. sp. and A.
petersoni revealed 13 (of 1,621 nt; 99.2% similarity in
the 28S), 8 (of 1,841 nt; 99.9% similarity in the 18S),
and 11 (of 442 nt; 97.5% similarity in the ITS2)
nucleotide differences. Collectively, these results
comprise an unexpectedly high degree of morpholog-
ical and molecular similarity given the geographical
(Mississippi River Basin vs Great Lakes Basin) and
phylogenetic (Polyodontidae vs Acipenseridae) sepa-
ration of these hosts but seemingly did not reject a
previous hypothesis concerning lake sturgeon disper-
sal from the Mississippi Refugium following the
Wisconsin glaciation *18,000 years ago. The new
species is the first nominal blood fluke described from
a sturgeon.
Introduction
The monophyletic fish blood flukes (Aporocotylidae
Odhner, 1912) (Bullard et al., 2009; Ore
´lis-Ribeiro
et al., 2014) comprise approximately 150 accepted
species of 35 genera infecting freshwater, marine and
estuarine fishes (Bullard 2014; Nolan et al.,
2014,2016; Ogawa et al., 2015; Ore
´lis-Ribeiro &
Bullard, 2015,2016; Santoro et al., 2015; Yong et al.,
2016a,b;Ore
´lis-Ribeiro et al., 2017; Palacios-Abella
This article was registered in the Official Register of Zoological
Nomenclature (ZooBank) as 8BEC1BAB-FACD-42FD-942F-
6B5FD4C64046. This article was published as an Online First
article on the online publication date shown on this page. The
article should be cited by using the doi number. This is the
Version of Record.
This article is part of the Topical Collection Digenea.
M. B. Warren J. R. Roberts S. A. Bullard (&)
School of Fisheries, Aquaculture, & Aquatic Sciences and
Aquatic Parasitology Laboratory, Auburn University, 203
Swingle Hall, Auburn, AL 36849, USA
e-mail: ash.bullard@auburn.edu
C. R. Arias
School of Fisheries, Aquaculture, & Aquatic Sciences and
Aquatic Microbiology Laboratory, Auburn University,
559 Duvall Drive, Auburn, AL 36832, USA
R. P. Koenigs
Wisconsin Department of Natural Resources, 625 East
County Road Y, Suite 700, Oshkosh, WI 54901, USA
123
Syst Parasitol (2017) 94:875–889
DOI 10.1007/s11230-017-9751-3
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... The 28S was amplified using primers outlined in . PCR amplifications were performed with the cycling profile identified by Warren et al. (2017b), except that the annealing temperature was set at 56 C for 30 sec. PCR reactions were carried out in a MJ Research Hercules,California). PCR products (12 ll) were verified on a 1% agarose gel and stained with ethidium bromide. ...
... The other freshwater fish blood fluke genera (Acipensericola, Plehniella, monotypic Cladocecum, monotypic Kritsky) differ from Sanguinicola by features associated with the anterior sucker, lateral tegumental spines, intestine, and genitalia. Species of Acipensericola, which infect sturgeons and paddlefish (Appy and Dadswell, 1978;Bullard et al., 2008;Ore´lis-Ribeiro and Bullard, 2015;Warren et al., 2017b), differ from Sanguinicola by having a large, pedunculate, bowl-shaped anterior sucker, lateral tegumental spines in transverse rows, an inverse U-shaped intestine, and a testicular column with 6 testes (including a postgenital testis) (Bullard et al., 2008;Warren et al., 2017b). Plehniella, monotypic Cladocecum, and monotypic Krtisky comprise species that infect catfishes only (Ore´lis-Ribeiro and Bullard, 2015). ...
... The other freshwater fish blood fluke genera (Acipensericola, Plehniella, monotypic Cladocecum, monotypic Kritsky) differ from Sanguinicola by features associated with the anterior sucker, lateral tegumental spines, intestine, and genitalia. Species of Acipensericola, which infect sturgeons and paddlefish (Appy and Dadswell, 1978;Bullard et al., 2008;Ore´lis-Ribeiro and Bullard, 2015;Warren et al., 2017b), differ from Sanguinicola by having a large, pedunculate, bowl-shaped anterior sucker, lateral tegumental spines in transverse rows, an inverse U-shaped intestine, and a testicular column with 6 testes (including a postgenital testis) (Bullard et al., 2008;Warren et al., 2017b). Plehniella, monotypic Cladocecum, and monotypic Krtisky comprise species that infect catfishes only (Ore´lis-Ribeiro and Bullard, 2015). ...
