Revision of  Johnston, 1937 (Acanthocephala: Polymorphidae) from a North American population using novel SEM images, Energy Dispersive X-ray Analysis, and molecular analysis

O. M. Amin; A. Chaudhary; H. S. Singh; T. Kuzmina

Detalles de publicación y publicación

Helminthologia

Detalles de la revista

Formato: Revista
eISSN: 1336-9083
Primera edición: 22 Apr 2006
Calendario de la edición: 4 veces al año
Idiomas: Inglés

The taxonomic literature of species of the genus Corynosoma Lühe, 1904 has been in flux, especially over the last few years with the erection of the genus Pseudocorynosoma Aznar, Pérez-Ponce de León and Raga, 2006 for freshwater species formerly classified under Corynosoma (Aznar et al., 2006; García-Varela et al., 2009; Amin, 2013). The history of Corynosoma australe, Johnston, 1937 originally described from an Australian sea lion Neophoca cinerea (Péron, 1816) with a host listing of the Australian hair seal Arctocephalus forsteri Lesson (Otariidae) off Pearson Island, South Australia, is less complex with its junior synonym Corynosoma obtuscens Lincicome, 1943 being redescribed from the California sea lion Zalophus californianus (Lesson, 1828) in California. Corynosoma otariae Morini and Boero, 1958 from the South American sea lion, Otaria flavescens Shaw, 1800 in Argentina is also considered a junior synonym of C. australe. Various reports have since used the two names alternatively with C. australe being more commonly reported from the Southern Hemisphere and the junior synonym C. obtuscens used along the Pacific coasts of North and South America (Van Cleave, 1953; Zdzitowiecki, 1984; Aznar et al., 2012; Lisitsyna et al., 2019). The confusion between these two entities was evident throughout the literature but the similarities were first noted by Johnston and Edmonds (1953) and later by Zdzitowiecki (1984). The differential distribution of ventral trunk spines in females was the primary distinguishing factor between the two species. More recently, Aznar et al. (2016) provided a scanning electron microscopy (SEM) study of trunk spine coverage in 6 species of Corynosoma from 5 species of marine mammals off Argentina including C. australe (N=10) from the South American sea lion, O. flavescens. Hernández-Orts et al. (2017a) reported on host switching in C. australe from Brazil, provided 4 SEM images of a male and female and their posterior trunk ends collected from the Magellanic penguin, Spheniscus magellanicus Forster 1781, and included Bayesian inference phylograms from 28SrRNA and cox1 data sets. Some SEM images, dissimilar Energy Dispersive x-ray analysis (EDXA) from a different population of C. australe from the Cape fur seal, Arctocephalus pusillus pusillus (Schreber, 1775) off the Namibian coast, South Africa were provided by Halajian et al. (2020).

We have studied many species of acanthocephalans using X-ray scans (EDXA) of Focused Ion Beam (FIB)-sectioned hooks and spines for metal composition. The biological significance of EDXA as a diagnostic tool is exemplified by the observation that populations of acanthocephalan species will consistently have similar EDXA spectra irrespective of host species or geography (Amin et al., 2022d). Results of the EDXA of the FIB-sectioned hooks (dual beam SEM) of C. australe show differential composition and distribution of metals in different hook parts characteristic of the species being examined.

A chronological history of the taxonomy of C. australe is listed in Table 1 emphasizing the variations in the distribution of ventral trunk spines in females. The present report and especially some SEM images explain, in part, the different interpretations of trunk spine distribution in females. The EDXA provides additional diagnostic support of the identity of C. australe. Previous studies showed that species delineation within the genus Corynosoma has been problematic for a long time (Sardella et al., 2005; Hernández-Orts et al., 2017a). Additionally, Stryukov (2004) also pointed out that heteropolar geographical distribution can be represented by the species that are similar in their morphology. Therefore, we carried out phylogenetic analyses using newly generated sequences of 18S ribosomal RNA and the mitochondrial cytochrome c oxidase subunit 1 (Cox1) gene that provide insights of the relationships of C. australe studied at the generic level and about their heteropolar geographical distribution.

Table 1.

Chronological taxonomic history of Corynosoma australe from marine mammals, with special reference to ventral trunk spines in females.

Author	Host	Locality	Described as	Stage	Ventral spines
Johnston (1937)	Neophoca cinerea (Péron)	South Australia	C. australe	Adults	Discontinuous
Lincicome (1943)	Zalophus californianis (Lesson)	San Diego, California	C. obtuscens	Adults	Continuous
Van Cleave (1953)	Mycteroperca pardalis Gilbert	Mazatalán, Mexico	C. obtuscens	Cystacanth	Continuous
Morini & Boero (1960)	Otaria flavescence Shaw	Argentina	C. otariae	Adults	Discontinuous
Zdzitowiecki (1984)	Hydrurga leptonyx (Blainville)	South Shetlands, Antarctica	C. australe	Adults	25% continuous
Smales (1986)	Neophoca cinerea (Péron)Arctocephalus pusillatus Schreber	South Australia	C. australe	Adults (Figs. 10,11)	Discontinuous
Zdzitowiecki (1991)	Few “suitable” definitive & paratenic hosts	Antarctica	C. australe	Adults (Figs. 15 b, e)	Discontinuous
Sardella et al. (2005)	Arctocephalus australis (Zimmerman)Mirounga leonina (Linn.)Cynoscion guatucupa (Cuvier)	Argentina	C. australeC. australeC. australe	AdultsAdultsCystacanths	85–100% continuous85–100% continuous85–89% continuous
Aznar et al. (2012)	Otaria flavescens (Shaw)	Argentina	C. australe	Adults (Fig. 1B)	Discontinuous
Hernández-Orts et al. (2017a)	Spheniscus magellanicus (Foster)	Brazil	C. australe	Adults (Fig. 2B)Adults (Fig. 4B)	Continuous & 82–89% continuous
Lisitsyna et al. (2018)	Zalophus californianus (Lesson)	SausalitoCalifornia	C. obtuscens	Adults	Continuous
Lisitsyna et al. (2019)	Zalophus californianus (Lesson)	SausalitoCalifornia	C. obtuscens & C. australe	Adults	1% discontinuous
Present paper	Zalophus californianus (Lesson)	SausalitoCalifornia	C. australe	Adults	Continuous with post. constriction

Materials and Methods

Collections

Thirty-three sea lions, Zalophus californianus found stranded on the Pacific coast near San Francisco, California (37°46′ N; 122°25′ W) in February and March 2012, 2015 and 2016 were kept alive and subsequently died and examined for parasites in the Marine Mammal Center (TMMC), Sausalito, California (see Kuzmina et al., 2018 for details). A total of 1,201 adult specimens of C. australe were collected from one 2-year-old female sea lion, necropsied at TMMC in 2015 (Lisitsyna et al., 2018). Fifty-one specimens of this collection were whole mounted and studied by Lisitsyna et al. (2019) to verify the synonymy of C. obtuscens with C. australe. A sub-set of about 170 specimens from the initial larger collection was made available to Omar M. Amin (OMA) for our study. Of these specimens, 29 specimens were processed for microscopical studies, 12 for SEM, and 2 for molecular analysis. Twelve of the whole-mounted specimens were deposited at the Harold W. Manter Laboratory (HWML) parasitology collection, University of Nebraska State Museum, Lincoln, Nebraska. The remaining specimens are in the OMA collection.

Methods for microscopical studies

Worms were punctured with a fine needle and subsequently stained in Mayer's acid carmine, destained in 4 % hydrochloric acid in 70 % ethanol, dehydrated in ascending concentrations of ethanol (24 hr each), and cleared in 100 % xylene then in 50 % Canada balsam and 50 % xylene (24 hr each). Whole worms were then mounted in Canada balsam. Measurements are in micrometers, unless otherwise noted; the range is followed by the mean values between parentheses. Width measurements represent maximum width. Trunk length does not include proboscis, neck, or bursa.

Line drawings

Line drawings were created by using a Ken-A-Vision micro projector (Ward's Biological Supply Co., Rochester, N.Y.) which uses cool quartz iodine 150W illumination. Images of stained whole mounted specimens are projected vertically on 300 series Bristol draft paper (Starthmore, Westfield, Massachusetts), then traced and inked with India ink. The completed line drawings are subsequently scanned at 600 pixels on a USB and subsequently downloaded on a computer.

Specimens

Voucher specimens were deposited at the University of Nebraska's State Museum Harold W. Manter Laboratory (HWML) collection in Lincoln, Nebraska, USA; No. 216825 (12 voucher specimens on 3 slides) were sectioned using the FEI Helios Dual Beam Nanolab mentioned above. A gas injection magnetron sputtering technique regulating the rate of cutting. The hooks of the acanthocephalans were centered on the SEM stage and cross-sectioned using an ion-accelerating voltage of 30 kV and a probe current of 2.7 nA following the initial cut. The sample goes through a cleaning cross-section milling process to obtain a smoother surface. The cut was analyzed with an X-ray normally at the tip, middle, and base of hooks for chemical ions with an electron beam (Tungsten) to obtain an X-ray spectrum. The intensity of the GIS was variable according to the nature of the material being cut. Results were stored with the attached imaging software and then transferred to a USB for future use.

Energy Dispersive X-Ray analysis (EDXA)

The Helios Nanolab 600 is equipped with an EDXA (Mahwah, NJ) TEAM Pegasus system with an Octane Plus detector. The sectioned cuts were analyzed by EDXA. Spectra of selected areas were collected from the center and the edge of each cross-section. EDXA spectra were collected using an accelerating voltage of 15 kV, and a probe current of 1.4 nA. Data collected included images of the displayed spectra as well as the raw collected data. Relative elemental percentages were generated by the TEAM software.

Molecular analyses

DNA extraction from ethanol-fixed specimens of C. australe (n=2) was performed using the DNeasy Blood & Tissue Kit (QIAGEN, Hilden, Germany) following the manufacturer's instructions. Sequences of the 18S rDNA and mitochondrial cox1 gene were obtained by sequencing PCR products. For 18S we used the primers 18SU467F and 18SL1310R (Suzuki et al., 2008) and PCR conditions according to Amin et al. (2022a). For cox1, we used the primers LCO1490 and HCO2198 (Folmer et al., 1994) and PCR conditions as described by Amin et al. (2022a). PCR products were electrophoresed and purified with the Purelink^TM PCR Purification Kit (Invitrogen). Sequencing was then performed in both directions with the same primers mentioned above using the Big Dye Terminator Cycle Sequencing Reaction Kit.

