Using DNA barcoding to relate cystacanths and adults of Corynosoma australe (Acanthocephala: Polymorphidae) of the Southeastern Pacific Ocean (Off Peru Coast)

doi:10.21203/rs.3.rs-2482271/v1

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Research Article

Using DNA barcoding to relate cystacanths and adults of Corynosoma australe (Acanthocephala: Polymorphidae) of the Southeastern Pacific Ocean (Off Peru Coast)

https://doi.org/10.21203/rs.3.rs-2482271/v1

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published 09 Jun, 2023

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The objective of this study is to use DNA barcoding to relate cystacanths and adults belonging to the acanthocephalans genus Corynosoma found in the southeastern Pacific Ocean off the coast of Peru. For this, we sampled three species of commercial fish (Paralichthys adspersus, Paralabrax humeralis and Cheilodactylus variegatus) and two South American sea lions Otaria byronia stranded on the beaches of the city of Huacho and Barranca, department of Lima. A total of 509 larvae were found in the body cavity of 95 fish (total prevalence 54.28%, total mean intensity 8.64), moreover, a total of 127 adults were found in the large intestine of two South American sea lion (P = 100%, MI = 63.5). We isolated 203 larvae of P. humeralis (P = 65.71%; MI = 8.83; MA = 5.8), 235 (P = 54.29%; MI = 12.37; MA = 6.71) of C. variegatus and 71 (P = 42.86%; MI = 4.73; MA = 2.03) of P. adspersus. All adult and larval specimens were morphologically identified as Corynosoma sp. We performed phylogenetic analysis and generated cytochrome c oxidase subunit 1 (cox1) gene sequences that were compared with sequences available from GenBank. Likewise, using maximum likelihood (ML) and Bayesian inference (BI) revealed that the 16 new sequences (four adults and twelve larvae) were grouped into a clade formed by Corynosoma australe. Therefore, our results contribute to broaden the range of paratenic hosts as well as to record the presence of C. australe in the definitive host. In addition, it is the first analysis that confirms the presence of C. australe using DNA barcoding, allowing its geographical distribution to be extended to the Southeast Pacific Ocean off the coast of Peru.

Acanthocephala

Corynosoma

DNA barcoding

pinnipeds

fishes

Peru

About 40 species of the genus Corynosoma Lühe, have been recorded worldwide (García-Varela et al. 2021), with C. australe having the greatest range in the southern hemisphere from South Australia, Antarctica, South Africa, South America (Zdzitowiecki 1984; Aznar et al. 2012; Ionita et al. 2008; Hernandez-Orts et al. 2017; Lisitsyna et al. 2018) and most recently reported in North America. (United States of America and Mexico) (García-Varela et al. 2021). Corynosoma species generally use pinnipeds as their definitive host, but they have also been found parasitizing cetaceans and waterfowl. (Sardella et al. 2005; Aznar et al. 2012; Hernández-Orts et al. 2017; Lisitsyna et al. 2018). The complete life cycle comprises benthic amphipods as intermediate hosts (Hoberg 1986; Sinisalo and Valtonen 2003) and a wide range of fish as potential paratenic hosts (Valtonen 1983; Laskowski and Zdzitowiecki 2005; Sasaki et al. 2019). In addition, Corynosoma has been reported to naturally infect terrestrial mammals, considered accidental hosts (Noronha 1988; Cabrera et al. 1990; Tantaleán et al. 2007).

In the Peruvian sea, cystacanths of the genus Corynosoma have been reported morphologically characterized in various fish of commercial importance (Tantaleán et al. 2005; Chero et al. 2014; Iannacone et al. 2015; Minaya et al. 2016), also in the South American sea lion Otaria byronia (Tantaleán 1993; Cabrera et al. 1994; Naupay et al. 2019). Evidence from a study of controlled infections in experimental hosts in Peru showed the process of development from juveniles to adults that reached full sexual maturity with oviposition, registering Corynosoma obtuscens (now syn. C. australe) as a parasite of great infective capacity and non-specific for the definitive host (Castro and Martínez 2002), likewise, it has been recorded in terrestrial mammals (Cabrera et al. 1999; Castro et al. 2004; Tantaleán et al. 2007; Acosta et al. 2015) and reproductive adults of C. australe have been reported in the Magellanic penguin Spheniscus magellanicus in Brazil, as a new avian host. (Hernández-Orts et al. 2017). In the present study, we used morphological data and the first analysis using DNA barcoding to confirm the identification of cystacanths and adults of Corynosoma australe present in the southeastern Pacific Ocean off the coast of Peru where we expanded its geographic distribution for the southern hemisphere of America and recorded new commercially important paratenic hosts.