Revision of Sanguinicola Plehn, 1905 with Redescription of Sanguinicola volgensis (Rašín, 1929) McIntosh, 1934, Description of a New Species, Proposal of a New Genus, and Phylogenetic Analysis
Article
  • Jul 2023
  • J Parasitol
Sanguinicola Plehn, 1905 comprises 26 species that collectively infect fishes from 8 orders (Cypriniformes, Characiformes, Siluriformes, Esociformes, Salmoniformes, Labriformes, Centrarchiformes, and Perciformes). Its revision is warranted because several species assigned to the genus could represent new genera, nucleotide sequences are wanting, many species have incomplete descriptions, and types for most species are missing or of poor quality. Herein, we emend Sanguinicola based on morphology and the first nucleotide-based phylogenetic analysis that includes multiple sequences from morphologically identified adult specimens. We describe Sanguinicola plehnae Warren and Bullard n. sp. from the heart of northern pike, Esox lucius Linnaeus, 1758 from Russia; provide supplemental observations of Sanguinicola volgensis (Rašín, 1929) McIntosh, 1934 from the heart of sabrefish (type species), Pelecus cultratus (Linnaeus, 1758) Berg, 1949 from Russia; describe Sanguinicola cf. volgensis from the heart of ide, Leuciscus idus (Linnaeus, 1758) Berg, 1949 from Russia; and describe Pseudosanguinicola occidentalis (Van Cleave and Mueller, 1932) Warren and Bullard n. gen., n. comb. from the heart of walleye, Sander vitreus (Mitchill, 1818) Bailey, Latta, and Smith, 2004 from eastern North America. Sanguinicola plehnae differs from its congeners by having lateral tegumental spines that total 118-122, are small (3% of body width), and protrude 2-3 µm from the tegument (lacking associated conical protrusion) as well as by having a large testis (>40% of body length). Sanguinicola volgensis differs from its congeners by having posteriorly directed lateral tegumental spines encased in a tegumental conical protrusion as well as by having an ovoid egg. Specimens of S. cf. volgensis differ from those of S. volgensis by having a body that is 5-6× longer than wide (vs. 2-3× in S. volgensis) and <90 lateral tegumental spines (vs. >95). Pseudosanguinicola Warren and Bullard n. gen. differs from Sanguinicola by having densely transverse rows of lateral tegumental spines (vs. a single column of large spines). The phylogenetic analysis utilizing the large subunit ribosomal DNA (28S) failed to reject monophyly of Sanguinicola.
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... This is the first recorded occurrence of this genus in North America and appears to be the first report of the genus in sturgeon since the description of Pristicola sturionis in 1930 [111]. Warren et al. (2017) [32] identified the trematoda Acipensericola glacialis in Acipenser fulvescens during a survey of the Great Lakes Basin, specifically the Lake Winnebago system in the USA. Acipensericola glacialis derives its name from the Latin-specific epithet "glacialis" (glacier). ...
... This is the first recorded occurrence of this genus in North America and appears to be the first report of the genus in sturgeon since the description of Pristicola sturionis in 1930 [111]. Warren et al. (2017) [32] identified the trematoda Acipensericola glacialis in Acipenser fulvescens during a survey of the Great Lakes Basin, specifically the Lake Winnebago system in the USA. Acipensericola glacialis derives its name from the Latin-specific epithet "glacialis" (glacier). ...
