Morphological identification of Skrjabinisakis Mozgovoi, 1951 (Nematoda: Anisakidae) in Kogia sima (Cetacea: Kogiidae) from Brazilian waters

Identificação morfológica de Skrjabinisakis Mozgovoi, 1951 (Nematoda: Anisakidae) em Kogia sima (Cetacea: Kogiidae) em águas brasileiras

Abstract

New morphological, morphometric and scanning electron microscopy data of a nematode of the family Anisakidae, recovered from a specimen of Kogia sima, a cetacean that died off the northern coast of Brazil, are presented in this paper. Morphological features such as the violin-shaped ventricle and short and equal spicules, as well as the distribution of post-cloacal papillae and specificity for the definitive host (Kogiidae cetaceans) demonstrate similarity to Skrjabinisakis paggiae. This research records Kogia sima and S. paggiae on the estuarine coast of Pará, northern Brazil.

Keywords:
Nematode; parasite; dwarf sperm whale; Amazon estuary

Resumo

São apresentados, neste trabalho, novos dados morfológicos, morfométricos e de microscopia eletrônica de varredura de um nematoide da família Anisakidae, recuperado de Kogia sima, um cetáceo que veio a óbito na costa norte do Brasil. Características morfológicas, como o ventrículo em forma de violino, espículos curtos e iguais, além da distribuição de papilas pós-cloacais e especificidade pelo hospedeiro definitivo (cetáceos Kogiidae) demonstram similaridade a Skrjabinisakis paggiae. Esta pesquisa registra Kogia sima e S. paggiae na costa estuarina paraense, norte do Brasil.

Palavras-chave:
Nematoide; parasito; cachalote anão; estuário amazônico

Introduction

The systematics and nomenclature of Anisakidae Railliet & Henry, 1912 nematodes belonging to the genus Anisakis Dujardin, 1845 was controversial and confused until the application of genetic and molecular methodologies that over the past 20 years have led to an apparently stable and widely accepted taxonomy (Mattiucci & Nascetti, 2006, 2008). Anisakid nematodes are parasites of aquatic organisms such as fish, marine mammals, and fish-eating birds and are distributed throughout much of the world (Anderson, 2000). They are grouped into two subfamilies and several genera, Contracaecinae Mozgovoi & Shakhmatova, 1971 (Contracaecum Railliet & Henry, 1912 and Phocascaris Höst, 1932) and Anisakinae Railliet & Henry, 1912 (Anisakis, Pseudoterranova Mozgovoi, 1951, Skrjabinisakis, Peritrachelius Diesing, 1851, Sulcascaris Hartwich, 1957, Pulchrascaris Vicente & Santos, 1972, Euterranova Moravec & Justine, 2020, Neoterranova Moravec & Justine, 2020), forming a group of biodiverse representatives with complex phylogenetic relationships, and containing several taxon inquirendum (Nemys, 2023).

The genus Anisakis had been grouped into two subgenera, Anisakis and Skrjabinisakis, based on the shape and length of the ventriculus and male spicules. Few authors have used these subgeneric names (Takano & Sata, 2022). Safonova et al. (2021) proposed the use of Skrjabinisakis as a genus name rather than a subgenus for Anisakis physeteris (Baylis, 1923), A. brevispiculata (Dollfus, 1966) and A. paggiae Mattiucci, Nascetti, Dailey, Webb, Barros, Cianchi & Bullini, 2005, and the resurrected generic status of Peritrachelius for A. typica. Takano & Sata (2022), in their studies based on molecular data, do not assign A. typica to Peritrachelius, since the species was nested in Anisakis s.s., with similar phylogenetic relationship for A. simplex s.s. and A. typica observed by cox1 sequences. Mostafa et al. (2020) characterizes A. simplex s.s., A. pegreffii and A. typica as non-monophyletic groups, therefore, the use of cox1 sequences may be inadequate for the reconstruction of relationships among Anisakis species.