Sample collection

Between January and March 2018, 95 specimens of three commercial fish species were examined, Paralichthys adspersus (length 34.83 ± 2.32 cm; weight: 325.78 ± 54.7 g), Paralabrax humeralis (length 39.17 ± 2.6 cm; weight 459.2 ± 45.2 g) and Cheilodactylus variegatus (length: 33 ± 2.7 cm; 315.5 ± 34.15 g) off the coast of the Peruvian Sea (Chorrillos, Lima, 12° 9'57.59’’S 77° 1'46.3’’O). Specimens were examined in fresh conditions in the laboratory of Parasitology in Wildlife and Zoonosis of “Universidad Nacional Mayor de San Marcos”, fishes were identified according to Chirichigno and Cornejo (2001).

In 2015, another research project had already collected acanthocephalans from two stranded specimens of O. byronia stranded on the beaches of Huacho (11° 06' S and 77° 36' W) and Barranca (10° 45' S and 77° 46' W), department of Lima.

Parasitological examination

A total of 509 cystacanths, mostly alive, were found encysted on the serosal surface of the intestine, stomach, and body cavity of P. adpersus, P. humeralis and C. variegatus, removed from their capsule and repeatedly washed in 0.9% saline solution and morphologically identified at genus level by optical microscope (Leica EZ4, Germany) following Sardella et al. (2005). Some cystacanths larvae were fixed and stored in 2 ml tubes with 70% alcohol for molecular analysis, furthermore, larvae and adults were fixed in 2.5% glutaraldehyde to be analyzed under the scanning electron microscope (SEM). The ethanol-preserved adult samples contained 127 acanthocephalan specimens that were used in this study to perform previous morphological descriptions (Zdzitowiecki, 1984; Serdella et al. 2005; Lisitsyna et al. 2019; García-Varela et al. 2021).

Molecular identification

DNA was extracted with the DNeasy tissue Kit (Qiagen, Chatsworth, California, USA), DNA quality and quantity was verified in a spectrophotometer Nanodrop®ND-2000 (Thermo Scientific). The primers used were CORY-COIF 5´ AGTTCTAATCATAARGATATYGG-3´ (Nadler et al., 2006) and CORY-COIR 5´TAAACTTCAGGGTGACCAAAAAATCA-3´ (Folmer et al. 1994). The locus was amplified by PCR in a Veriti™ 96-well thermocycler (Applied Biosystems, California, USA) with a final volume of 50 µL, including 5 µL of genomic DNA. The reaction mixture contained 2.5 U/µl Taq polymerase (Hot Star Taq DNA Polymerase Qiagen Kit, Hilden, Germany), and 0.5 µM of each primer (Macrogen, South Korea). The amplification condition was optimized as follows: one cycle at 94°C for 3 min; 35 cycles of 94°C for 1 min, 40°C for 60 sec, 72°C for 1 min, and a final cycle of 72°C for 5 min; storage at 4˚C. Amplied fragments were visualized on agarose gel (1.5%) detected by the gel documentation system (ENDURO™ GDS Touch, USA) and fragment sizes were determined by comparison with a GeneRuler Express DNA Ladder marker (#SM 1551, Thermo Scientific). The PCR products were sent to Macrogen Inc. (Seoul, South Korea) for purification and sequencing. The PCR primers were used for sequencing. Nucleotide sequences obtained by PCR were subjected to known sequences by BLAST search. (http://blast.ncbi.nlm.nih.gov/Blast.cgi). All sequences have been deposited in Genbank data set (Table 1).