diversity Sturgeon Parasites: A Review of Their Diversity and Distribution
Article
Full-text available
  • Mar 2024
  • Diversity
Sturgeon species have inhabited the world's seas and rivers for more than 200 million years and hold significant taxonomic significance, representing a strong conservation interest in aquatic biodiversity as well as in the economic sector, as their meat and eggs (caviar) are highly valuable goods. Currently, sturgeon products and byproducts can be legally obtained from aquaculture as a sustainable source. Intensive farming practices are accompanied by parasitic infestations, while several groups of parasites have a significant impact on both wild and farmed sturgeons. The present article is a review of common sturgeon parasites from the genus: Protozoa, Trematoda,
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... The partial 28S rDNA fragment from most samples was amplified using the primers LSU5 (5 -TAG GTC GAC CCG CTG AAY TTA AGC A-3 ) (Littlewood, 1994) and 1500R (5 -GCT ATC CTG AGG GAA ACT TCG-3 ) (Snyder and Tkach, 2001) with internal primers 300F (5 -CAA GTA CCG TGA GGG AAA GTT G-3 ) (Littlewood et al., 2000) and ECD2 (5 -CCT TGG TCC GTG TTT CAA GAC GGG-3 ) (Littlewood et al., 1997). Polymerase chain reactions (PCRs) were performed using 50-μl samples mixed according to the protocols and methods of Warren et al. (2017) with annealing temperature set of 50°C for ITS2 and 56°C for 28S rDNA. PCR products were verified and purified following protocols of Warren et al. (2017). ...
... Polymerase chain reactions (PCRs) were performed using 50-μl samples mixed according to the protocols and methods of Warren et al. (2017) with annealing temperature set of 50°C for ITS2 and 56°C for 28S rDNA. PCR products were verified and purified following protocols of Warren et al. (2017). DNA sequencing was performed by GENEWIZ (South Plainfield, New Jersey, U.S.A.). ...
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... Two EtOH-preserved and microscopically identified fish blood flukes were used for DNA extraction and sequencing. DNA extraction, primers used, PCR amplification, sequencing, sequence assembly and analysis follow that of Warren et al. [6,12,13,25]. The phylogenetic analyses included the new freshwater fish blood fluke sequence and selected sequences representing species of sanguinicolids that were available on GenBank (Warren et al. [6]; Warren and Bullard [9]). ...
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... Whereas many adult digeneans have an obvious oral sucker and pharynx visible with conventional light microscopy (LM) of properly collected (heat-killed and formalin-fixed), stained, and whole-mounted specimens, the fish blood flukes (Aporocotylidae Odhner, 1912) collectively exhibit some morphological diversity in the presence/absence and appearance of those features. Some genera comprise species that have a large, bowl-shaped anterior sucker (''oral sucker'') as well as an obvious, strongly muscular pharynx in the foregut, e.g., Elopicola Bullard, 2014 andAcipensericola Bullard, Snyder, Jensen, and (see Bullard, 2014;Ore´lis-Ribeiro et al., 2014Warren et al., 2017). Other genera comprise species that have no apparent sucker adorning the mouth nor a pharynx discernible with light microscopy, e.g., Sanguinicola Plehn, 1905(see Plehn, 1905Smith, 2002;. ...
Foregut Ultrastructure of Adult Sanguinicola volgensis (RAŠÍn, 1929) Mcintosh, 1934 (Digenea: Aporocotylidae)
Article
  • Feb 2023
  • J Parasitol
Herein, we use scanning and transmission electron microscopy to describe the foregut (mouth, pharyngeal canal, and associated epithelia and musculature) of an adult freshwater fish blood fluke, Sanguinicola volgensis (Rašín, 1929) McIntosh, 1934, infecting the blood of sabre, Pelecus cultratus Linnaeus, 1758 (Cypriniformes: Leuciscidae) from the Volga River, Russia. Our results indicate that S. volgensis has a pharynx and lacks an oral sucker and that its pharyngeal canal acts as a peristaltic pump that sucks blood into the esophagus, whereupon digestion commences with granules secreted from the esophageal epithelium. We saw no evidence of longitudinal muscle fibers beneath the pharyngeal canal epithelium, pharyngeal glands, or pharyngeal epithelial cells or muscle cells within the pharyngeal muscular complex; collectively indicating the presence of a pharynx rather than an oral sucker. The specialized epithelial lining associated with the mouth and pharyngeal canal evidently is unique among neodermatans; it is smooth, ∼40 nm thick anteriorly, and thickens (∼250-700 nm) posteriorly as the mouth cavity transitions into the pharyngeal canal. The pharyngeal canal epithelium has lumps of dense material resembling those of the basal lamina and fibrous coat of the tegument. The actin-like material within the pharyngeal cavity epithelium could provide structural support to the pharynx.
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... Lineages IV and VI are both minor in terms of number of taxa, each comprising only two known species. Lineage IV, species of Acipensericola , are only known from acipenseriform fishes of North America Warren et al., 2017). Nothing is known of their intermediate hosts or larval morphology. ...