The sequences obtained were edited in BioEdit software (Hall, 1999) and aligned using ClustalW implemented in MEGA v.11 (Tamura et al., 2021). List of acanthocephalans used in the phylogenetic analyses is presented in Tables 2 and 3. The best nucleotide substitution model was determined for 18S (GTR + I + G) and Cox1 (HKY+G+I) based on Akaike Information Criterion in MEGA MEGA v.11 (Tamura et al., 2021). Phylogenetic analyses were performed using Maximum Likelihood (ML) and Bayesian inference (BI) methods. ML tree was computed in MEGA v.11 and 1000 bootstrap pseudoreplicates were estimated for nodal support. The BI analysis was performed in TOPALi software (Milne et al., 2009) using Markov chain Monte Carlo (MCMC) searches on two simultaneous runs of four chains for 1,000,000 generations and sampling every 100th generation. The first 25 % of the sampled trees were discarded as ‘burn-in’. Information on the sequences used in the phylogenetic analyses is presented in Table 2. Pairwise genetic distances (uncorrected p-distance model) were calculated in MEGA v. 11. The new sequences obtained for C. australe in the present study were deposited in GenBank.

Table 2.

List of acanthocephalan species used for phylogenetic analysis based on the 18S rDNA gene sequences. Newly generated sequences are presented in bold, NA=host name not available.

Species	Host	Host origin	GenBank accession nos.	References
Corynosoma australe	Zalophus californianus	USA	ON614192, ON614199	present study
	Zalophus californianus	USA	MK119255	Lisitsyna et al., 2019
	Phocarctos hookeri	Mexico	JX442168	García-Varela et al., 2013
Corynosoma obtuscens	Callorhinus ursinus	Mexico	JX442169	García-Varela et al., 2013
Corynosoma validum	Callorhinus ursinus	Mexico	JX442170	García-Varela et al., 2013
Corynosoma enhydri	NA	USA	AF001837	Near et al., 1998
Corynosoma magdaleni	Phoca hispida botnica	Mexico	EU267803	García-Varela et al., 2009
Corynosoma strumosum	Phoca vitulina	Mexico	EU267804	García-Varela et al., 2009
Bolbosoma balaenae	Nyctiphanes couchii	Spain	JQ040306	Gregory et al., 2011^*
Bolbosoma turbinella	Eschrichtius robustus	Mexico	JX442166	García-Varela et al., 2013
Bolbosoma vasculosum	Lepturacanthus savala	Indonesia	JX014225	Verweyen et al., 2011
Andracantha gravida	Phalacrocorax auritus	Mexico	EU267802	García-Varela et al., 2009
Hexaglandula corynosoma	Nyctanassa violacea	Mexico	EU267808	García-Varela et al., 2009
Pseudocorynosoma anatarium	Bucephala albeola	Mexico	EU267801	García-Varela et al., 2009
Pseudocorynosoma constrictum	Anas clypeata	Mexico	EU267800	García-Varela et al., 2009
Profilicollis bullocki	Emerita analoga	Mexico	JX442174	García-Varela et al., 2013
Profilicollis botulus	Somateria mollissima	Mexico	EU267805	García-Varela et al., 2009
Polymorphus trochus	Fulica americana	Mexico	JX442196	García-Varela et al., 2013

*

– direct submission of unpublished data to GenBank

Table 3.

List of acanthocephalan species used for phylogenetic analysis based on the mt Cox1 gene sequences. Newly generated sequences are presented in bold.

Species	Host	Host origin	GenBank accession nos.	References
Corynosoma australe	Zalophus californianus	USA	ON619618, ON614719	present study
	Zalophus californianus	USA	MK119245–MK119249	Lisitsyna et al., 2019
	Zalophus californianus	Mexico	MT676808–MT676818	García-Varela et al., 2020
	Merluccius hubbsi	Argentina	MT676819–MT676822	García-Varela et al., 2020
	Raneya brasiliensis	Argentina	MT676823–MT676824	García-Varela et al., 2020
	Paralichthys isosceles	Brazil	KU314822	Fonseca et al., 2019
	Stenella clymene	Argentina	MW724483	Hernández-Orts et al., 2021
	Arctocephalus australis	Argentina	MF497333	Hernández-Orts et al., 2017a
	Spheniscus magellanicus	Brazil	MF497335	Hernández-Orts et al., 2017a
	Otaria flavescens	Argentina	KX957714, MF497334	Hernández-Orts et al., 2017a, b
	Paralichthys adspersus	Peru	MZ920052–MZ920055	Mondragon-Martinez et al., 2021^*
	Paralabrax humeralis	Peru	MZ920056–MZ920059	Mondragon-Martinez et al., 2021^*
	Cheilodactylus variegatus	Peru	MZ920060–MZ920063	Mondragon-Martinez et al., 2021^*
	Otaria byronia	Peru	MZ920064–MZ920067	Mondragon-Martinez et al., 2021^*
Corynosoma hannae	Colistium guntheri	New Zealand	KX957724, KX957725	Hernández-Orts et al., 2017b
	Leucocarbo chalconotus	New Zealand	KX957718–KX957721, KX957723	Hernández-Orts et al., 2017b
	Phalacrocorax punctatus	New Zealand	KX957722	Hernández-Orts et al., 2017b
	Phocarctos hookeri	New Zealand	KX957715–KX957717, JX442191	Hernández-Orts et al., 2017b; García-Varela et al., 2013
	Peltorhamphus novaezeelandiae	New Zealand	KY909260–KY909263	Anglade & Randhawa, 2018
Corynosoma semerme	Halichoerus grypus	Germany	MF001277	Waindok et al., 2018
Corynosoma semerme	Callorhinus ursinus	USA	MK119253	Lisitsyna et al., 2019
Corynosoma obtuscens	Halichoerus grypus	New Zealand	JX442192	García-Varela et al., 2013
Corynosoma villosum	Callorhinus ursinus	USA	MK119251	Lisitsyna et al., 2019
Corynosoma validum	Callorhinus ursinus	USA	MK119252	Lisitsyna et al., 2019
Corynosoma enhydri	Enhydra lutris	USA	DQ089719	García-Varela & Nadler, 2006
Corynosoma magdaleni	Phoca vitulina	Germany	MF078642	Waindok et al., 2018
Corynosoma nortmeri	Phoca vitulina	Germany	MF001278	Waindok et al., 2018
Corynosoma strumosum	Phoca vitulina	USA	EF467870	García-Varela & Pérez-Ponce de León, 2008
	Pusa hispida botnica	Finland	EF467871	García-Varela & Pérez-Ponce de León, 2008
	Zalophus californianus	USA	MK119250	Lisitsyna et al., 2019
Bolbosoma balaenae	Balaenoptera physalus	Italy	MZ047281	Santoro et al., 2021
Bolbosoma turbinella	Eschrichtius robustus	USA	JX442189	García-Varela et al., 2013
Andracantha phalacrocoracis	Zalophus californianus	USA	MK119254	Lisitsyna et al., 2019
Hexaglandula corynosoma	Nyctanassa violacea	Mexico	EU189488	Guillén-Hernández et al., 2008
Pseudocorynosoma anatarium	Bucephala albeola	Mexico	KX688148	García-Varela et al., 2017
Pseudocorynosoma tepehuanesi	Oxyura jamaicensis	Mexico	KX688139	García-Varela et al., 2017
Polymorphus obtusus	Aythya affinis	Mexico	JX442195	García-Varela et al., 2013
Profilicollis bullocki	Emerita analoga	Mexico	JX442197	García-Varela et al., 2013
Profilicollis chasmagnathi	Oligosarcus jenynsii	Argentina	MT580124	Levy et al., 2020
Polymorphus trochus	Fulica americana	Mexico	JX442196	García-Varela et al., 2013

*

– direct submission of unpublished data to GenBank

Among the populations of C. australe, we examined Cox1 haplotype frequency using the DNAsp v5 program (Librado & Rozas, 2009) and calculated the number of haplotypes (H) and the haplotype diversity (Hd). The haplotype network was constructed using Network software 10.2.0.0 version (Bandelt et al., 1999).

Ethical Approval and/or Informed Consent

The authors declare that they have observed all applicable ethical standards.

Results

Of the 1,201 specimens originally collected from the single sea lion in California in 2015, 51 specimens (24 males, 27 females) were initially reported as C. obtuscens (Lisitsyna et al., 2018; Kuzmina et al., 2018) and re-identified as C. australe by Lisitsyna et al. (2019) and studied for morphological variability and morphometric comparisons. See Table 1 for hosts. Measurements of our subset of 29 specimens (16 males, 13 females) of the same collection were comparable to those of the 51 specimens reported by Lisitsyna et al. (2019, Table 2) from the same original collection from the same single sea lion. Lisitsyna et al. (2019) did not provide a qualitative description of the California specimens but included schematic line drawings of the outline of a whole male and a female (Figs. 1, 2) and photomicrographs of the posterior body wall of type females of C. obtuscens (Figs. 3 – 8).

SEM of whole male (Fig. 1) and female (Fig. 2) specimens of Corynosoma australe from the intestines of Zalophus californianus in California. Note the continuity of the ventral field of spines from the neck to the genital area in the female which is covered with a copulation plug (Fig. 2).

SEM of male and female specimens of Corynosoma australe from the intestines of Zalophus californianus in California. 3. Praesoma of a male worm showing the conical neck and the ventral spinose part of the anterior part of the trunk just anterior to the bulbus (white arrow) and the sensory pore (black arrow). 4. The anterior proboscis of a specimen showing the organization of the longitudinal rows of large hooks and the external appearance of the apical organ (arrow). 5. Apical view of the proboscis in Fig. 4 showing the external surface of the apical organ. 6. Lateral view of apical and subapical hooks. 7. Lateral view of middle hooks. 8. Posterior-most spine-like hooks. Note their arched curvature compared to more anterior hooks.