Table 1

List of species used in the phylogenetic analyses, with data on the life-cycle stage, host locality and GenBank accession number for sequences mitochondrial cytochrome c oxidase subunit 1 (*cox*1) gene. Abbreviations: A, adult; C, cystacanth.
Species	Stage	Locality
OUTGROUP
Andracantha phalacrocoracis	C	Japón: Hokkaido, Nemuro	Osmerus dentex	LC465354	Sasaki et al. 2019
Andracantha sigma	A	New Zealand	Phalacrocorax punctatus	MF527035	Presswell et al. 2017
INGROUP
Corynosoma villosum	A	USA: Alaska, isla St. Paul	Callorhinus ursinus	MK119251	Lisitsyna et al. 2018
Corynosoma villosum	C	Japan: Hokkaido, Hamatonbetsu	Platichthys stellatus	LC465388	Sasaki et al. 2019
Corynosoma validum	A	USA: Alaska, isla St. Paul	Callorhinus ursinus	JX442193	García-Varela et al. 2013
Corynosoma validum	A	USA: Alaska, isla St. Paul	Callorhinus ursinus	MK119252	Lisitsyna et al. 2018
Corynosoma enhydri	A	USA: Monterey Bay, California	Enhydra lutris	DQ089719	García-Varela and Nadler, 2006
Corynosoma magdaleni	A	Baltic Sea	Phoca vitulina	MF078642	Waindok et al. 2018
Corynosoma magdaleni	A	Lake Saimaa, Finland	Phoca hispida saimensis	EF467872	García-Varela et al. 2006
Corynosoma strumosum	A	USA: California, Sausalito	Zalophus californianus	MK119250	Lisitsyna et al. 2018
Corynosoma strumosum	A	Japan: Hokkaido, Erimo	Phoca vitulina	LC465394	Sasaki et al. 2019
Corynosoma semerme	C	Japan: Hokkaido, Nemuro	Osmerus dentex	LC465392	Sasaki et al. 2029
Corynosoma semerme	A	USA: Alaska, isla St. Paul	Callorhinus ursinus	MK119253	Lisitsyna et al. 2018
Corynosoma obtuscens	A	USA: Alaska, isla St. Paul	Callorhinus ursinus	JX442192	García-Varela et al. 2013
Corynosoma hannae	C	New Zealand: Kaka Point, Otago	Peltorhamphus novaezeelandiae	KX957726	Hernandez-Orts et al. 2016
Corynosoma hannae	C	New Zealand: Kaka Point, Otago	Colistium guntheri	KY909263	Anglade and Randhawa, 2017
Corynosoma australe	A	Mexico: Isla Guadalupe, Baja California Norte	Zalophus californianus	MT676814	Garcia-Varela et al. 2020
Corynosoma australe	A	Mexico: Isla Guadalupe, Baja California Norte	Zalophus californianus	MT676815	Garcia-Varela et al. 2020
Corynosoma australe	A	Mexico: Isla San Pedro Nolasco, Sonora	Zalophus californianus	MT676809	Garcia-Varela et al. 2020
Corynosoma australe	A	Mexico: Isla San Pedro Nolasco, Sonora	Zalophus californianus	MT676811	Garcia-Varela et al. 2020
Corynosoma australe	A	USA: California, Sausalito	Zalophus californianus	MK119249	Lisitsyna et al. 2018
Corynosoma australe	A	Mexico: Isla Guadalupe, Baja California Norte	Zalophus californianus	MT676813	Garcia-Varela et al. 2020
Corynosoma australe	A	Brazil: Rio de Janeiro	Spheniscus magellanicus	MF497335	Hernandez-Orts et al.2017
Corynosoma australe	A	Brazil: Rio de Janeiro	Spheniscus magellanicus	MF497334	Hernandez-Orts et al.2017
Corynosoma australe	C	Argentina	Raneya brasiliensis	MT676823	Garcia-Varela et al. 2020
Corynosoma australe	C	Argentina: Golfo de San Matias	Merluccius hubbsi	MT676821	Garcia-Varela et al. 2020
Corynosoma australe	C	Argentina	Raneya brasiliensis	MT676824	Garcia-Varela et al. 2020
Corynosoma australe	C	Peru: Lima	Paralichthys adspersus	MZ920052	This study
Corynosoma australe	C	Peru: Lima	Paralichthys adspersus	MZ920053	This study
Corynosoma australe	C	Peru: Lima	Paralichthys adspersus	MZ920054	This study
Corynosoma australe	C	Peru: Lima	Paralichthys adspersus	MZ920055	This study
Corynosoma australe	C	Peru: Lima	Paralabrax humeralis	MZ920056	This study
Corynosoma australe	C	Peru: Lima	Paralabrax humeralis	MZ920057	This study
Corynosoma australe	C	Peru: Lima	Paralabrax humeralis	MZ920058	This study
Corynosoma australe	C	Peru: Lima	Paralabrax humeralis	MZ920059	This study
Corynosoma australe	C	Peru: Lima	Cheilodactylus variegatus	MZ920060	This study
Corynosoma australe	C	Peru: Lima	Cheilodactylus variegatus	MZ920061	This study
Corynosoma australe	C	Peru: Lima	Cheilodactylus variegatus	MZ920062	This study
Corynosoma australe	C	Peru: Lima	Cheilodactylus variegatus	MZ920063	This study
Corynosoma australe	A	Peru: Lima	Otaria byronia	MZ920064	This study
Corynosoma australe	A	Peru: Lima	Otaria byronia	MZ920065	This study
Corynosoma australe	A	Peru: Lima	Otaria byronia	MZ920066	This study
Corynosoma australe	A	Peru: Lima	Otaria byronia	MZ920067	This study