Evidence that a lineage of teleost-infecting blood flukes (Aporocotylidae) infects bivalves as intermediate hosts
Article
  • Oct 2022
  • Int J Parasitol
The family Aporocotylidae is recognized as having the widest intermediate host usage in the Digenea. Currently, intermediate host groups are clearly correlated with definitive host groups; all known life cycles of marine teleost-infecting aporocotylids involve polychaetes, those of freshwater teleost-infecting aporocotylids involve gastropods, and those of chondrichthyan-infecting aporocotylids involve bivalves. Here we report the life cycle for a marine elopomorph-infecting species, Elopicola bristowi Orélis-Ribeiro & Bullard in Orélis-Ribeiro, Halanych, Dang, Bakenhaster, Arias & Bullard, 2017, as infecting a bivalve, Anadara trapezia (Deshayes) (Arcidae), as the intermediate host in Moreton Bay, Queensland, Australia. The cercaria of E. bristowi has a prominent fin-fold, distinct anterior and posterior widenings of the oesophagus, a tail with symmetrical furcae with fin-folds, and develops in elongate to oval sporocysts. We also report molecular data for an unmatched aporocotylid cercaria from another bivalve, Megapitaria squalida (G. B. Sowerby I) (Veneridae), from the Gulf of California, Mexico, and six unmatched cercariae from a gastropod, Posticobia brazieri (E. A. Smith) (Tateidae), from freshwater systems of south-east Queensland, Australia. Phylogenetic analyses demonstrate the presence of six strongly-supported lineages within the Aporocotylidae, including one of elopomorph-infecting genera, Elopicola Bullard, 2014 and Paracardicoloides Martin, 1974, now shown to use both gastropods and bivalves as intermediate hosts. Of a likely 14 aporocotylid species reported from bivalves, six are now genetically characterised. The cercarial morphology of these six species demonstrates a clear distinction between those that infect chondrichthyans and those that infect elopomorphs; chondrichthyan-infecting aporocotylids have cercariae with asymmetrical furcae that lack fin-folds and develop in spherical sporocysts whereas those of elopomorph-infecting aporocotylids have symmetrical furcae with fin-folds and develop in elongate sporocysts. This morphological correlation allows predictions of the host-based lineage to which the unsequenced species belong. The Aporocotylidae is proving exceptional in is propensity for major switches in intermediate host use, with the most parsimonious interpretation of intermediate host distribution implying a minimum of three host switches within the family.
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Systematic Revision of the Fish Blood Flukes with Diagnoses of Chimaerohemecidae Yamaguti, 1971, Acipensericolidae N. Fam., Sanguinicolidae Poche, 1926, Elopicolidae N. Fam., and Aporocotylidae Odhner, 1912
Article
  • Aug 2023
  • J Parasitol
We herein morphologically diagnose the 5 natural groups of fish blood flukes and name them. Species of Chimaerohemecidae Yamaguti, 1971 infect chimeras, sharks, and rays (Chondrichthyes) and have C-shaped lateral tegumental spines and a non-sinusoidal testis or lack spines and have a sinusoidal testis. Species of Acipensericolidae n. fam. infect sturgeons and paddlefish (Acipenseriformes) and have a robust, bowl-shaped, pedunculate anterior sucker, lateral tegumental spines that are spike-like (not C shaped), an inverse U-shaped intestine (anterior ceca absent) with posterior ceca terminating near the excretory bladder, 6 testes (inter-cecal ovoid or oblong, lacking deep lobes; including 1 post-ovarian testis), a Laurer's canal, and a dextral common genital pore. Species of Sanguinicolidae Poche, 1926 infect primarily later-branching freshwater ray-finned fishes (Teleostei) and have a diminutive anterior sucker, a medial esophageal swelling (pouch), short, radial ceca of approximately equal length or short anterior ceca plus an elongate, dendritic posterior cecum, testis with appendix-like lateral lobes, no Laurer's canal, and separate or common genital pores. Species of Elopicolidae n. fam. infect ladyfishes, tarpons, and catadromous eels (Elopomorpha) and have a robust, bowl-shaped, pedunculate anterior sucker, lateral tegumental spines that are spike-like (can be lost in adult), short or indistinct anterior ceca, posterior ceca that terminate at level of the testis(es), a single testis or 2 testes, a Laurer's canal present or absent, and a sinistral common genital pore and atrium. Species of Aporocotylidae Odhner, 1912 primarily infect later-branching marine and estuarine ray-finned fishes (Teleostei) and have a spheroid anterior sucker with concentric rows of circumferential spines or the spheroid anterior sucker is lost in adults or adults have a diminutive anterior sucker, a sinuous esophagus lacking a pouch, an X- or H-shaped intestine having 4 ceca, long anterior ceca (or secondarily lost), smooth posterior ceca that extend posteriad in parallel with respective body margin and terminate near the posterior body end, testis(es) that lack appendix-like lateral lobes, no Laurer's canal, and a sinistral common genital pore or separate genital pores that are sinistral. Our 28S phylogeny recovered the fish blood flukes as monophyletic and each of the morphologically diagnosed families as monophyletic and sister to the remaining blood flukes infecting turtles and homeotherms. Acipensericolidae was recovered sister to the clade comprising Chimaerohemecidae + Sanguinicolidae and Elopicolidae + Aporocotylidae. The branching order and interrelationships of these families remains unsettled perhaps because of low taxon sampling among non-aporocotylids and extinction of intermediate taxa.