In this presentation, we provide (1) a qualitative description of the California population of C. australe; (2) additional measurements and counts not available in Lisitsyna et al. (2019, Table 2) including dimensions of neck, lemnisci, cement glands, bursa, and length of the anterior, middle, and posterior hooks, and of the female reproductive system, and numbers of genital spines; (3) a complete set of SEM images now available for the first time, with noted exceptions (see below), depicting features not previously described or impossible to delineate using light microscopy and line drawing. Aznar et al. (2016) provided elaborate SEM of trunk spines. Hernández-Orts et al. (2017a) provided 4 SEM images of a male and a female and their posterior trunk. Halajian et al. (2020) provided a limited number of good quality SEM images missing whole male and female, anterior, middle and posterior hooks, sections of anterior, middle and posterior spines, detail and sensory structures of a male bursa, differentiation of micropores in various trunk regions, distribution of trunk spines in females; (4) a detailed EDXA of hook, spine, and egg spectra that shows notable differences from the pattern in a different population of C. australe from the Cape fur seal Arctocephalus pusillus pusillus in South Africa.

Scanning electron microscopy (SEM)

Twelve specimens that had been fixed and stored in 70 % ethanol were processed for SEM following standard methods (Lee, 1992) These included critical point drying (CPD) (Tousimis Automandri 931.GL) and mounting on aluminium SEM sample mounts (stubs) using conductive double-sided carbon tape. Samples were sputter coated with an 80 % – 20 % gold-palladium target for 3 minutes using a sputter coater (Quorum (Q150T ES) www.quorumtech.com) equipped with a planetary stage, depositing an approximate thickness of 20 nm. Samples were placed and observed in an FEI Helios Dual Beam Nanolab 600 (FEI, Hillsboro, Oregon) Scanning Electron Microscope (FEI, Hillsboro, Oregon). Samples were imaged using an accelerating voltage of 5 kV, and a probe current of 86 pA, at high vacummusing a SE detector.

Focused Ion Beam (FIB) sectioning of hooks

A dual-beam SEM with gallium (Ga) ion source (GIS) is used for the LIMS (Liquid Ion Metal Source) part of the process. Hooks (Halajian et al., 2020), and (5) phylogenetic reconstruction using mt Cox1 sequences, a median-joining haplotype networks based on Cox1 sequence data of C. australe and a phylogenetic tree from Maximum likelihood and Bayesian inference analysis of the Cox1 sequences for our California material.

Of the taxonomic accounts listed in Table 1, only Smales (1986) provided a redescription of C. australe from Neophoca cinerea in South Australia that included a few qualified differences noted following. Zdzitowiecki (1984) also provided a detailed redescription of C. australe from pinnipeds which, however, included differences in the interpretation of the female reproductive system; see our Fig. 36 and corrections in Figs. 33, 34, and associated text. Lisitsyna et al. (2019) included an analysis for species of Corynosoma based on cox 1 and 18S sequences. The following description is based on 29 specimens from Zalophus californianus in California. Characters reported for the first time are bolded.

Description

General. With characters of the genus Corynosoma Lühe, 1904 (Polymorphidae). Worms small, spindle-shaped, with main longitudinal lacunar canals lateral, lemniscal, cement gland, and hypodermal nuclei fragmented, and ligament sacs in females single, not persistent. Worms with slight sexual dimorphism in size of trunk, proboscis, hooks, and other structures in common (Figs. 1, 2). Praesoma, proboscis, and anterior receptacle bent ventrad. Swollen fore-trunk tapers gradually to more cylindrical hind-trunk. About 6 – 8 incomplete circles of ventro-lateral spines just posterior to neck (Fig. 3) preceding complete compact circles of anterior trunk spines (crown spines) extending posteriorly to area of maximum diameter of swollen fore-trunk dorsally in both sexes (Fig. 9). Ventral extension of spines between neck and the larger genital trunk spines continuous in females (Fig. 2) but invariably interrupted posteriorly in males (Fig. 1). Distribution of ventral spines from neck to genital spines (Fig. 18) not homogeneous. Ventral space between crown spines (Figs. 9, 15) and spines on posterior cylindrical part of trunk (Fig. 17) occupied by smaller, weaker, and more thinly distributed transitional spines (Fig. 16; arrow) varying significantly in their size (smaller) and metal composition (poorer) using EDXA than other spines (Table 4). See differences in anatomy, size and strength of anterior, transitional and posterior trunk spines (Figs. 22 – 24, respectively). Continuous field of ventral trunk spines in females constricts posteriorly (Figs. 18 – 19, arrows) but never interrupted. Genital spines most robust (Figs. 20 and 25). Electron-dense micropores cover cuticular surfaces of anterior proboscis, hooks, spines, and aspinose areas of trunk (Figs. 10 – 14). See higher magnification of micropores on posterior and anterior trunk spines (Figs. 14 and 21, respectively). Proboscis long, cylindrical, slightly widening posteriorly, with elevated apical disc suggestive of surface of apical organ anteriorly (Figs. 4 – 5) and 17 – 19 longitudinal alternating rows of 11 – 14 hooks each. Hooks of 3 types. First type: anterior 7 – 9 hooks almost equally long and most slender anteriorly, with posteriorly directed, simple roots shorter than blades especially apical and subapical hooks (Figs. 6, 35 AH). Second type: Posterior 2 or 3 hooks as long as anterior hooks but more robust and wider at base with posteriorly directed roots longer than blades (Figs. 7, 35 PH). Third type: posterior-most 2 – 4 hooks (Figs. 8, 35 BH) smallest, curving, with shorter but distinct roots directed anteriorly (manubria). Neck conical with paired lateral sensory pores (Fig. 3, black arrow). Proboscis receptacle double-walled with cerebral ganglion about halfway at middle. Lemnisci equal, broad, rounded to irregular, shorter than receptacle.

SEM of anterior bulbus and micropores of male and female specimens of Corynosoma australe from the intestines of Zalophus californianus in California. 9. Anterio-ventral view of the proboscis and bulbus of a female specimen. 10. Micropores at the anterior end of a proboscis. 11. Micropores on an anterior proboscis hook. 12. Micropores on anterior trunk spine. 13. Micropores at anterior end of a male trunk away from spines. 14. Micropores on the base of a posterior trunk spine in a male specimen.

Table 4.

Chemical composition of trunk spines and eggs of Corynosoma australe from Zalophus californianus in California.

Elements^*	Spines (longitudinal sections)			Eggs (cross sections)

	Anterior	Middle	Posterior	Edge (shell)	Center (acanthor)
Magnesium (Mg)	0.00	0.00	0.09	0.00	0.50
Sodium (Na)	0.00	0.00	0.00	0.00	0.00
Phosphorous (P)	1.39	0.00	1.16	0.91	7.73
Sulfur (S)	12.64	5.97	15.61	0	2.30
Calcium (Ca)	1.64	1.07	1.96	1.34	3.41

*

Palladium (Pd) and gold (Au) were used to count the specimens and the gallium for the cross-cut of the hooks. These and other elements: carbon (C), oxygen (O), nitrogen (N)) common in organic matter are omitted. Data is reported in weight (WT%).

Males. Based on 16 sexually mature adults with sperm. See Lisitsyna et al. (2019) for measurements and see additional measurements listed below. Apical, middle and basal hooks 37 – 47 (43), 40 – 45 (43), and 20 – 28 (25) long, respectively. Hook roots 30 – 37 (28), 40 – 47 (43), 15 – 22 (19), in the same order. Neck 157 – 218 (197) long by 333 – 395 (363) wide. Lemnisci 464 – 724 (602) long by 214 – 412 (325) wide. Genital spine 20 – 32 (25) in 3 – 4 circles. Reproductive system in all trunk space posterior to level of mid-receptacle. Testes relatively large, rounded, usually equal, crowded diagonally or laterally. Six pyriform cement glands, 300 – 522 (419) long by 187 – 270 (220) wide, in 3 pairs contiguous with testes, with long ducts joining 2 common cement gland ducts overlapping claviform Saefftigen's pouch, all draining into terminal genital terminalia in bursa. Bursa muscular, large, longer than wide, 364 – 800 (570) long by 364 – 605 (433) wide, with slightly undulating lip (Figs. 25, 26), and with inner plump interface studded with 2 sets of sensory papillae. Central inner set of large round papillae encircled by many rings of complex, and less elevated papillae (Figs. 27, 28) at the outer edge of which flat-headed penis (Figs. 28, 29) is found.

SEM of spines in male and female specimens of Corynosoma australe from the intestines of Zalophus californianus in California. 15. Anterior trunk spines in the bulbus area. 16. Transition area between bulbus spines (right) and posterior trunk spines. 17–19. Continuous ventral spines in one female specimen: 17. Midventral spines. 18. Posterior ventral spines. Note that the field of spines anterior to the genital spines constricts (arrow) but remains continuous with the genital spines without breaks. 19. Another, more detailed, perspective of posterior ventral spines of the same female in Fig. 17, 18 with arrow pointing to greatest constriction. Female gonopore is on the opposite, ventral, side (dorso-subterminal). 20. Posterior end of a male specimens with invaginated bursa revealing the organization of the genital spines there.

Detail of spines in specimens of Corynosoma australe from the intestines of Zalophus californianus in California using SEM and Gallium-cut sections. 21. SEM of an anterior trunk spine in the bulbus area. 22. A longitudinal Gallium-cut section of an anterior bulbus spine. Note the structure of the core element. 23. A longitudinal Gallium-cut section of a mid-trunk spine. 24. A longitudinal Gallium-cut section of a posterior spine. Note the structural differences between the outline and core of the spine types. 25. A dorso-terminal view of the posterior end of a male specimen showing the arrangement of the genital spines. Compare with Fig. 20. 26. A lateral view of a bursa showing its distal undulations and part of the genital spines (right).