Phylogenetic analyses

The sequences obtained were assembled and edited in the ChromasPro version 2.0.1 (Technelysium Pty Ltd., South Brisbane, Queensland, Australia). Generated contigs were compared with sequences available for species of the genus Corynosoma. Two members of the genus Andracantha Schmidt, 1975, A. sigma Presswell, García-Varela & Smales, 2017 and A. phalacrocoracis (Yamaguti, 1939), were chosen as outgroups according to Lisitsyna et al. 2018. The alignment was obtained using the ClustalW method implemented in the MEGA version X program (Kumar et al. 2018). The resulting alignment was also corrected (removing misaligned positions and divergent regions) and trimmed using Gblock web server (http://phylogeny.lirmm.fr/; Dereeper et al. 2008), with adjustments for less stringent parameters.

Phylogenetic reconstructions were performed using Bayesian inference (BI) and maximum likelihood (ML) algorithms. The best nucleotide substitution model, HKY + G + I, was selected according to Bayesian information criterion. ML analysis was performed using MEGA X and nodal supports were inferred based on 1000 bootstrap replicates. The BI analysis was conducted using Mr. Bayes v.3.2.6 (Ronquist et al. 2012), running two independent Markov Chain Monte Carlo runs of four chains setting for 1,000,000 generations and sampling every 100 generations. The first 25% of the trees sampled were discarded as “burn-in”, and consensus topology and posterior probability values were calculated from the remaining trees and visualized in FigTree v. 1.4.3 (http://tree.bio.ed.ac.uk/software/fgtree/). Uncorrected p distances were calculated using MEGA X.

Parameters of parasitological analyses

Descriptors quantitative of parasite infection such as prevalence (P%), mean intensity (MI) and mean abundance (MA) were calculated using the software Quantitative Parasitology 3.0 (Reiczigel and Rózsa 2005). Sterne's exact test was used at 95% confidence limits for prevalence. To compare MI and MA, the bootstrap procedure was applied with 1000 replications at the 95% confidence interval. Differences were considered significant when p < 0.05.

Morphological analysis

All the larval stage collected from P. adspersus, P. humeralis and C. variegatus were morphologically characterized as Corynosoma sp. We observed 30 larvae has a thick and short trunk with length 1950 ± 200 µm and SEM showed the presence of cylindrical proboscis is 560 ± 40 µm long and 195 ± 15 µm wide, armed with 18–20 longitudinal rows consisting of 12–14 hooks per each row, like also, tegumental spines in the body (Fig. 1). The adult stage collected from South American sea lions O. byronia, were examined in this study and exhibited similarity morphological characteristics like cystacanths, but with larger morphometrics. We observed that 30 adults have a thick trunk with length 2300 ± 200 µm and SEM showed the presence of cylindrical proboscis is almost of same size as cystacanths with 2–4 spiniform hooks, 17–19 hook rows, 11–14 hooks per row and 8–11 rooted hooks (Fig. 2).

Molecular Identification and phylogenetic analyses

The amplification of 16 partial sequences of cox1 (524 bp) were obtained for C. australe from paratenics hosts (C. variegatus, P. humeralis and P. adspersus) and definitive host (O. byronia) from the coast of Peru. The newly generated sequences were 100% identical, with the exception of two isolates (MZ920054, MZ920063), which detected 0.4% genetic divergence. The phylogenetic trees based on cox1 sequences performed by ML and BI were almost identical, with a better resolution in the ML reconstruction. The isolates of the present study are nested in a strongly supported clade with other isolates of C. australe and this species appears as a sister taxon of Corynosoma hannae (Fig. 3). The differences between groups of isolates of C. australe were evidenced with the uncorrected p-distance. The genetic divergence between Peruvian sequences of C. australe and other registered in the American continent ranged from 1.3 to 3.8% (Table 2). In ML tree was recovered a clade formed by Peruvian isolates, separated from isolates registered in other countries (Argentina, Brazil, Mexico, United States). The reference sequences and newly generated sequences deposited in GenBank are summarized in Table 1.