Morphologically, species in the genus Skrjabinisakis are characterized by presenting a short, straight ventriculus whose length is equal or nearly equal to width, vulva located in the anterior fourth or third of the body, spicules short, with length not exceeding 0.67 mm (Safonova et al., 2021). Four Anisakis species have been reclassified as Skrjabinisakis: S. physeteris (type species) (syn. Anisakis physeteris and Anisakis skrjabini (Mozgovoy, 1949)); S. schupakovi (Mozgovoy, 1951); S. brevispiculata and S. paggiae (Safonova et al., 2021; Chero et al., 2023). Species of Anisakis and Skrjabinisakis have a complex life cycle. In the parasite’s adult stage it lives in marine mammals, mainly cetaceans (ziphiids, delphinids, sperm whales, or a wide array of delphinoid odontocetes and mysticetes), while planktonic or semi-planktonic crustaceans act as first intermediate hosts of the parasite, and fish and squid represent intermediate/paratenic hosts (Mattiucci & Nascetti, 2008; Kuhn et al., 2016; Cipriani et al., 2022). Cetaceans of the families Physeteridae (Physeter macrocephalus Linnaeus, 1758) and Kogiidae (Kogia sima (Owen, 1866) and K. breviceps (de Blainville, 1838)) are the main definitive hosts for the species S. physeteris, S. brevispiculata and S. paggiae (Mattiucci et al., 2001, 2005; Mattiucci & Nascetti, 2006).

Parasite infections are important bioindicators of marine mammal ecology and health because they provide information on habitat use, diet, social behavior, and population dynamics (Mattiucci & Nascetti, 2008). They also enable inferences regarding parasite/host evolutionary relationships, as well as biogeographic and phylogenetic relationships throughout history (Anderson, 1982; Balbuena & Raga, 1994; Leidenberger et al., 2007; Marcogliese & Pietrock, 2011; Lehnert et al., 2014).

Although the Brazilian literature includes several studies on the parasitic fauna in terrestrial mammals in Brazil (Vicente et al., 1997; Vieira et al., 2008; Pinto et al., 2011), these data are scarce for the Amazon region when related to helminthological studies in aquatic mammals. With that in mind, this study taxonomically describes the anisakid parasites, recovered post-mortem from a female pygmy sperm whale, found stranded on the northern coast of Pará State, Brazilian Amazon.

Materials and Methods

Nematodes were recovered during necropsy of a female dwarf sperm whale (Kogia sima) stranded on Humaitá beach (0°55’37”S; 48°17’12”W), municipality of Colares, state of Pará, northern Brazil, on 4 October 2018. Nematodes were fixed with 10% formaldehyde, stored at room temperature and examined using light microscopy and scanning electron microscopy following procedures described by Pinheiro et al. (2018). For light microscopy 18 females, 1 male and 6 fourth-stage larvae were examined and, for scanning electron microscopy 5 females and 1 male were observed. All measurements are presented in micrometers, unless otherwise indicated. The taxonomic classification of nematodes was in accordance with Safonova et al. (2021) and Takano & Sata (2022).

Results

A total of 42 nematodes (32 females, 4 males and 6 fourth-stage larvae - L4) were recovered from the intestine of a specimen of Kogia sima. The morphological and morphometric characteristics of the nematodes recovered from dwarf sperm whale are presented below, Figures 1, 2, 3 and in Table 1.

Figure 1
Light microscopy of S. paggiae identified in the present study: (a) lateral view of cephalic region showing muscular esophagus (me); nerve ring (nr); ventriculus (ve) and intestine (in). Bar = 200µm. (b) Lateral view of vulva (arrowhead). Bar = 100µm. (c) Posterior end of female lateral view: intestine (in), rectum (re) and anus (an). Bar = 100µm. (d) Detail posterior end of male, lateral view intestine (in), cloacal opening (cl) and spicules (arrowheads). Bar = 100µm. (e) Posterior end of male, lateral view cloacal opening (cl) and spicules (arrowheads). Bar = 200µm.

Figure 2
Scanning electron microscopy of S. paggiae identified in the present study. (a) apical view of the anterior end showing three lips (two ventrolateral lips, one dorsolateral lip) with dentigerous ridges, lips papillae (pa), amphids (arrowheads) and excretory pore (ep). Bar = 20µm. (b) Posterior end of female, ventral view anus (an), on pair of phasmids lateral (arrowheads). Bar = 20µm. (c) Posterior end of male, ventral view, 2 of the lateral cuticular dilatations (arrow). Bar = 100µm. (d) Detail of caudal papillae sessile: 1 median papilla (me); 1 pair of single proximal papillae (a) lateral to cloaca; 1 pair of double paracloacal papillae (b); 4 pairs of distal papillae (c, d, e, f), of which (a, c, f) are equal in size and larger than (d, e), (d, e, f) are very close each other and one pair of very small papilla-like phasmids (ph), situated more laterally and posterior to last pair of distal papillae. Bar = 50µm. (e) Detail of plectanes (arrowheads) in cloacal (*). Bar = 20µm.