Females. Based on 13 gravid females with many eggs. See Lisitsyna et al. (2019) for measurements and see additional measurements below. Apical, middle, and basal hooks 42 – 50 (47), 45 – 50 (48), and 22 – 31 (27) long, respectively. Hook roots 35 – 47 (41), 45 – 57 (50), 20 – 27 (24) in the same order. Neck 166 – 260 (216) long by 343 – 437 (391) wide. Genital spines 8 – 16 in 1 – 2 circles. Lemnisci obscured by eggs. Gonopore dorso-subterminal (Fig. 30) leading anteriorly to vaginal orifice, double sphincters, very long muscular uterus in 2 parts; lower and upper uterus joined by uterine bell cells (selective apparatus; SA) near its mid-point, then uterine bell adhering to ventral body wall (Figs. 33, 34). Reproductive system measuring 2.43 – 2.44 mm in two 3.45 mm long females not congested with eggs, (70 % of trunk length). Other length measurements: vagina 186 – 189, lower uterus 707 – 718, selector apparatus 177 – 225, upper uterus 1,021 – 1,040, uterine bell 300 – 312, and width measurements: selector apparatus 146 – 156, and uterine bell 208 – 215. Lower uterus inflated anteriorly irre-spective of presence or absence of eggs in it (Figs. 33, 34). Para-vaginal muscular sheet wrapping around vagina and lining posterior tip of trunk, particularly prominent ventrally. Four para-vaginal ligament cords, short and long ones each dorsally and ventrally, originating from posterior body wall and vaginal interface dorsally and ventrally and extending anteriorly. Short cords insert in body wall just anterior to posterior tubular trunk region (para-vaginal-body wall ligament cords). Long cords reaching to base and side of uterine bell (para-vaginal-uterine-bell ligament cords) (Fig. 33). Eggs elliptic, oblong, smooth, without distinguishing markings or ornamentation (Fig. 31), with marked polar prolongation of fertilization membrane and 4 membranes (Fig. 32) with markedly lower level of metals than egg center.

External orifices of male and female reproductive systems and eggs of Corynosoma australe from the intestines of Zalophus californianus in California using SEM and Gallium-cut sections. 27–29. The male bursa. 27. Bursa with the undulating lip, penis (white arrows), central cluster of prominent sensory bulbs (black arrows), and surrounding circles of specialized sensory domes (short black arrows). 28. The central part of a bursa showing the two types of sensory structures and the penis. 29. A higher magnification of the penis and the surrounding type of sensory domes. 30. The posterior end of a female showing the dorsal gonopore (right) and the continuity of the posterior ventral spines with the genital spines. 31. A smooth egg with no external ornamentation or dentations. 32. A cross Gallium-cut section of an egg showing 3 external egg shell membranes FM: fertilization membrane, IM: inner membrane, OM: outer membrane) with the fourth tightly enveloping the acanthor (A).

Taxonomic summary

Type host. Australian sea lion (hair seal) Neophoca cinerea (Otariidae)

Additional host. California sea lion, Zalophus californianus (Otariidae).

Type locality. Pearson Island, South Australia

Current locality: The Pacific coast near San Francisco, California (37°46′ N; 122°25′ W).

Site of infection. Intestine (caecum, colon)

Specimens. HWML Helminthological Coll. No. 216825 (12 voucher specimens on 3 slides). Specimens from the South Australian Museum and the U.S. National Museum were not available; loans were banned since COVID times.

Representative DNA sequence. The 18S rDNA and mt Cox1 sequences of Corynosoma australe were deposited in Gen-Bank under the accession numbers ON614192, ON614199 and ON619618, ON614719, respectively.

Remarks

Our subset of 29 specimens allowed us to give the first complete description of the California population of 1,201 specimens C. australe collected from 1 sea lion. Lisitsyna et al. (2019, Table 2) provided measurements of another set of 51 specimens from the same sea lion. These measurements, not repeated herein, did not distinguish between anterior vs. posterior testes (similar sizes) and included measurements of the blade and root of one hook (the largest); additional measurements and counts were not included. We added measurements of cement glands, bursa, neck, and three hooks (apical, middle and posterior), female reproductive system, and the number of genital spines, to our description. An account of our smaller subset of 10 males and 12 females from the same California collection was briefly outlined by Lisitsyna et al. (2018) and the fewer measurements provided there were similar to those reported by Lisitsyna et al. (2019).

Smales (1986) redescribed C. australe from Neophoca cinerea (type host) and Arctocephalus pusillatus in South Australia with measurements comparable to but at variance with measurements of our California material from Zalophus californianus. All variations, and those among other collections compared in Tables 3, 4 of Lisitsyna et al. (2019), fell within the expected range of intraspecific variations. A number of differences, however, marred the redescription based only on the actual text since the Australian materials were not available on loan. For instance, Smales (1986), described the small posterior spine-like hooks as “last 4 to 5 hooks without roots” (p. 92), “the last one to four small without roots” (p. 95), and later in the Remarks section as “posterior three to four are smaller and rootless” (p. 95). The difference in the number of these hooks aside, these small posterior hooks are not rootless as shown in figure 9 of Smales (1986) (p. 93); they have prominent anterior roots (manubria) as observed by us and demonstrated by a few other observers, i.e., Zdzitowiecki (1984, Fig. 2B, p. 362). Zdzitowiecki (1984, Table I, p. 363) also provided measurements of 1 complete row of hook blades and roots in a male. Lisitsyna et al. (2018, p. 187) also noted the anterior roots of the small posterior spine-like hooks, and also described “1–2 hooks transitional with small roots in the shape of inverted Y (fig. 2E).” In her line drawing (Fig. 8, p. 93), Smales (1986) also showed a large space, between the anterior larger hooks and the posterior spine-like hooks, which was not observed. Among the large hooks, Smales (1986) stated “First 9 to 10 hooks have well-developed roots, as long as or longer than the hook” (p. 92) and in Fig. 9 depicts roots as long as blades anteriorly but considerably longer than blades posteriorly. We have, however, observed that the roots are markedly shorter than the blades of all hooks except the last two where they are of a comparable length; see Table I in Zdzitowiecki (1984).

After having reported 22 California specimens as C. obtuscens (Lisitsyna et al., 2018), Lisitsyna et al. (2019) compared a similar subset of 51 specimens with those in 5 other collections reaching the conclusion that C. australe and C. obtuscens are the same species. This conclusion is novel and should be seen in the light of Johnston and Edmonds (1953) and Zdzitowiecki (1984) who have already noted the similarity of the two species before, and the history of the synonymy is listed in Gibson and Wayland (2022).

Morphometric variability was primarily of intraspecific nature as the dimensions of the trunk, neck, proboscis, hooks, spines, receptacle, lemnisci, reproductive structures usually overlapped. The only distinguishing difference between the 2 species was the distribution of ventral trunk spines in females; being invariably discontinuous posteriorly in males. In their original description, the female ventral spines were discontinuous posteriorly in C. australe but continuous throughout the total ventral aspect of C. obtuscens. The taxonomic history listed in Table 1 demonstrates this distinction in a few accounts but also demonstrates the opposite to various degrees in a few more accounts; see for instance Zdzitowiecki (1984), Sardella et al. (2005) and Hernández-Orts et al. (2017a). Lisitsyna et al. (2019) also found a small spine-free zone in an allotype of C. obtuscens, among other overlaps and inconsistencies, and “confirmed the variability in the arrangement of somatic spines on the ventral surface of the body of females.” The constriction of the field of posterior ventral spines in our specimens (Figs. 18, 19) offers a plausible resolution for the controversy of the presence or absence of posterior ventral spines in females. We propose that spines on this part of the female ventral trunk are labile and may constrict to the extreme point of total absence and separation of the two spine fields, or not at all.

There are also additional issues with spines. Zdzitowiecki (1984) reported 11 – 28 and 20 – 40 genital spines in males and females, respectively. We found considerably more genital spines in males than in females. Zdzitowiecki (1984) also correctly mentioned that the male genital opening is terminal while Lisitsyna et al. (2018) reported a subterminal opening in both sexes and Johnston (1937) reported a terminal opening in females; both are not in agreement with our observations.

Our microscopic study revealed most unique anatomy of the female reproductive system first observed among the thousands of specimens of many acanthocephalan species that we have examined. We noted in two clear specimens that were not congested with eggs a reproductive system making up 70 % of worm length with normal vaginal sphincters, uterine bell and a very long uterus with the uterine bell cells (SA) in the mid-point of the long uterus and not at the base of the uterine bell where it is commonly found in other species of acanthocephalans. This unique position of the SA away from the uterine bell where they normally function in direct coordination with the uterine bell is of great diagnostic value that represents a functional aenigma. No reference was made to the complete female reproductive system in the descriptions of Johnston (1937) or Lincicome (1943) or any other taxonomic accounts except for an occasional line drawing of the vagina and posterior female trunk tip as in Zdzitowiecki (1984, Fig. 2d, p. 362). However, Zdzitowiecki's (1984) Fig. 2e of a “uterine bell” was incomplete; showing a questionable position of a 4-nucleated selective apparatus cells overlapping its base and appeared to be at the distal end of the reproductive system. In reality, the glands are multicellular and are found in the middle of the uterus and not at its anterior end as characteristically peculiar in this species. The operational aspects of the selective apparatus need to be revised in light of this finding. In her redescription of C. australe, Smales (1986, Fig. 10, p. 93) drew an outline of a small female reproductive system with barely visible uterine bell and vagina showing no selective apparatus glands anywhere, within a female body; without an accompanying text. Only Zdzitowiecki (1984, p. 363) stated that “Total length of the (female) genital system, from the anterior margin of the uterine bell to the genital opening is equal to 1.1 – 1.4 (mm)” in his Antarctic specimens is comparable to our measurements of the posterior half of the genital system up to the selective apparatus pouches which Zdzitowiecki (1984) apparently interpreted as the uterine bell and created a figure (Fig. 2e, p. 362) for it. He clearly did not see the anterior half of the reproductive system ending up with the real uterine bell perhaps because of the usual congestion of the body cavity with eggs which has been the case in almost all our other specimens.

Micropores

The trunk and other structures including the proboscis, proboscis hooks, and spines (Figs. 10 – 14) had apparent osmiophilic micropores of various diameters, shapes and distribution in various body parts. In this small acanthocephalan, every possible external surface is studded with micropores. In some areas, the micropores were more widely spaced compared to the usual more widely distributed micropores more often observed in other acanthocephalan species.

Energy Dispersive x-ray analysis (EDXA)

The relative WT% concentrations obtained by the TEAM software for hooks, spines, and eggs of C. australe from a California sea lion, Z. californianus in California are reported in Tables 4 – 5 and Figs. 37 – 39. Our EDXA results of C. australe show a center core with a high level of sulfur at the tip of the middle and posterior hook's edge (15.38 %) and cross-section (23.52 %), respectively, but considerably lower (2.96 %) at the tip of anterior hooks. The EDXA spectra of cross sections of the middle of all hooks showed extremely high concentrations of Calcium and Phosphorus characteristic of the center core of hooks. The presence of Sulfur, Calcium, and Phosphorus in the EDXA spectra obtained from the edge of the hook base cross-section is attributed to the proximity of the exterior shell to the center core. In anterior and posterior spines, the sulfur level was highest, 12.64 and 15.61, respectively, but markedly lower in the weak middle spines at 5.97 % (Table 4) while the levels of phosphorus and calcium were minimal. The egg center had a higher level of metals especially phosphorous (7.73 %) compared to the egg shell (0.91 %) (Table 4). It is worth noting that, these reported WT% numbers should not be interpreted as compositional. They are, however, indicative of general compositional differences observed between the selected areas.