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New collections of blood flukes (Aporocotylidae) from fishes of the tropical Indo-west Pacific, including a new genus, two new species and molecular evidence that Elaphrobates chaetodontis (Yamaguti, 1970) is widespread in the region
Article
  • Feb 2022
  • Parasitol Int
We report new collections of the Aporocotylidae from Australia, French Polynesia, and Japan. A new species of Cardicola Short, 1953 is described from Scomberomorus commerson (Lacépède) (Scombridae), off Lizard Island. Cardicola nolani n. sp. can be distinguished from its congeners based on the position of the oötype, the position of the male genital pore, and the absence of an oral sucker. A new species is described from Abalistes stellatus (Anonymous) (Balistidae), also from off Lizard Island. Phylogenetically the new species forms a strongly-supported clade with Cardicola yuelao Yong, Cutmore & Cribb, 2018, which also infects balistids. These two species are distinct from all other aporocotylids in the combination of exceptionally short anterior and long posterior caeca, a lanceolate body, a single testis, an entirely post-ovarian uterus and the position of the oötype; a new genus, Balistidicola, is proposed for them. Balistidicola corneri n. sp. and B. yuelao (Yong, Cutmore & Cribb, 2018) n. comb. are essentially morphologically cryptic, only distinguishable by the form of the spination (B. corneri has five spines per row and B. yuelao has six). Elaphrobates chaetodontis (Yamaguti, 1970) is reported from 21 species of butterflyfishes (Chaetodontidae) from nine locations in tropical Indo-west Pacific; cox1 sequence data demonstrate extensive geographical structuring in this species. Braya jexi Nolan & Cribb, 2006, Elaphrobates milleri (Nolan & Cribb, 2006), and P. corventum Overstreet & Køie, 1989 are each re-reported from their type-hosts, and Pearsonellum pygmaeus Nolan & Cribb, 2004 and Balistidicola yuelao are each reported from a new host.
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A new order of fishes as hosts of blood flukes (Aporocotylidae); description of a new genus and three new species infecting squirrelfishes (Holocentriformes, Holocentridae) on the Great Barrier Reef
Article
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  • Jan 2021
  • Parasite
A new genus and three new species of blood flukes (Aporocotylidae) are described from squirrelfishes (Holocentridae) from the Great Barrier Reef. Holocentricola rufus n. gen., n. sp. is described from Sargocentron rubrum (Forsskål), from off Heron Island, southern Great Barrier Reef, and Lizard Island, northern Great Barrier Reef, Australia. Holocentricola exilis n. sp. and Holocentricola coronatus n. sp. are described from off Lizard Island, H. exilis from Neoniphon sammara (Forsskål) and H. coronatus from Sargocentron diadema (Lacepède). Species of the new genus are distinct from those of all other aporocotylid genera in having a retort-shaped cirrus-sac with a distinct thickening at a marginal male genital pore. The new genus is further distinct in the combination of a lanceolate body, X-shaped caeca, posterior caeca that are longer than anterior caeca, a single, post-caecal testis that is not deeply lobed, a post-caecal, post-testis ovary that is not distinctly bi-lobed, and a post-ovarian uterus. The three new species can be morphologically delineated based on the size and row structure of the marginal spines, as well by total length, oesophagus and caecal lengths, and the position of the male genital pore, testes and ovary relative to the posterior extremity. The three species of Holocentricola are genetically distinct from each other based on cox 1 mtDNA and ITS2 rDNA data, and in phylogenetic analyses of 28S rDNA form a well-supported clade sister to species of Neoparacardicola Yamaguti, 1970. This is the first report of aporocotylids from fishes of the family Holocentridae and the order Holocentriformes.