Table 2. Uncorrected p-distance (%) between cox1 sequences of Corynosoma australe from Peru and other American countries.

Corynosoma australe isolates			Corynosoma australe Peru
Corynosoma australe isolates			MZ920052-53, MZ920055-62, MZ920064-67	MZ920054, MZ920063
	Peru
	-	MZ920052-53, MZ920055-62, MZ920064-67	0	0.4
	-	MZ920054, MZ920063	0.4	0
	Argentina		1.3-1.9	1.7-2.3
	Brazil		2.1	2.1
	Mexico		3.4	3.8
	USA		2.3	2.7

Ecological analysis

A total of 509 cystacanths larvae were found in 95 fish (total prevalence 54.28%, total mean intensity 8.64). After morphological analysis and molecular identification, all cystacanths larvae isolated were identified as C. australe. The hosts examined during 2018, presented the following ecological indices: P. humeralis (P = 65.71%; MI = 8.83; MA = 5.8), C. variegatus (P = 54.29%; MI = 12.37; MA = 6.71) and P. adspersus (P = 42.86%; MI = 4.73; MA = 2.03), in addition, the intensity and mean abundance was significantly higher in C. variegatus than in the other hosts.

In this study, we report for the first-time using DNA barcoding the presence of cystacanths larvae and adults of Corynosoma australe obtained from three different commercial fish species (P. humeralis, P. adspersus and C. variegatus) and from South American sea lions (O. byronia) from the Southeast Pacific Ocean off Peru. This parasite turned out to be the only dominant acanthocephalan isolated from the intestine, stomach, and body cavity of paratenic hosts. The elucidation of C. australe in P. adspersus, P. humeralis and C. variegatus represent new host records for this species of parasite and expands its distribution range in Peruvian sea waters. Studies carried on more than 20 species of marine teleost fishes located in the waters of the southwestern Atlantic Ocean (off the coasts of Argentina and Brazil) recorded cystacanths of C. australe (Santos et al. 2008; Hernández-Orts et al. 2019a; Hernández-Orts et al. 2019b). Similarly, for the southeastern Pacific Ocean (off the coasts of Peru and Chile) they have recorded Corynosoma spp. morphologically characterized in more than 40 species of marine teleost fishes (Tantaleán et al. 2005; Muñoz and Olmos 2008; Chero et al. 2014; Chero et al. 2016). Our molecular data confirmed the phylogenetic relationship of cystacanths larvae and adults strongly supported in a clade together with C. australe sequences from the northern and southern hemisphere of the Americas (García-Varela et al. 2021), as well as coincided with previously inferred phylogenies consistent with those of Hernández-Orts et al. (2017) and Lisitsyna et al. (2019). A recent study explored the genetic diversity of C. australe specimens isolated from otariids of the northern hemisphere (United States of America and Mexico) and southern hemisphere (Argentina and Brazil), where the low level of genetic divergence found among specimens from the same species (Garcia-Valera et al. 2021), furthermore, to support the synonymy between C. obtuscens and C. australe, data from cox1 sequences were compared and a low genetic divergence (1.1–1.6%) was evidenced. which corresponds to the intraspecific level (Lisitsyna et al. 2019). Similarly, we obtained the genetic divergence between Peruvian sequences of C. australe and other registered in the American continent ranged from 1.3 to 3.8%. In addition, they recorded the presence of C. australe in Magellanic penguins in the southern hemisphere (Brazil) but with lower levels of infection than in otariid definitive hosts (Hernández-Orts et al. 2017a).