Line drawings of the female reproductive system and 3 selected hooks of Corynosoma australe from the intestines of Zalophus californianus in California. Fig. 33. The whole reproductive system of a 3.2 mm. long female. Note the presence of the Selective apparatus (SA) almost half way between the upper uterus (UU) connecting with the uterine bell (UB) and the lower uterus (LU) connecting with the dorsal vagina (V). Also note the dorsal and ventral short paravaginal ligament cords inserting in the body wall (PVBWLC) and the dorsal and ventral longer paravaginal ligament cords connecting with the uterine bell (PVUBLC). The para-vaginal muscular sheet wrapping around vagina can be observed. The continuity of trunk spines on the ventral side is evident. Fig. 34. A higher magnification of the posterior half of the reproductive system of a second female. Posterior muscular wrap not shown. Fig. 35. The 3 hook types: an anterior slender subapical hook (AH) with shorter root; a robust hook at the inflated part of the posterior proboscis (PH) with slightly longer root; and a small curved basal or near-basal hook (BH) with anteriorly directed root (manubrium). Fig. 36. The “uterine bell” of Corynosoma australe after Zdzitowiecki (1984, Fig. 2e, p. 362).

Energy Dispersive X-Ray spectra of Gallium cut anterior hook tip x-section (37), middle hook tip x-section (38), and posterior hook tip x-section (39) showing levels of sulfur in calcium and phosphorous in all hooks See Table 2 for more specific figures (bolded). Inserts: SEM of Gallium cut anterior hook tip cross-section (37), SEM of Gallium cut middle hook tip cross-section (38), and SEM of Gallium cut posterior hook tip cross-section (39). Note the high levels of calcium and phosphorous in anterior and middle hooks and the high level of sulfur in posterior hooks.

Molecular results

In the present study, a total of four partial 18S and Cox1 sequences of C. australe were generated. On the GenBank database, most of the sequences available for C. australe are of mt gene Cox1 and only two sequences are of 18S gene. So, for a better comparative phylogeny and to provide information related to the population relationship of C. australe we have provided a detailed analysis of Cox1 gene along with 18S gene analysis. Newly generated 18S sequences of C. australe were almost identical, shows 0.02 % genetic divergence. The sequence for C. australe from USA (MK119255) infecting the same host Z. californianus exhibited genetic divergence was 0.27 %, while with another isolate from Mexico (JX442168) infected Phocarctos hookeri divergence was 1.5 %. The phylogenetic analyses inferred with maximum likelihood (ML) and Bayesian inference (BI) methods yielded similar topologies (Fig. 40). In both phylogenetic trees, C. australe was placed with the other isolates of similar species in a clade having strong bootstrap and Bayesian probability values (Fig. 40).

Phylogenetic relationships inferred using 18S gene sequences of Corynosoma australe and other acanthocephalan species. Nodal support from the two analyses is indicated as ML/BI and indicates values of bootstrap >70%. The scale-bar indicates the expected number of substitutions per site.

In the newly generated Cox1 sequences of C. australe shows only 0.04 % intraspecific genetic divergences. Our phylogenetic tree showed that the genus Corynosoma is comprised of two main subclades – the first one A comprises specimens of C. australe from different regions in North America, i.e., the USA and Mexico, and the second one B comprises Brazil, Argentina and Peru in South America available in the GenBank database. All isolates of subclades A and B were nested in a monophyletic clade as they are the same species (Fig. 41). In the present study, Cox1 sequences of C. australe showed a strong relationship with sequences of Lisitsyna et al. (2019) from California, USA (genetic divergence was 0.9 %). The phylogenetic analyses deduced with ML and BI methods produced the same topologies. Both trees placed the specimens of C. australe in a clade obtaining strong bootstrap support and Bayesian posterior probability values (Fig. 41). The genetic divergence between the present isolates and those available in GenBank from different regions ranged from 0.9 to 3.0 %. The sequence for C. australe suggests that in comparison with other isolates of C. australe it exhibited the lowest divergence level with the isolates from the USA and the highest divergence level with the isolates from Peru (3.0 %). We also agreed with Hernández-Orts et al. (2017b) that C. hannae is a sister taxon to C. australe as both species shares close clades (Fig. 41). Another clade comprises species as different lineages as C. semerme together with C. obtuscens, C. villosum plus the sequence of C. validum, C. enhydri along with C. magdaleni isolates and a separate lineage was formed by the sequences identified as Corynosoma strumosum (Fig. 41). Lisitsyna et al., 2019 mentioned in their study that the morphological study of the isolates in the publication of García-Varela et al. (2013) was not possible due to the lack of specimens and that the species was misidentified. They also made it clear in their study that the cox1 sequence (JX442192) (Fig. 41) as well as the 18S rDNA sequence (JX442169) (Fig. 40) of C. obtuscens published by García-Varela et al. (2013) show C. semerme instead of C. obtuscens. In our study, a haplotype network was constructed inferred with 46 specimens of C. australe as shown in Fig. 42. In the complete analysis, 22 haplotypes were detected (Table 3). The H1 haplotype (H1, n = 2) are the specimens collected in the present study from the Pacific coast near San Francisco, California corresponded to specimens from North America. H2 Haplotype (H2, n = 8) are shared by C. australe populations from Mexico and Sausalito, California, the USA (approximately 10 miles north of San Francisco from where we have collected our specimens). Haplotypes H3 and H4 were found in Brazil and Argentina, respectively corresponding to the population of C. australe from South America. Haplotypes H5–H8 and H10, H11, H14, and H17 were found in Mexico corresponding to the specimens from North America. Haplotypes H9, H12, H13, H15, H16 and H20 were reported as C. australe populations of Argentina. Haplotypes H18 and H19 were found from Brazil and corresponded to specimens from South America. Furthermost haplotype (H21, n=14) and haplotype H22 were found off the Peruvian coasts (Fig. 42). A separate tree was also constructed in the present analysis for the isolates of C. australe representing clusters as in congruence of the haplotype network (Fig. 43). Additionally, isolates collected in the present study fell within a strongly supported clade representing the North American isolates of C. australe (Fig. 43).

Phylogenetic reconstruction using mt Cox1 sequences of Corynosoma australe and sequences of other Acanthocephala deposited in the GenBank. The numbers indicate values of bootstrap >50%. Numbers above branches indicate nodal support as maximum likelihood (ML) and posterior probabilities from BI. The scale-bar indicates the expected number of substitutions per site.

Median-joining haplotype networks based on Cox1 sequence data of Corynosoma australe. Each circle size represents the frequency of a haplotype as in the population.

Phylogenetic tree from Maximum likelihood and Bayesian inference analysis of the Cox1 sequences of Corynosoma australe population. Outgroup: Corynosoma hannae. The scale-bar indicates the expected number of substitutions per site. Abbreviations used for isolates country: U1- present study isolates from USA, U- USA, M- Mexico, B- Brazil, A- Argentina, P- Peru. The color refers to isolates obtained as in the haplotype network (Fig. 42; red: USA, blue: Mexico, orange: Argentina, magenta: Brazil, aqua blue: Peru).

Discussion

Morphological findings

Our report provides new insights on the morphology of structures not previously reported in the many descriptive accounts of C. australe against the backdrop of works by other observers summarized in Table 1. We explore these new insights in the following points.

The controversy of the identity of C. australe vs. that of its synonym C. obtuscens boiled down to differences in the distribution of ventral trunk spines in females, being continuous in C. obtuscens and disjunct in C. australe. A summary of these controversies is presented in Table 1 which shows that this character is variable but no plausible explanation was provided to explain this variability. We provided evidence of variable constriction in the posterior field of ventral spines (Figs. 18, 19) that when extremely restricted will produce a separation in the more anterior and posterior fields. In our specimens, the ventral trunk spines were invariably continuous but the degree of posterior constriction varied.

The anatomy of the female reproductive system was invariably incompletely reported. In almost all reports, only the posterior-most part showing the vagina and posterior-most extremity of the uterus could be seen; for example, see Smales (1986) and Zdzitowiecki (1984, 1991). Only Zdzitowiecki (1984) measured the posterior part of the reproductive system interpreting it as the whole system; the true uterine bell must have been obscured by eggs. He considered the SA as the uterine bell (see his Fig. 2e, p. 362 copied as our Fig. 36). The confusion is readily understandable as these acanthocephalan females are usually congested with eggs that almost invariably occupy the anterior inflated part of the trunk obscuring the anterior part of the reproductive system. We have provided the first description of the complete reproductive system and identified the SA for the first time almost in the middle of the long uterus (Figs. 33, 34) and not at the base of the terminal anterior uterine bell where it has been invariably reported by other observers to date until our present finding. We have also provided the first description of four para-vaginal ligament cords; two short ones connecting to the body wall dorsally and ventrally, and two longer ones connecting to the uterine bell more anteriorly.

We have identified micropores on all body surfaces (Figs. 10 – 14) in an apparent adaptation to utilize as much body surface as possible for the process of nutrient absorption accommodating the small size of this acanthocephalan.

We provide considerable detail on the organization of the male reproductive system and show for the first time the elaborate sensory system of the bursa necessary for the successful completion of the copulatory process in C. australe. The shape and complexity of bursal sensory structures are species-specific but have rarely been reported by other observers. Halajian et al. (2020, p. 128) made a brief reference to “Bursal papillae surrounding the genital opening (their Figs. 9, 10) are noted” and Hernández-Orts et al. (2017a, Fig. 4 D, p. 9) showed an SEM of the genital spines on the posterior end of a male trunk. For a detailed SEM study of these sensory structures in the male reproductive organs of 28 species in 10 families and 5 orders of acanthocephalans, see Amin et al. (2020a).

We discuss trunk spines in new detail. Their distribution on all trunk surfaces (Figs. 1, 2), their ventral presence anterior to the usually reported anterior rings only (first report: Fig. 3, white arrow), the scanty and weak transitional spines (Fig. 16, arrow) with the lowest level of sulfur (Table 4) (first report) and comparative anatomy of anterior, transitional, and posterior spines (Figs. 22 – 24) (first report).