Figure 3
Light microscopy of fourth-stage larvae of S. paggiae identified in the present study. (a) lateral view of cephalic region showing nerve ring (nr), muscular esophagus (me); ventriculus (ve) and intestine (in). Bar = 200µm. (b) Posterior portion, portion of the intestine (in), rectum (re), three unicellular rectal (*) glands and anus (an), the tail without mucron. Bar = 50µm.

Table 1
Morphological and morphometric comparison of S. paggiae specimens collected from Kogiidae.

Character	Morphological and morphometric comparison Skrjabinisakis paggiae
Hosts	K. sima Atlantic coast of Brazil (State of Pará)				K. breviceps and K. sima, Atlantic coast of Florida		K. sima Atlantic coast of Brazil (State of Ceará)
Locality
Sex	Male	Females with eggs	Females without eggs	L4	Male	Female	Male	Female
Length (mm)	21	19−28	18−25	15−21	23−40	29−50	32−35	28−42
Width	343	600−800	571−800	443−643	−	−	−	−
Nerve ring	371	314−429	286−386	257−343	−	−	−	−
Esophagus (mm)L	2	1.9−2.3	1.6−2	1.4−1.8	2−5	2.6−2.8	2.15−2.3	2.5−2.7
EsophagusW	429	329−386	271−386	257−343	400−450	300−400	360−390	290−320
Ventriculus shape	violin				violin		violin
VentriculusL	343	243−443	314−400	257−386	350−400	410−450	370−400	390−420
Ventriculusw	200	200−229	157−271	143−229	240−270	300−350	240−250	280−330
Vulva (mm)	−	6−8	6−7	−	−	−	−	−
Spicules (mm)	0.18	−	−	−	0.17−0.22	−	0.18−0.19	−
Tail	267	147−233	137−207	77−110	150−170	−	−	−
Reference	Present study				Mattiucci et al. (2005)		Di Azevedo et al. (2015)

• L: length, W: width.

Anisakidae Railliet & Henry, 1912

Skrjabinisakis Mozgovoi, 1951

Skrjabinisakis paggiae (Mattiucci, Nascetti, Dailey, Webb, Barros, Cianchi & Bullini, 2005)

Robust, medium-sized nematode, morphology of the anterior region similar in both sexes. Transverse cuticular striae present throughout body except for lips. Cephalic extremity long and rounded, triangular mouth opening, surrounded by three lips (one dorsal with two papillae present and each ventro-lateral lip having one papilla and one amphid) (Figures 1a and 2a). Projection with dentigerous ridges on surface inner in lips (Figure 2a). Interlabia absent. Esophagus muscular, flask-shaped, opening into the ventriculus (Figure 1a). Excretory pore at the base of the dorsal lip (Figure 2a). Ventriculus short, robust, violin-shaped (Figure 1a), with a distinct constriction in the middle, connected to the intestine by a slightly oblique junction (in dorsal view).

Males (based on 1 specimen): body 21 mm, maximum width at ventricule/intestinal junction 343. Nerve ring 371, measured to the anterior end. Muscular esophagus 2 mm long, 429 wide; the esophagus represents 9.5% of the total body length. Ventriculus 343 in length, 200 in width at level of constriction. Length of entire esophagus and ventriculus representing 11% of body length. Caudal papillae sessile, proximal and disposed in single row (Figure 2c): 1 median papilla; 1 pair of single proximal papillae (a) lateral to cloaca; 1 pair of double paracloacal papillae (b); 4 pairs of distal papillae (c, d, e, f), of which (a, c, f) are equal in size and larger than (d, e), and (d, e, f) are very close to each other (Figure 2d). The papillae all have the same circular structure surrounded by wrinkled cuticle and provided with a small central knob. One pair of extremely small papilla-like phasmids situated more laterally and posterior to last pair of distal papillae (Figure 2d). Spicules short, stout, slightly equal and sclerotized 0.18 mm long, representing 0.85% of total body length (Figure 1d). Gubernaculum Absent. Tail rounded, 267 in length; distal extremity of tail rounded (Figure 1e) and 2 cuticular dilatation structures (Figure 2c). Three narrow denticulate caudal plates (plectanes) are present (Figure 2e).