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Freshwater Trematodes Sanguinicola (Digenea: Aporocotylidae) in Europe: Distribution, Host Range, and Characteristics of Fish and Snail Infestation (Review)
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Full-text available
  • May 2021
Data on trematode life cycles, fish host distribution, transmission, and fish and snail infection are reported in this review. European freshwater trematodes of the genus Sanguinicola (Aporocotylidae) remain an insufficiently studied group of trematodes. Five species of Aporocotylidae ( Sanguinicola armata , S. inermis , S. intermedia , S. volgensis , and S. rutili ) in freshwater fish of Europe are described. In addition, they have been found in the water bodies of Central Asia and West Siberia (Ob-Irtysh River basin). The life cycle allowing us to assign the cercariae and adults to a certain species is known only for S. armata , S. inermis , and S. rutili . Trematodes of the genus Sanguinicola are found in 26 fish species assigned to 7 families and 4 orders and 24 gastropod species assigned to 7 families. With few exceptions, the sanguinicolid infection of fish and snails is rather low in the natural water bodies.
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A Field Guide for the Identification of Stages of Gonad Development in Lake Sturgeon (Acipenser fulvescens Rafinesque) With Notes on Lake Sturgeon Reproductive Biology and Management Implications
Technical Report
Full-text available
  • Jan 2001
This technical report aims to provide a pictorial color field guide for sex and stage of gonadal development of lake sturgeon. In addition, it describes the spawning characteristics of lake sturgeon and discusses the role of the reproductive biology of lake sturgeon in its management.
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Skoulekia erythrini n. sp. (Digenea: Aporocotylidae): a parasite of Pagellus erythrinus (L.) (Perciformes: Sparidae) from the western Mediterranean with an amendment of the generic diagnosis
Article
Full-text available
  • Jul 2017
  • Syst Parasitol
A new aporocotylid, Skoulekia erythrini n. sp., is described from the heart, cephalic kidney and gill blood vessels of the common pandora Pagellus erythrinus (L.) collected from several localities of the western Mediterranean off Spain. The new species differs from the type- and only species of the genus, S. meningialis Alama-Bermejo, Montero, Raga & Holzer, 2011 in possessing a symmetrical body (vs laterally curved), short tegumental spines (3-4 vs 7-10 µm) without hooked ends, diffuse (vs conspicuous) oesophageal gland-cells, a relatively longer oesophagus, a testis that is shorter in relation to body length and a much smaller seminal vesicle (17-34 × 10-26 vs 33-101 × 27-97 μm). Elongated ellipsoidal eggs of S. erythrini n. sp. were found trapped in gill vessels in histological sections. Phylogenetic analyses based on partial 28S rDNA and ITS2 sequences supported the placement of the new species within Skoulekia and the close relationships of this genus with Psettarium Goto & Ozaki, 1929 and Pearsonellum Overstreet & Køie, 1986. Skoulekia meningialis is described from a new sparid host, Diplodus puntazzo (Walbaum), collected off Santa Pola, Spain. The new morphological data for the two Skoulekia spp. and a re-examination of three paratypes of S. meningialis pinpointed features amending both the description of S. meningialis and the generic diagnosis of Skoulekia.