We provide EDXA of anterior, middle and posterior hooks and eggs for the first time (Tables 2, 3, Figs. 37 – 39) that clearly varied from that of another C. australe population studied from the Cape fur seal, A. pusillus pusillus in South Africa.

We provide SEM images suggesting the presence of an apical organ (Figs. 4, 5) and the anteriorly directed roots (manubrial) of the posterior-most spine-like hooks (Fig. 35). These hooks have been usually described as rootless spines/hooks; see the redescription by Smales (1986). The only other related reports are those of Lisitsyna et al. (2018, p. 187) who described them as “simple roots directed anteriorly or without roots” and Zdzitowiecki (1984) who included his Fig. 2b (p. 362) showing a lateral view of 1 hook row with the posterior-most hooks having anteriorly directed roots without a corresponding text reference.

Micropores

The micropores of C. australe, like those reported from other species of the Acanthocephala, are associated with internal crypts and vary in diameter and distribution in different trunk regions corresponding with differential absorption of nutrients. In C. australe, the micropores were distributed in most body surfaces that we have observed including the proboscis, proboscis’ hooks, trunk, and trunk spines as though to maximize the absorptive function of all surfaces of their small body. We have reported micropores in a large number of acanthocephalan species (Heckmann et al., 2013) and in a few more since, and demonstrated the tunnelling from the cuticular surface into the internal crypts by TEM. Amin et al. (2009) gave a summary of the structural-functional relationship of the micropores in various acanthocephalan species including Rhadinorhynchus ornatus Van Cleave, 1918, Polymorphus minutus (Goeze, 1782) Lühe, 1911, Moniliformis moniliformis (Bremser, 1811) Travassos, 1915, Macracanthorhynchus hirudinaceus (Pallas, 1781) Travassos 1917, and Sclerocollum rubrimaris Schmidt and Paperna, 1978. Wright and Lumsden (1969) and Byram and Fisher (1973) reported that the peripheral canals of the micropores are continuous with canalicular crypts. These crypts appear to “constitute a huge increase in external surface area. implicated in nutrient up take.” Whitfield (1979) estimated a 44-fold increase at a surface density of 15 invaginations per 1 μm² of M. moniliformis tegumental surface. The micropores and the peripheral canal connections to the canaliculi of the inner layer of the tegument were demonstrated by transmission electron micrographs in Corynosoma strumosum (Rudolphi, 1802) Lühe, 1904 from the Caspian seal Pusa caspica (Gmelin, 1788) in the Caspian Sea (Figs. 19, 20 of Amin et al., 2011) and in Neoechinorhynchus personatus Tkach, Sarabeev, Shvetsova, 2014 from flathead grey mullet Mugil cephalus Linn. 1758 in Tunisia (Figs. 26, 29, 30 in Amin et al., 2020a).

Energy Dispersive X-ray Analysis (EDXA)

Our studies of acanthocephalan worms have usually involved EDXA of FIB-sectioned hooks and spines (Heckmann, 2006, Heckmann et al., 2007, 2012; Standing & Heckmann, 2014). Our results of chemical ions of hooks, spines, and eggs of C. australe from the California sea lion, Z. californianus in California varied from those obtained by Halajian et al. (2020, Table 1, p. 129) for a different population of the same species, C. australe, from the Cape fur seal Arctocephalus pusillus pusillus off the Namibian coast, South Africa. In specimens from South Africa, one hook had markedly lower levels of Calcium (36.10 – 43.2 %) and of Sulfur (0.2 – 0.38) (Halajian et al., 2020) compared to our specimens with 32.03 – 72.06 % and 0.34 – 3.50 % Calcium, respectively reaching 23.52 % Calcium at the tip of posterior hooks (Table 5), and spines had higher levels of Sulfur of 15.35 – 29.87 % than in our California specimens with 5.97 – 15.61 % (Table 4), among differences in other elements. The eggshell of the Namibian specimens also had considerably higher levels of Sulfur and Phosphorous. Such differences are probably related to parasite population variations, host species, and geography.

Table 5.

Chemical composition and localization of elements in hooks of Corynosoma australe from Zalophus californianus in California.

	Anterior hooks		Middle hooks					Posterior hooks

Element^*	Tip x-section	Middle	Longitudinal section	Tip x-section	Tip edge	Middle x-section	Middle edge	Tip x-section	Middle edge
Magnesium (Mg)	1.21	0.23–1.67^**	0.02–0.07	0.63	0.62	1.61	0.66	0.02	0.78–1.52
Sodium (Na)	0.25	0.00–0.04	0.00–0.03	0.00	0.03	0.08	0.00	0.02	0.05–0.07
Phosphorous (P)	9.95	15.74–18.71	12.78–20.35	10.64	11.00	21.32	16.10	2.82	14.91–20.49
Sulfur (S)	2.96	0.09–7.10	0.34–3.50	5.50	15.38	0.03	4.34	23.52	1.18–14.09
Calcium (Ca)	18.99	30.80–34.84	32.03–72.06	19.98	19.11	42.48	34.18	3.16	27.05–40.39

*

Palladium (Pd) and gold (Au) were used to count the specimens and the gallium for the cross-cut of the hooks. These and other elements (carbon (C), oxygen (O), nitrogen (N)) common in organic matter are omitted. Data is reported in weight (WT%). Bolded numbers are represented in Figs. 25–27.

**

A range indicates that 3 hooks were analyzed.

Sulfur is usually seen at the outer edge of large hooks and Calcium and Phosphorus are major ions in the base and middle of hooks where tension and strength are paramount for hook function. The following results of the EDXA of the FIB-sectioned hooks (dual beam SEM) are limited to those from our California C. australe material. The edge of the hook tips and the tip x-section of C. australe showed the highest level of Sulfur (15.38, 23.52). Comparable or higher levels of Sulfur were observed in other species of acanthocephalans. For instance, Cavisoma magnum (Southwell, 1927) Van Cleave, 1931 from Mugil cephalus in the Arabian Sea, has a similar pattern but considerably higher levels of sulfur in hook tips (43.51 wt. %) and edges (27.46 wt. %) (Amin et al., 2018). Our results are comparable to those of mammalian teeth enamel. The chemical elements present in the hooks are typical for acanthocephalans (Heckmann et al., 2007, 2012).

On the other hand, all trunk spines of C. australe had the highest level of sulfur reaching 15.61 % in posterior spines, and negligible levels of calcium and phosphorous. The middle weaker transitional spines (Figs. 16, 23) had the lowest level of sulfur of only 5.97 %. These levels are characteristic of C. australe as the level of sulfur in the anterior and posterior spines of Southwellina hispida (Van Cleave, 1925) Witenberg, 1932 was only 0.98 % and 0.96 % and the levels of calcium and phosphorous was also negligible (Table 5 of Amin et al., 2022a). In cystacanths of Profilicollis altmani (Perry, 1942) Van Cleave, 1947, another marine acanthocephalan, the pattern of sulfur levels in anterior, middle, and posterior spines was comparable to that in C. australe but the % weight was considerably lower (2.70 – 3.21 %, 2.56 %, and 3.28 – 3.94 %, respectively) and the % weight of phosphorous and calcium was considerably higher (Table 5, Amin et al., 2022a). This comparison suggests that water salinity is not involved in the distribution of elements in the spines of marine species of acanthocephalans.

The acanthor of C. australe had much higher levels of metals, especially phosphorous (7.73 %) compared to the egg shells (0.91 %) (Table 4). In terrestrial acanthocephalans such as Macracanthorhychus hirudanaceus (Pallas, 1781) infecting a mammalian host, Sus scrofa Linn.,1758, WT % of all metals, especially phosphorous was considerably higher in the cortical layer (23.48 %), compared to the middle of the egg (acanthor) (2.26 %), and moderate levels of sulfur and calcium (Table 3 in Amin et al., 2021). Phosphorous is a basic element in the hardening of egg shell, especially of terrestrial acanthocephalans and may be related to the protection of eggs from desiccation. “The 4 outer eggshell layers E1–E4 surrounding the acanthor of M. hirudinaceus were shown to contain glycoproteins (Peters et al., 1991). Glycoproteins are structural molecules forming collagen and some include phosphorus in phosphoserine (an ester of serine and phosphoric acid) in the process of P-glycosylation (Murray et al., 2006) which may explain the high Phosphorous content of 23.48 % in the cortical eggshell layer only” (Amin et al., 2021). “Results of X-ray scans of eggs are available in one other terrestrial species of acanthocephalans, Centrorhynchus globocaudatus (Zeder, 1800) Lühe, 1911 (Centrorhynchidae) were obtained from Falco tinnunculus Linn., 1758, (Falconidae) and Buteo buteo Linn., 1758 (Accipitridae) in northern Italy. Eggs of C. globocaudatus had the highest levels of sulfur in the cortical (12.94 %) and core areas (8.04 %) and a high level of Phosphorus (9.01 %) in the middle (Table 6, Fig. 32 in Amin et al., 2020b).

Table 6.

Data for the population of Corynosoma australe used in the haplotype networking using mt Cox1 gene. Asterisk shows sequences unpublished on NCBI database. Newly generated sequences are presented in bold.

Geographical Locality^*	Cox1Haplotype no.	ID in Fig. 46	GenBank accession nos.	References
Pacific coast near San Francisco, California, USA	H1	U1	ON619618, ON614719	Present study
Sausalito, California, USA	H2	U	MK119245-MK119249	Lisitsyna et al. 2019
Baja California, Mexico	H2	M	MT676816-MT676818	García-Varela et al. 2021
Rio de Janeiro, Brazil	H3	B	KU314822	Fonseca et al. 2019
Chubut, Argentina	H4	A	MW724483	Hernández-Orts et al. 2021
Baja California, Mexico	H5	M	MT676813	García-Varela et al. 2021
Sonora, Mexico	H6	M	MT676811	García-Varela et al. 2021
Baja California, Mexico	H7	M	MT676814	García-Varela et al. 2021
Sonora, Mexico	H8	M	MT676810	García-Varela et al. 2021
Northern Patagonia, Argentina	H9	A	MT676821	García-Varela et al. 2021
Sonora, Mexico	H10	M	MT676809	García-Varela et al. 2021
Baja California Sur, Mexico	H11	M	MT676808	García-Varela et al. 2021
Northern Patagonia, Argentina	H12	A	MT676823	García-Varela et al. 2021
Northern Patagonia, Argentina	H13	A	MT676819, MT676820, MT676822	García-Varela et al. 2021
Baja California, Mexico	H14	M	MT676815	García-Varela et al. 2021
Northern Patagonia, Argentina	H15	A	MT676824	García-Varela et al. 2021
Northern Patagonia, Argentina	H16	A	MF497333	Hernández-Orts et al. 2021
Baja California, Mexico	H17	M	MT676812	García-Varela et al. 2021
Rio de Janeiro, Brazil	H18	B	MF497335	Hernández-Orts et al. 2021
Northern Patagonia, Argentina	H19	A	MF497334	Hernández-Orts et al. 2021
Northern Patagonia, Argentina	H20	A	KX957714	Fonseca et al. 2019
Peru	H21	P	MZ920052, MZ920053, MZ920055, MZ920056-MZ920062, MZ920064-MZ920067	Mondragon-Martinez et al. 2021^*
Peru	H22	P	MZ920054, MZ920063	Mondragon-Martinez et al. 2021^*

*

Abbreviations used for isolates country: U1 – present study isolates from USA, U – USA, M – Mexico, B – Brazil, A – Argentina, P – Peru.