Females with eggs (based on 6 specimens): body 23 mm (19–28 mm), maximum width at the height of the vulvar region 671 (600–800). Nerve ring 362 (314–429), measured to the anterior end. Muscular esophagus 2 mm (1.9–2.3 mm) long, 357 (329–386) wide; the esophagus represents 9% (8–10%) of body length. Ventriculus 357 (243–443) in length, 217 (200–229) in width at level of constriction. Length of entire esophagus and ventriculus representing 11% (9–12%) of body length. Vulva situated at 7 mm (6–8 mm) from anterior end, at about 30% (22–33%) of body length; vulval lips not elevated (Figure 1b). Muscular vagina directed posteriorly; uterus eggs elliptical or round shape, shell single, thin, smooth and transparent and embryo morulate. The eggs are 54 (47–67) long by 36 (30–47) wide. Rectum is a short hyaline tube; 3 small, unicellular rectal glands are present measuring 204 (180‒233). Anus with prominent upper lip. Tail is conical, 176 (147‒233) in length (Figures 1c and 2b).

Females without eggs (based on 6 specimens): body 21 mm (18–25 mm), maximum width at the height of the vulvar region 676 (571–800). Nerve ring 336 (286–386), measured to the anterior end. from anterior extremity. Muscular esophagus 2 mm (1.6–2 mm) long, 329 (271–386) wide; the esophagus represents 9% (8–10%) of body length. Ventriculus 343 (314–400) in length, 198 (157–271) in width at level of constriction. Length of entire esophagus and ventriculus represents 11% (10–12%) of body length. Vulva situated at 6 mm (6–7 mm) from anterior end, at about 30% (29–33%) of body length; vulval lips not elevated. Muscular vagina directed posteriorly, uterus without eggs. Rectum is a short hyaline tube; 3 small, unicellular rectal glands are present measuring 183 (167‒200). Anus with prominent upper lip. Tail conical with a length of 166 (137–207).

Fourth-stage larvae (based on 6 specimens): body 18 mm (15–21 mm), maximum width at ventriculus/intestinal junction 512 (443–643). Mouth has three lips: one dorsal showing two double papillae and each subventral lip presenting a single double papilla. Excretory pore opening between two subventral lips (Figure 3a). Nerve ring 288 (257–343), measured to the anterior end. Muscular esophagus 1.6 mm (1.4–1.8 mm) long, 286 (257–343) wide; the esophagus represents 9.5% of the total body length. Ventriculus 317 (257–386) in length, 186 (143–229) in width at level of constriction. Length of entire esophagus and ventriculus represents 11% of body length. Rectum is a short hyaline tube; 3 small, unicellular rectal glands are present measuring 113 (103‒123) (Figure 3b). Tail is conical, 91 (77‒110) in length, mucron absent.

Discussion

The nematode parasites from Kogia sima collected in the municipality of Colares, State of Pará, have similar characteristics to those of other species of the family Anisakidae and genus Skrjabinisakis. Based on the morphological features of the violin-shaped ventriculus, short and equal spicules and the distribution of caudal papillae in the male, the anisakid adult and L4 specimens were identified as S. paggiae. Although there are few articles related to parasitic helminths of cetaceans in Brazil, different researchers have sporadically attempted to learn about the biodiversity of whale parasites present along the Brazilian coast (see Yamaguti, 1959, 1963, 1971; Travassos, 1965; Travassos et al., 1969; Vicente et al., 1997; Muniz-Pereira et al., 1999). Muniz-Pereira et al. (1999) presented the first checklist of helminths in cetaceans in Brazil. Later Vieira et al. (2008) and Muniz-Pereira et al. (2009), seeking a more comprehensive and integrated description of the parasitic helminth fauna of vertebrates (host, locality and geographical distribution), included records of parasitism in cetaceans present in the Helminthology Collection of the Instituto Oswaldo Cruz (CHIOC).