Genetic/molecular markers based on mitochondrial DNA allow discriminating morphologically indistinguishable species and linking the different developmental stages of a species (Hebert and Gregory 2005). Lisitsyna et al. (2018), demonstrated that C. obtuscens is synonymous with C. australe by morphological and molecular analysis using the cox1 marker, and showed that C. australe appears to be the only species of the genus Corynosoma that parasitizes pinnipeds in both hemispheres. Specimens of Corynosoma spp. have been frequently studied using the cox1 gene (García-Varela and Nadler 2006; García-Varela and Pérez-Ponce de León 2008; García-Varela et al. 2013; Hernández-Orts et al. 2017a, b; Lisitsyna et al. 2018; Sasaki et al. 2019; García-Varela et al. 2021), thus, we provide in this study the first consistent molecular data through analysis of the cox1 mtDNA sequence and identify C. australe in the two stages of the biological cycle. The paratenic hosts of the present study are not recorded in the diet of South American sea lions in the Peruvian Sea, which is basically composed of Engraulis ringens, Normanichthys crockeri y Merluccius gayi (Zavalaga et al. 1998; Arias-Schreiber 2000), however, C. obtuscens has been reported M. gayi, Sarda chiliensis, Cilus gilberti y Cynoscion analis in very low prevalence (Chero et al. 2014a; Chero et al. 2014b; Chero et al. 2016; Minaya et al. 2016) for the central Peruvian Sea. In addition, a study of the parasitic community in Isacia conceptionis reported C. obtuscens (now C. australe) as one of the species with the highest prevalence and mean abundance (Iannacone et al. 2015). In the present study, we recorded C. australe with a higher prevalence in P. humeralis but C. variegatus presented the highest abundance and mean intensity. The results obtained contribute to improve the knowledge in different biological aspects such as the mapping of the definitive and paratenic host association, tropic ecology, occurrence, and systematic position of C. australe, considering account the wide range of commercial fish present in the Peruvian sea, there is a possibility that corynosomiasis, considered a minor parasitic zoonosis, occurs in Peru.

Acknowledgments The present study is supported by Faculty of Biological Sciences, National University of San Marcos, Peru. The authors extend their appreciations to members of Biomedical Sciences Research Institute,Universidad Ricardo Palma, Peru, Laboratory of Parasitology in helping to complete this study.

Author contribution Aarón Mondragón-Martínez (AMM), Rosa Martínez-Rojas (RMR) and Eduardo A. Pulido-Murillo (EDPM): designed the study. AMM, RMM, Martín Dávila-Rios (MDR) and Estrellita Rojas De-Los-Santos (ERS): field work. MDR, Miguel Dávila-Robles (MDR) and Juan C. Ramos-Gorbeña (JCRG): performed laboratory analyses. Lidia Cruz-Neyra (LCN), RMR and J.R Sanchez-Venegas (JRSV): performed statistical analyses. EDPM and Enrique Garcia-Candela (EGC): performed bioinformatics analyses. AMM, EDPM and EGC: prepared figures 1 - 3 and tables 1 - 2. AMM, RMR, MDR and LCN: wrote the first draft of the manuscript. All authors revised the manuscript. All authors read and approved the final version of the manuscript.

Funding We want to thank UNMSM for financing the project with internal funds with R.R. 05753-R-21 and code B21102151 and Universidad Ricardo Palma (URP) for financing.

Data availability The obtained sequences are deposited in GenBank under the accession numbers MZ920052-MZ920067.

Ethics approval This study was performed in agreement with the recommendations of all applicable institutional, national and international guidelines for the care and use of animals. The responsible conduct of the research was approved by the university council N° 0689-2020 of the “Universidad Ricardo Palma”.

Consent to participate Not applicable.

Consent for publication All the authors provided their consent for the publication of this manuscript.

Conflicts of interest The authors declare that they have no competing interests.