X-ray scan analysis provides insight into the hardened components, e.g., calcium, sulfur, and phosphorus, of acanthocephalan hooks. The EDXA appears to be species-specific, as in fingerprints. For example, EDXA is shown to have significant diagnostic value in acanthocephalan systematics. For example, Moniliformis cryptosaudi Amin, Heckmann, Sharifdini, Albayati, 2019 from Iraq is morphologically identical to Moniliformis saudi Amin, Heckmann, Mohammed, Evans, 2016 from Saudi Arabia, and it was erected based primarily on its distinctly different EDXA pattern (Amin et al., 2019) as a cryptic species. Our methodology for the detection of the chemical profile of hooks in the Acanthocephala has also been used in other parasitic groups including the Monogenea (Rubtsova et al., 2018, Rubtsova & Heckmann, 2019) and Cestoda (Rubtsova & Heckmann, 2020).

Biological significance of EDXA

The taxonomic identity of species is deep-seated at the genetic level which is expressed by the organism's morphology and biochemistry as revealed, in part, by its elemental spectra. Amin et al. (2022a,b,c,d) discussed in detail the biological significance of EDXA as a diagnostic tool exemplified by the observation that populations of an acanthocephalan species will consistently have similar EDXA spectra irrespective of host species or geography. Metal analysis of hooks has become a diagnostic standard since hooks have the highest level of elements compared to the mid- and posterior trunk regions of the acanthocephalan body (Heckmann et al., 2012). Specifically, the Sulfur content in the proboscis is paramount in the composition of disulfide bonds in the thiol groups for cysteine and cystine of the polymerized protein molecules (Stegman, 2005). The formed disulfide bonds are direct by-products of the DNA-based process of protein synthesis which makes up the identity of a biological species. Accordingly, the level of sulfur in our EDXA profiles will indicate the number of sulfur bonds that along with the levels of calcium phosphates, will characterize the elemental identity of a species based on its nuclear DNA personality. Variations in chemical compositions probably indicate differences in allele expression. The DNA-generated sulfide bonds evident in our EDXA profiles have an important role in the stability and rigid nature of the protein accounting for the high sulfur content of the proboscis (Heckmann et al., 2012). The above processes explain the observed species-specific nature of EDXA profiles noted in our many findings.

Molecular analysis

The present study contributes further continuation to the heteropolar geographical distribution for isolates of C. australe after the work of Lisitsyna et al. (2019) and García-Varela et al. (2021) having the novel information presented in the molecular study is the inclusion of cox1 sequences of C. australe from Peru. In the present study, a total of two partial 18S and Cox1 sequences were generated for C. australe. Newly generated 18S and Cox1 sequences of C. australe were very similar and show low intraspecific genetic divergence. The sequence for C. australe of Lisitsyna et al. (2019) and García-Varela et al. (2021) from the USA and Mexico revealed a robust relationship with the present study isolates showing genetic divergence ranging between 0.9 to 1.0 %. This result suggests that the above sequence from the USA and Mexico in comparison with other populations of C. australe exhibited the lowest divergence level and that they all belong to the Northern Hemisphere. Genetic divergence among the current study population with isolates from the Southern Hemisphere ranged from 1.8 to 3.0 %. The systematic position of the C. australe isolates in the phylogenetic tree strongly suggested that the isolates fit the similar evolutionary lineage and follow the same pattern in the haplotype network (Figs. 42 and 43). For that reason, molecular data used in the studies of acanthocephalans will make available valuable information about their diversity and population studies. Our study represents the new isolates clustered together, and displayed shared haplotypes, with isolates sequenced by Lisitsyna et al. (2019) and García-Varela et al. (2021). The haplotype network in the current study was constructed using Cox1 sequences of 46 specimens of C. australe from North and South American countries. The 46 sequences of C. australe were collapsed into 22 haplotypes and our haplotype network strongly comprised two clusters based in the Northern and Southern Hemispheres. The first (I) group related to the population of C. australe from North America that includes specimens from the USA and Mexico and the study of García-Varela et al. (2021) also supports the present analysis.

The second (II) group resembled populations from South America that comprises specimens from Peru, Argentina and Brazil. These data, in association with the phylogeny evidence, support the distinct population status of C. australe. Though, the distribution of specimens of C. australe population from different regions was in consensus in representing species group at the genetic level (Figs. 42 and 43). The newly generated sequences in the present study clustered within the first (I) group clade representing species of the USA and Mexico while the specimens from Peru, Argentina and Brazil appeared associated with the second (II) group clade and these relationships were also supported by the previous study of García-Varela et al. (2021).

In the present study, molecular data clearly represented the wide distribution of a single species that might be the leading step in further understanding the speciation and evolution of this species in the future.

Figuras y tablas

Chemical composition and localization of elements in hooks of Corynosoma australe from Zalophus californianus in California.

	Anterior hooks		Middle hooks					Posterior hooks

Element^*	Tip x-section	Middle	Longitudinal section	Tip x-section	Tip edge	Middle x-section	Middle edge	Tip x-section	Middle edge
Magnesium (Mg)	1.21	0.23–1.67^**	0.02–0.07	0.63	0.62	1.61	0.66	0.02	0.78–1.52
Sodium (Na)	0.25	0.00–0.04	0.00–0.03	0.00	0.03	0.08	0.00	0.02	0.05–0.07
Phosphorous (P)	9.95	15.74–18.71	12.78–20.35	10.64	11.00	21.32	16.10	2.82	14.91–20.49
Sulfur (S)	2.96	0.09–7.10	0.34–3.50	5.50	15.38	0.03	4.34	23.52	1.18–14.09
Calcium (Ca)	18.99	30.80–34.84	32.03–72.06	19.98	19.11	42.48	34.18	3.16	27.05–40.39

Chronological taxonomic history of Corynosoma australe from marine mammals, with special reference to ventral trunk spines in females.

Author	Host	Locality	Described as	Stage	Ventral spines
Johnston (1937)	Neophoca cinerea (Péron)	South Australia	C. australe	Adults	Discontinuous
Lincicome (1943)	Zalophus californianis (Lesson)	San Diego, California	C. obtuscens	Adults	Continuous
Van Cleave (1953)	Mycteroperca pardalis Gilbert	Mazatalán, Mexico	C. obtuscens	Cystacanth	Continuous
Morini & Boero (1960)	Otaria flavescence Shaw	Argentina	C. otariae	Adults	Discontinuous
Zdzitowiecki (1984)	Hydrurga leptonyx (Blainville)	South Shetlands, Antarctica	C. australe	Adults	25% continuous
Smales (1986)	Neophoca cinerea (Péron)Arctocephalus pusillatus Schreber	South Australia	C. australe	Adults (Figs. 10,11)	Discontinuous
Zdzitowiecki (1991)	Few “suitable” definitive & paratenic hosts	Antarctica	C. australe	Adults (Figs. 15 b, e)	Discontinuous
Sardella et al. (2005)	Arctocephalus australis (Zimmerman)Mirounga leonina (Linn.)Cynoscion guatucupa (Cuvier)	Argentina	C. australeC. australeC. australe	AdultsAdultsCystacanths	85–100% continuous85–100% continuous85–89% continuous
Aznar et al. (2012)	Otaria flavescens (Shaw)	Argentina	C. australe	Adults (Fig. 1B)	Discontinuous
Hernández-Orts et al. (2017a)	Spheniscus magellanicus (Foster)	Brazil	C. australe	Adults (Fig. 2B)Adults (Fig. 4B)	Continuous & 82–89% continuous
Lisitsyna et al. (2018)	Zalophus californianus (Lesson)	SausalitoCalifornia	C. obtuscens	Adults	Continuous
Lisitsyna et al. (2019)	Zalophus californianus (Lesson)	SausalitoCalifornia	C. obtuscens & C. australe	Adults	1% discontinuous
Present paper	Zalophus californianus (Lesson)	SausalitoCalifornia	C. australe	Adults	Continuous with post. constriction

List of acanthocephalan species used for phylogenetic analysis based on the mt Cox1 gene sequences. Newly generated sequences are presented in bold.