The species in this study (Skrjabinisakis paggiae), is recorded worldwide as a parasite of whales of the families Kogiidae (i.e., dwarf sperm whale, K. sima, and pygmy sperm whale, K. breviceps), which serve as definitive hosts, mainly in the mid- and southern Atlantic Ocean (Valentini et al., 2006; Mattiucci & Nascetti, 2008; Quiazon, 2016; Shamsi, 2021; Cipriani et al., 2022). The association observed between Anisakis species and various cetacean taxa may reflect a coevolutionary history between these endoparasites and their hosts that has been estimated as older than 50 million years ago, driven by common trophic adaptations (Mattiucci & Nascetti, 2008; Klimpel & Palm, 2011; Li et al. 2018).

When proposing the description of Skrjabinisakis paggiae the authors associated the morphology of the ventricle (the adult ventriculus is short, never sigmoid and broader than long) and the spicules (the male spicules are short, stout and of similar length). These characteristics are observed in Skrjabinisakis physeteris and S. brevispiculata, which are parasites of cetaceans of the families Physeteridae and Kogiidae (Mattiucci & Nascetti, 2008). Skrjabinisakis paggiae and S. brevispiculata share the pygmy sperm whale as definitive hosts (Paggi et al., 1998; Mattiucci et al., 1986, 1997, 2001, 2005; Mattiucci & Nascetti, 2006, 2008; Safonova et al., 2021). This host preference allows anisakids to be used as biological indicators of their distribution and ultimate host abundance, since they closely follow the trophic relationships of their successive hosts (Mattiucci & Nascetti, 2008; Kuhn et al., 2011).

For Brazilian waters, Luque et al. (2010) presented a checklist that adds data to previous sparse publications but does not mention the occurrence of S. paggiae, only that of A. insignis, A. simplex, S. physeteris and P. typica, in addition to Anisakis sp., Contracaecum sp. and Pseudoterranova sp. along the Brazilian coast in different hosts. The same authors recorded S. physeteris, Anisakis sp. and Pseudoterranova sp. in Rio de Janeiro State, Ceará State and Pernambuco State (Fernando de Noronha Archipelago), parasitizing the stomach of pygmy sperm whales.

This is the first record of S. paggiae on the northern coast of Brazil (brackish water), although not its first record for K. sima. Among anisakid parasites infecting stranded cetaceans, especially Kogiidae whales, Di Azevedo et al. (2017) recorded P. typica, A. ziphidarum, S. brevispiculata and S. paggiae, parasitizing K. sima on the northeast coast (marine environment) of the country. Skrjabinisakis paggiae was recorded by Di Azevedo et al. (2015) in dwarf sperm whales stranded on Barra das Moitas beach, municipality of Amontada in Ceará state, northeastern Brazil, with details obtained by scanning electron microscopy for this parasite. Di Azevedo et al. (2017) recorded parasitism by Skrjabinisakis paggiae infecting K. breviceps in the country.

Although in this study the specimens observed were recovered from the intestine, factors such as time of host death and deterioration can cause parasites to migrate between organs, thus modifying the usual site of infection, which for Skrjabinisakis paggiae is the stomach. Skrjabinisakis paggiae was described from the stomach of K. breviceps on the Atlantic coast of Florida (United States) based on three males and four females collected and on one male K. sima from the same locality (Mattiucci et al., 2005). Subsequently, its known geographic distribution was expanded to include the Philippine archipelago, western Atlantic Ocean, Caribbean Sea, Gulf of Mexico, Atlantic coast of Brazil and Australian waters (Quiazon et al., 2013; Di Azevedo et al., 2015, 2017; Shamsi et al., 2019).