Acosta M, Tantaleán M, Serrano-Martínez E (2015) Identificación de parásitos gastrointestinales por coproscopía en carnívoros silvestres del Zoológico Parque de las Leyendas, Lima, Perú. Rev investig vet Perú 26(2): 282-290
Arias-Schreiber M (2000) Los lobos marinos y su relación con la abundancia de la anchoveta peruana durante 1979-2000. Bol Instit Mar Perú 19 (1-2): 133-138
Aznar FJ, Hernández-Orts J, Suárez AA, García-Varela M, Raga JA, Cappozzo HL (2012) Assessing hostparasite specificity through coprological analysis: a case study with species of Corynosoma (Acanthocephala: Polymorphidae) from marine mammals. J Helminthol 86: 156–164
Cabrera R, Coronado C, Ampuero S (1994) Parásitos de Otáridos de la costa peruana y su importancia sanitaria. Bol de Lima 16 (91-96): 77- 80
Cabrera R, Rojas R, Davalos M (1999) Corynosoma obtuscens Lincicome, 1943 (Acanthocephala: Polymorphidae) in Canis familiaris de la Ciudad de Chincha, Peru. Parasitol Día 23: 59–62
Castro M, Martínez R (2004) Proceso del desarrollo de Corynosoma obtuscens (Acanthocephala: Polymorphidae) en Canis familiaris y su posible implicancia en salud publica. Parasitol Latinoam 59: 26–30
Chero J, Cruces C, Iannacone J, Sáez G, Alvariño L, Rodríguez C, Rodríguez H, Tuesta E, Pacheco A, Huamani N (2014a) Índices parasitológicos de la merluza peruana Merluccius gayi peruanus (Ginsburg, 1954) (Perciformes: Merlucciidae) adquiridos del terminal pesquero de Ventanilla, Callao, Perú. Neotrop Helminthol 8:1
Chero J, Iannacone J, Cruces C, Sáez G, Alvariño L (2014b) Comunidad de metazoos parásitos de la corvina Cilus gilberti (Abbott, 1899) (Perciformes: Sciaenidae) en la zona costera de Chorrillos, Lima, Perú. Neotrop Helminthol 8:1
Chero J, Sáez G, Iannacone J, Cruces C, Alvariño L, Luque J (2016) Ecología comunitaria de metazoos parásitos del bonito Sarda chiliensis Cuvier, 1832 (Perciformes: Scombridae) de la costa peruana. Rev investig vet Perú 27(3): 539-555
Chirichigno N, Cornejo RM (2001) Catálogo comentado de los peces marinos del Perú. Callao, Perú: Instit del Mar del Perú
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic acids res 36(suppl 2): 465-469
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3: 294–299
García-Varela M, Nadler SA (2006) Phylogenetic relationships among Syndermata inferred from nuclear and mitochondrial gene sequences. Mol Phylogenet Evol 40: 61–72
García-Varela M, Pérez-Ponce de León G (2008) Validating the systematic position of Profilicollis Meyer, 1931 and Hexaglandula Petrochenko, 1950 (Acanthocephala: Polymorphidae) using cytochrome c oxidase (cox 1). J Parasitol 94: 212–217
García-Varela M, Masper A, Crespo EA, Hernández-Orts JS (2021) Genetic diversity and phylogeography of Corynosoma australe Johnston, 1937 (Acanthocephala: Polymorphidae), an endoparasite of otariids from the Americas in the northern and southern hemispheres. Parasitol Int 80: 102205
Hebert PD, Gregory TR (2005) The promise of DNA barcoding for taxonomy. Syst Biol 54: 852–859
Hernandez-Orts JS, Brandão M, Georgieva S, Raga JA, Crespo EA, Luque JL, Aznar F J (2017a) From mammals back to birds: Host-switch of the acanthocephalan Corynosoma australe from pinnipeds to the Magellanic penguin Spheniscus magellanicus. PLoS One, 12(10): e0183809
Hernández-Orts JS, Smales LR, Pinacho-Pinacho CD, García-Varela M, Presswell B (2017b) Novel morphological and molecular data for Corynosoma hannae Zdzitowiecki, 1984 (Acanthocephala: Polymorphidae) from teleosts, fish-eating birds and pinnipeds from New Zealand, Parasitol Int 66: 905–916
Hernández-Orts JS, Alama-Bermejo G, García NA, Crespo EA, Montero FE, Raga JA, Aznar FJ (2019a) Acanthocephalans from marine fishes from Patagonia, Argentina. J Parasitol 105(1): 162-169
Hernández-Orts JS, Montero FE, García NA, Crespo EA, Raga JA, García-Varela M, Aznar FJ (2019b) Transmission of Corynosoma australe (Acanthocephala: Polymorphidae) from fishes to South American sea lions Otaria flavescens in Patagonia, Argentina. Parasitol res 118(2): 433-440
Iannacone J, Alvariño L, Chero J, Sáez G (2015) Comunidad Parasitaria de Cabinza Isacia conceptionis (Cuvier & Valenciennes, 1830) (Perciformes: Haemulidae) en la Zona de Chorrillos, Lima, Perú. Rev de Investig Vet del Perú 26(1): 96-110