Species	Host	Host origin	GenBank accession nos.	References
Corynosoma australe	Zalophus californianus	USA	ON619618, ON614719	present study
	Zalophus californianus	USA	MK119245–MK119249	Lisitsyna et al., 2019
	Zalophus californianus	Mexico	MT676808–MT676818	García-Varela et al., 2020
	Merluccius hubbsi	Argentina	MT676819–MT676822	García-Varela et al., 2020
	Raneya brasiliensis	Argentina	MT676823–MT676824	García-Varela et al., 2020
	Paralichthys isosceles	Brazil	KU314822	Fonseca et al., 2019
	Stenella clymene	Argentina	MW724483	Hernández-Orts et al., 2021
	Arctocephalus australis	Argentina	MF497333	Hernández-Orts et al., 2017a
	Spheniscus magellanicus	Brazil	MF497335	Hernández-Orts et al., 2017a
	Otaria flavescens	Argentina	KX957714, MF497334	Hernández-Orts et al., 2017a, b
	Paralichthys adspersus	Peru	MZ920052–MZ920055	Mondragon-Martinez et al., 2021^*
	Paralabrax humeralis	Peru	MZ920056–MZ920059	Mondragon-Martinez et al., 2021^*
	Cheilodactylus variegatus	Peru	MZ920060–MZ920063	Mondragon-Martinez et al., 2021^*
	Otaria byronia	Peru	MZ920064–MZ920067	Mondragon-Martinez et al., 2021^*
Corynosoma hannae	Colistium guntheri	New Zealand	KX957724, KX957725	Hernández-Orts et al., 2017b
	Leucocarbo chalconotus	New Zealand	KX957718–KX957721, KX957723	Hernández-Orts et al., 2017b
	Phalacrocorax punctatus	New Zealand	KX957722	Hernández-Orts et al., 2017b
	Phocarctos hookeri	New Zealand	KX957715–KX957717, JX442191	Hernández-Orts et al., 2017b; García-Varela et al., 2013
	Peltorhamphus novaezeelandiae	New Zealand	KY909260–KY909263	Anglade & Randhawa, 2018
Corynosoma semerme	Halichoerus grypus	Germany	MF001277	Waindok et al., 2018
Corynosoma semerme	Callorhinus ursinus	USA	MK119253	Lisitsyna et al., 2019
Corynosoma obtuscens	Halichoerus grypus	New Zealand	JX442192	García-Varela et al., 2013
Corynosoma villosum	Callorhinus ursinus	USA	MK119251	Lisitsyna et al., 2019
Corynosoma validum	Callorhinus ursinus	USA	MK119252	Lisitsyna et al., 2019
Corynosoma enhydri	Enhydra lutris	USA	DQ089719	García-Varela & Nadler, 2006
Corynosoma magdaleni	Phoca vitulina	Germany	MF078642	Waindok et al., 2018
Corynosoma nortmeri	Phoca vitulina	Germany	MF001278	Waindok et al., 2018
Corynosoma strumosum	Phoca vitulina	USA	EF467870	García-Varela & Pérez-Ponce de León, 2008
	Pusa hispida botnica	Finland	EF467871	García-Varela & Pérez-Ponce de León, 2008
	Zalophus californianus	USA	MK119250	Lisitsyna et al., 2019
Bolbosoma balaenae	Balaenoptera physalus	Italy	MZ047281	Santoro et al., 2021
Bolbosoma turbinella	Eschrichtius robustus	USA	JX442189	García-Varela et al., 2013
Andracantha phalacrocoracis	Zalophus californianus	USA	MK119254	Lisitsyna et al., 2019
Hexaglandula corynosoma	Nyctanassa violacea	Mexico	EU189488	Guillén-Hernández et al., 2008
Pseudocorynosoma anatarium	Bucephala albeola	Mexico	KX688148	García-Varela et al., 2017
Pseudocorynosoma tepehuanesi	Oxyura jamaicensis	Mexico	KX688139	García-Varela et al., 2017
Polymorphus obtusus	Aythya affinis	Mexico	JX442195	García-Varela et al., 2013
Profilicollis bullocki	Emerita analoga	Mexico	JX442197	García-Varela et al., 2013
Profilicollis chasmagnathi	Oligosarcus jenynsii	Argentina	MT580124	Levy et al., 2020
Polymorphus trochus	Fulica americana	Mexico	JX442196	García-Varela et al., 2013

Data for the population of Corynosoma australe used in the haplotype networking using mt Cox1 gene. Asterisk shows sequences unpublished on NCBI database. Newly generated sequences are presented in bold.

Geographical Locality^*	Cox1Haplotype no.	ID in Fig. 46	GenBank accession nos.	References
Pacific coast near San Francisco, California, USA	H1	U1	ON619618, ON614719	Present study
Sausalito, California, USA	H2	U	MK119245-MK119249	Lisitsyna et al. 2019
Baja California, Mexico	H2	M	MT676816-MT676818	García-Varela et al. 2021
Rio de Janeiro, Brazil	H3	B	KU314822	Fonseca et al. 2019
Chubut, Argentina	H4	A	MW724483	Hernández-Orts et al. 2021
Baja California, Mexico	H5	M	MT676813	García-Varela et al. 2021
Sonora, Mexico	H6	M	MT676811	García-Varela et al. 2021
Baja California, Mexico	H7	M	MT676814	García-Varela et al. 2021
Sonora, Mexico	H8	M	MT676810	García-Varela et al. 2021
Northern Patagonia, Argentina	H9	A	MT676821	García-Varela et al. 2021
Sonora, Mexico	H10	M	MT676809	García-Varela et al. 2021
Baja California Sur, Mexico	H11	M	MT676808	García-Varela et al. 2021
Northern Patagonia, Argentina	H12	A	MT676823	García-Varela et al. 2021
Northern Patagonia, Argentina	H13	A	MT676819, MT676820, MT676822	García-Varela et al. 2021
Baja California, Mexico	H14	M	MT676815	García-Varela et al. 2021
Northern Patagonia, Argentina	H15	A	MT676824	García-Varela et al. 2021
Northern Patagonia, Argentina	H16	A	MF497333	Hernández-Orts et al. 2021
Baja California, Mexico	H17	M	MT676812	García-Varela et al. 2021
Rio de Janeiro, Brazil	H18	B	MF497335	Hernández-Orts et al. 2021
Northern Patagonia, Argentina	H19	A	MF497334	Hernández-Orts et al. 2021
Northern Patagonia, Argentina	H20	A	KX957714	Fonseca et al. 2019
Peru	H21	P	MZ920052, MZ920053, MZ920055, MZ920056-MZ920062, MZ920064-MZ920067	Mondragon-Martinez et al. 2021^*
Peru	H22	P	MZ920054, MZ920063	Mondragon-Martinez et al. 2021^*

Chemical composition of trunk spines and eggs of Corynosoma australe from Zalophus californianus in California.

Elements^*	Spines (longitudinal sections)			Eggs (cross sections)

	Anterior	Middle	Posterior	Edge (shell)	Center (acanthor)
Magnesium (Mg)	0.00	0.00	0.09	0.00	0.50
Sodium (Na)	0.00	0.00	0.00	0.00	0.00
Phosphorous (P)	1.39	0.00	1.16	0.91	7.73
Sulfur (S)	12.64	5.97	15.61	0	2.30
Calcium (Ca)	1.64	1.07	1.96	1.34	3.41

List of acanthocephalan species used for phylogenetic analysis based on the 18S rDNA gene sequences. Newly generated sequences are presented in bold, NA=host name not available.

Species	Host	Host origin	GenBank accession nos.	References
Corynosoma australe	Zalophus californianus	USA	ON614192, ON614199	present study
	Zalophus californianus	USA	MK119255	Lisitsyna et al., 2019
	Phocarctos hookeri	Mexico	JX442168	García-Varela et al., 2013
Corynosoma obtuscens	Callorhinus ursinus	Mexico	JX442169	García-Varela et al., 2013
Corynosoma validum	Callorhinus ursinus	Mexico	JX442170	García-Varela et al., 2013
Corynosoma enhydri	NA	USA	AF001837	Near et al., 1998
Corynosoma magdaleni	Phoca hispida botnica	Mexico	EU267803	García-Varela et al., 2009
Corynosoma strumosum	Phoca vitulina	Mexico	EU267804	García-Varela et al., 2009
Bolbosoma balaenae	Nyctiphanes couchii	Spain	JQ040306	Gregory et al., 2011^*
Bolbosoma turbinella	Eschrichtius robustus	Mexico	JX442166	García-Varela et al., 2013
Bolbosoma vasculosum	Lepturacanthus savala	Indonesia	JX014225	Verweyen et al., 2011
Andracantha gravida	Phalacrocorax auritus	Mexico	EU267802	García-Varela et al., 2009
Hexaglandula corynosoma	Nyctanassa violacea	Mexico	EU267808	García-Varela et al., 2009
Pseudocorynosoma anatarium	Bucephala albeola	Mexico	EU267801	García-Varela et al., 2009
Pseudocorynosoma constrictum	Anas clypeata	Mexico	EU267800	García-Varela et al., 2009
Profilicollis bullocki	Emerita analoga	Mexico	JX442174	García-Varela et al., 2013
Profilicollis botulus	Somateria mollissima	Mexico	EU267805	García-Varela et al., 2009
Polymorphus trochus	Fulica americana	Mexico	JX442196	García-Varela et al., 2013

Referencias

Amin, O.M. (2013): Classification of the Acanthocephala. Folia Parasitol, 60: 273 – 305. DOI: 10.14411/fp.2013.031 AminO.M. 2013 Classification of the Acanthocephala Folia Parasitol 60 273 305 10.14411/fp.2013.031 Abierto DOI Search in Google Scholar

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Helminthologia

Revision of Corynosoma australe Johnston, 1937 (Acanthocephala: Polymorphidae) from a North American population using novel SEM images, Energy Dispersive X-ray Analysis, and molecular analysis

O. M. Amin,O. M. Amin,A. Chaudhary,A. Chaudhary,H. S. Singh yH. S. Singh yT. KuzminaT. Kuzmina

Publicado en línea: 04 Jun 2023

Volumen & Edición: Volumen 60 (2023) - Edición 1 (March 2023)

Páginas: 1 - 27

Recibido: 03 Aug 2022

Aceptado: 14 Feb 2023

Detalles de publicación y publicación

Helminthologia

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Artículo

Figs. 1, 2.

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Fig. 40.

Fig. 41.

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Figuras y tablas

Figs. 1, 2.

Figs. 3–8.

Figs. 9–14.

Figs. 15–20.

Figs. 21–26.

Figs. 27–32.

Figs. 33–36.

Figs. 37–39.

Fig. 40.

Fig. 41.

Fig. 42.

Fig. 43.

Chemical composition and localization of elements in hooks of Corynosoma australe from Zalophus californianus in California.

Chronological taxonomic history of Corynosoma australe from marine mammals, with special reference to ventral trunk spines in females.

List of acanthocephalan species used for phylogenetic analysis based on the mt Cox1 gene sequences. Newly generated sequences are presented in bold.

Data for the population of Corynosoma australe used in the haplotype networking using mt Cox1 gene. Asterisk shows sequences unpublished on NCBI database. Newly generated sequences are presented in bold.

Chemical composition of trunk spines and eggs of Corynosoma australe from Zalophus californianus in California.

List of acanthocephalan species used for phylogenetic analysis based on the 18S rDNA gene sequences. Newly generated sequences are presented in bold, NA=host name not available.

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