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A new species of Spirorchis MacCallum, 1918 (Digenea: Schistosomatoidea) and Spirorchis cf. scripta from chicken turtle, Deirochelys reticularia (Emydidae), with an emendation and molecular phylogeny of Spirorchis
Article
Full-text available
  • Dec 2016
Chicken turtles, Deirochelys reticularia (Latreille in Sonnini et Latreille) (Testudines: Emydidae) from Alabama, USA were infected by Spirorchis collinsi Roberts et Bullard sp. n. and Spirorchis cf. scripta. The new species is most easily differentiated from its congeners by the combination of having caeca that extend far beyond the genitalia, intercaecal genitalia positioned in the middle portion of the body, a testicular column that nearly abuts the caecal bifurcation, a cirrus sac positioned between the testes and ovary, a massive Mehlis' gland, an elongate, longitudinal metraterm that extends anteriad beyond the level of the ovary, a pre-ovarian genital pore, and a prominent, intercaecal Manter's organ. The specimens of S. cf. scripta differed from the holotype and published descriptions of Spirorchis scripta Stunkard, 1923 by several subtle morphological features, perhaps comprising intraspecific variation, but collectively warranted a detailed description herein. Based on examinations of the aforementioned specimens plus the holotype, paratypes and vouchers of morphologically-similar congeners, Spirorchis MacCallum, 1918 is emended to include the presence of oral sucker spines, a pharynx, lateral oesophageal diverticula ('plicate organ') and a median oesophageal diverticulum ('oeseophageal pouch'). Phylogenetic analysis of the nuclear large subunit rDNA (28S) recovered S. collinsi sister to Spirorchis picta Stunkard, 1923, > 99% similarity between S. cf. scripta and S. scripta, and a monophyletic Spirorchis MacCallum, 1918. No blood fluke infection has been reported previously from these drainages, Alabama, or this turtle species. This is the first new species of Spirorchis to be described from North America in 26 years.
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A complex of Cardicola Short, 1953 (Digenea: Aporocotylidae) species infecting the milkfish Chanos chanos Forsskål (Gonorynchiformes), with descriptions of two new species
Article
Full-text available
  • Nov 2016
  • Syst Parasitol
Two new species of Cardicola Short, 1953 are described from the milkfish, Chanos chanos Forsskål (Gonorynchiformes: Chanidae), obtained from off Lizard Island on the northern Great Barrier Reef (GBR) and North Stradbroke Island in southeast Queensland. These are the first known blood flukes from this order of fishes. Cardicola suni n. sp. differs from all other Cardicola spp. by a combination of a large ovoid oral sucker surrounding a subterminal mouth, recurved tegumental spines up to 16 μm long, anterior caeca occupying 25.1–31.3% (28.7%) of total body length and a mostly-intercaecal ovary. Cardicola jiigurru n. sp. differs from C. suni n. sp. and all other species of Cardicola by a combination of a narrowly lanceolate body, weakly-muscularised and poorly-demarcated oral sucker, minute tegumental spines <1 µm in length, and anterior caeca occupying 15.9–22.0% (19.4%) of total body length, an almost entirely post-caecal ovary and the male genital pore terminal on a dorsolateral protuberance. A third species, closely resembling C. suni n. sp., was also discovered off Wangetti Beach, north Queensland, but is not described due to lack of material. Molecular phylogenetic analysis, based on both ITS2 and partial 28S rDNA regions, shows that these three species form a clade nested within that formed by existing species of Cardicola.
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Catalog of Fishes: Genera, Species, References
Book
Full-text available
  • Apr 2016
The Catalog of Fishes covers more than 61,700 species and subspecies, over 11,000 genera and subgenera, and includes in excess of 34,000 bibliographic references. Entries for species, for example, consist of species/subspecies name, genus, author, date, publication, pages, figures, type locality, location of type specimen(s), current status (with references), family/subfamily, and important publication, taxonomic, or nomenclatural notes. Nearly all original descriptions have been examined, and much effort has gone into determining the location of type specimens. Online version: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp
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Two new species of Elopicola (Digenea: Aporocotylidae) from Hawaiian ladyfish, Elops hawaiensis (Eastern Sea) and Atlantic tarpon, Megalops atlanticus (Gulf of Mexico) with a comment on monophyly of elopomorph blood flukes
Article
  • Mar 2017
Elopicola bristowi sp. n. infects the blood vascular system of Hawaiian ladyfish, Elops hawaiensis, in the Eastern Sea. It differs from the only nominal congener Elopicola nolancribbi by the combination of having rows of ventrolateral tegumental spines, a proportionally long oesophagus, anterior caeca, vasa efferentia coalescing ventral to the posterodextral margin of the testis, a post-testicular metraterm, a dextral common genital pore lateral to the oötype, and genitalia that are enantiomorphic relative to those of E. nolancribbi. Elopicola franksi sp. n. infects the heart and blood vascular system of Atlantic tarpon, Megalops atlanticus, in the Gulf of Mexico. It differs from its congeners by the combination of lacking ventrolateral tegumental spines and having an elongate body (6 × longer than wide), a proportionally long oesophagus, a compact testis at level of the distal ends of the posterior caeca, and a post-testicular common genital pore at level of the oötype. Phylogenetic analyses based on the small subunit ribosomal DNA (18S), large subunit ribosomal DNA (28S), and internal transcribed spacer 2 (ITS2) genes revealed considerable genetic differences between these taxa. The 18S + 28S tree showed a monophyletic Elopicola sister to all aporocotylids infecting fishes of Euteleosteomorpha. The ITS2 tree showed Paracardicoloides yamagutii as the sister taxon to Elopicola spp.