Ionita M, Varela MG, Lyons ET, Spraker TR, Tolliver SC (2008) Hookworms (Uncinaria lucasi) and acanthocephalans (Corynosoma spp. and Bolbosoma spp.) found in dead northern fur seals (Callorhinus ursinus) on St. Paul Island, Alaska in 2007. Parasitol Res 103: 1025–1029
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol biol evol 35(6): 1547
Laskowski Z, Zdzitowiecki K (2005) The helminth fauna of some notothenioid fishes collected from the shelf of argentine islands, West Antarctica, Polar Res 26: 315–324
Minaya D, Chero J, Sáez G, Rodriguez L, Sandoval M, Alvariño L, Iannacone J (2016) Comunidad de parásitos de “Cachema” Cynoscion analis (Jenyns, 1842) (Perciformes: Sciaenidae) en el Pacífico Oriental. Neotrop Helminthol 10(1)
Muñoz G, Olmos V (2008) Revisión bibliográfica de especies endoparásitas y hospedadoras de sistemas acuáticos de Chile. Rev biol mar oceanogr 43(2): 173-245
Lisitsyna OI, Kudlai O, Spraker TR, Kuzmina TA (2018) New records on acanthocephalans from California sea lions Zalophus californianus (Pinnipedia: Otariidae) from California, USA. Vestn Zool 52: 181–192.
Lisitsyna OI, Kudlai O, Spraker TR, Tkach VV, Smales LR, Kuzmina TA (2019) Morphological and molecular evidence for synonymy of Corynosoma obtuscens Lincicome, 1943 with Corynosoma australe Johnston, 1937 (Acanthocephala: Polymorphidae). Syst Parasitol 96(1): 95-110.
Naupay A, Castro J, Rojas V, Suarez D (2019) Helmintos gastrointestinales de Otaria flavescens Shaw 1800 (Mammalia: Otariidae) león marino sudamericano de la costa central del Perú. Neotrop Helminthol 13(2)
Noronha D (1988) Corynosoma clementei Giovannoni y Fernandes, 1965 y su sinónimo Corynosoma seropedicus Machado Filho, 1970, un parásito accidental de Canis familiaris L., 1758. Arq Flum Med Vet 3:119–120
Reiczigel J, Rózsa L (2005) Quantitative Parasitology 3.0 Budapest. Distributed by the authors
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Bret Larget, Liang Liu, Marc A Suchard, John P Huelsenbeck (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst biol 61(3): 539-542
Santos CP, Gibson DI, Tavares LE, Luque JL (2008) Checklist of Acanthocephala associated with the fishes of Brazil. Zootaxa 1938(1): 1-22
Sardella NH, Mattiucci S, Timi JT, Bastida RO, Rodrıguez DH, Nascetti G (2005) Corynosoma australe Johnston, 1937 and C. cetaceum Johnston & Best, 1942 (Acanthocephala: Polymorphidae) from marine mammals and fishes in Argentinian waters: allozyme markers and taxonomic status. Syst Parasitol 61: 143–156.
Sasaki M, Katahira H, Kobayashi M, Kuramochi T, Matsubara H, Nakao M (2019) Infection status of commercial fish with cystacanth larvae of the genus Corynosoma (Acanthocephala: Polymorphidae) in Hokkaido, Japan. Int J Food Microbiol 305: 108256
Sinisalo T, Valtonen ET (2003) Corynosoma acanthocephalans in their paratenic fish hosts in the northern Baltic Sea. Parasite 10:227–233
Tantaleán VM (1993) Algunos helmintos de mamíferos marinos del Perú y su importancia médica. Rev peru med trop 67-71
Tantaleán M, Sánchez L, Gómez L, Huiza A (2005) Acantocéfalos del Perú. Rev peru biol 12(1): 83-92
Valtonen ET, Niinimaa A (1983) Dispersion and frequency distribution of Corynosomas pp. (Acanthocephala) in the fish of the Bothnian Bay, Aquilo Ser. Zool 22: 1–11
Zavalaga C, Paredes R, Arias-Schreiber M (1998) Dieta del lobo fino Arctocepbatus australis y el lobo chusco Otaria byronia en la costa sur del Perú en febrero de 1998. lnf Prog Inst Mar Perú 79:3-16
Zdzitowiecki K (1984) Some antarctic acanthocephalans of the genus Corynosoma parasitizing Pinnipedia, with descriptions of three new species. Acta Parasitol 29: 359–377

No competing interests reported.

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Using DNA barcoding to relate cystacanths and adults of Corynosoma australe (Acanthocephala: Polymorphidae) of the Southeastern Pacific Ocean (Off Peru Coast)

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Abstract

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Introduction

Material And Methods

Sample collection

Parasitological examination

Molecular identification

Phylogenetic analyses

Parameters of parasitological analyses

Results

Morphological analysis

Molecular Identification and phylogenetic analyses

Ecological analysis

Discussion

Declarations

References

Additional Declarations

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