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High-intensity cardiac infections of Phthinomita heinigerae n. sp. (Digenea: Aporocotylidae) in the orangelined cardinalfish, Taeniamia fucata (Cantor), off Heron Island on the Great Barrier Reef
Article
  • May 2016
We report a new species of aporocotylid trematode (Platyhelminthes: Digenea) from the heart of the orangelined cardinalfish, Taeniamia fucata (Cantor), from off Heron Island on the southern Great Barrier Reef. We used an integrated approach, analysing host distribution, morphology, and genetic data from the internal transcribed spacer 2 of the ribosomal DNA, to circumscribe Phthinomita heinigerae n. sp. This is the first species of Phthinomita Nolan & Cribb, 2006 reported from the Apogonidae; existing species and known ‘types’ are recorded from species of the Labridae, Mullidae, and Siganidae. The new species is distinguished from its 11 congeners in having a body 2977–3539 long and 16.5–22.4 times longer than wide, an anterior testis 6.2–8.2 times longer than wide and 8.3– 13.0 times longer than the posterior testis, a posterior testis whose width is 35–56% of the body width, and an ovary positioned 11–13% of the body length from the posterior end, and is entirely anterior to the posterior margin of the anterior testis. In addition, 2–34 base differences (0.4–7.0% sequence divergence over 485 base positions) were detected among the ITS2 sequence representing P. heinigerae n. sp. and the 14 representing other Phthinomita species/molecular types. Prevalence and intensity of infection with P. heinigerae n. sp. was relatively high within the heart tissue of T. fucata, with 19 of 20 fish examined from off Heron Island infected (95%) with 7– 25 adult worms (arithmetic mean 16.6). Infections by these parasites accounted for an occupation of 7–30% of the total estimated heart volume.
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Three new species of blood flukes (Digenea: Aporocotylidae) infecting pufferfishes (Teleostei: Tetraodontidae) from off Bali, Indonesia
Article
  • May 2016
We describe three new species of blood flukes (Aporocotylidae) and propose their classification within the genus Psettarium Goto & Ozaki, 1929. All three species were collected from the circulatory systems of pufferfishes caught off Bali, central Indonesia. Psettarium pulchellum n. sp. was found in the gills of both the narrow-lined puffer (Arothron manilensis de Proce) and the spiny blaasop (Tylerius spinosissimus Regan), while P. ogawai n. sp. and P. jimbaranense n. sp. were found in the gills of the reticulated puffer (Arothron reticularis Bloch & Schneider). The morphological characteristics of these taxa necessitated emendation of the diagnosis for the genus Psettarium, to accommodate the presence of an oral sucker, multiple or entirely post-caecal testes and a degenerate posterior testis. Features such as proportion of body length occupied by the oesophagus, and posterior caeca being ≥ 7 × the length of anterior caeca, are no longer regarded as useful genus-level characters. Additionally, Sasala nolani is reassigned to this genus as Psettarium nolani n. comb. In phylogenetic analyses of the 28S and ITS2 rDNA regions, all three new taxa form a well-supported clade, together with Psettarium sinense and Psettarium nolani n. comb., the two other species of tetraodontid-infecting aporocotylids for which comparative rDNA data were available. The short branch lengths within this clade, despite dramatic morphological differences between the five species, suggest that rapid morphological diversification has occurred among the tetraodontid-infecting aporocotylids. The genus Psettarium has long been considered problematic. Further commentary is given on the history of this genus and how the issues presented might be resolved.
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