In this work, observations by light microscopy and scanning electron microscopy highlight important features for future taxonomic studies for Skrjabinisakis paggiae, such as anterior end morphology (denticles that may be related to fixation on host tissue, double papillae in the dorsal lip), location and morphology of the vulva (6−8 mm), in addition to the distribution of the postcloacal papillae (1 median papilla; 1 pair of adcloacal papillae; 1 pair of double paracloacal papillae; 4 pairs of distal papillae) in males, confirming the data observed in SEM by Di Azevedo et al. (2015) for Skrjabinisakis paggiae and in light microscopy by Mattiucci et al. (2005). The spicule size (0.18 mm) of this study showed equivalence to that in Mattiucci et al. (2009) (0.17−0.22 mm); Di Azevedo et al. (2015) (0.18−0.19 mm) and Shamsi et al. (2019) (0.18−0.25 mm) for S. paggiae. Additional morphometric comparisons between S. paggiae are presented in Table 1.

Due to the type of preservation of the material (in 10% formaldehyde) we do not present molecular data, although Di Azevedo et al. (2017) have provided molecular records based on cox2 mtDNA sequences, for the occurrence of an A. paggiae-like species, with a genetic distance between the A. paggiae-like specimen and S. paggiae of (0.06), which is the same as between A. simplex and A. pegreffii, defined as distinct species (see Mattiucci et al., 1997, 2014) which are possibly being reported because they are different genera. According to phylogenic analyses, the branching order so far proposed for the Anisakis/Skrjabinisakis taxa showed that nematodes from the sperm whale and pygmy sperm whales (i.e., S. physeteris, S. brevispiculata and S. paggiae) always occupy a well-supported basal lineage (Mattiucci & Nascetti, 2008). Cipriani et al. (2022) when presenting the phylogeny of some Anisakids, based on cox2 mtDNA sequences, divided the species into three clades: Clade (I) comprises species of the A. simplex (s.s.) complex, A. pegreffii, A. berlandi; Clade (II) A. ziphidarum and A. nascettii and Clade (III) S. physeteris, S. brevispiculata, and S. paggiae, the last clade also being confirmed with the morphological data for the three species.

Conclusion

This research records S. paggiae parasitizing Kogia sima in brackish water of northern Brazil, adding clarifying taxonomic features in SEM for S. paggiae.

Acknowledgements

The authors are grateful to Luane Gabriela Botelho Rebelo, Marceli Batista Martins Lima, Lia Torres Amaral for the donation of nematodes recovered from Kogia sima and the Laboratório de Histologia e Embriologia Animal and Laboratório de Microscopia Eletrônica de Varredura – Instituto da Saúde e Produção Animal – Universidade Federal Rural da Amazônia – UFRA, campus Belém, state of Pará, Brazil for the use of the scanning electron microscope. Dra. Elane Giese was supported by a research fellowship from the Conselho Nacional de Pesquisa e Desenvolvimento Tecnológico (CNPq-Brasil) (#313763/2020-8).

• How to cite: Pinheiro RHS, Bezerra AM, Giese EG. Morphological identification of Skrjabinisakis Mozgovoi, 1951 (Nematoda: Anisakidae) in Kogia sima (Cetacea: Kogiidae) from Brazilian waters. Braz J Vet Parasitol 2023; 32(4): e013423. https://doi.org/10.1590/S1984-29612023064

References

• Anderson R. Host-parasite relations and evolution of the Metastrongyloidea (Nematoda). Mém Mus Natl Hist Nat, Serie A. Zoologie 1982; 123(1): 129-133.
• Anderson RC. Nematode parasites of vertebrates. Their development and transmission 2nd ed. London: CABI Publishing; 2000. http://dx.doi.org/10.1079/9780851994215.0000
  » http://dx.doi.org/10.1079/9780851994215.0000
• Balbuena J, Raga J. Intestinal helminths as indicators of segregation and social structure of pods of long-finned pilot whales (Globicephala melas) off the Faeroe Islands. Can J Zool 1994; 72(3): 443-448. http://dx.doi.org/10.1139/z94-062
  » http://dx.doi.org/10.1139/z94-062
• Chero JD, Ñacari L, Cruces CL, Lopez DF, Cacique E, Severino R, et al. Morphological and molecular characterization of Anisakid nematode larvae (Nematoda: Anisakidae) in the Black Cusk eel Genypterus maculatus from the Southeastern Pacific Ocean off Peru. Diversity (Basel) 2023; 15(7): 820. http://dx.doi.org/10.3390/d15070820
  » http://dx.doi.org/10.3390/d15070820
• Cipriani P, Palomba M, Giulietti L, Marcer F, Mazzariol S, Santoro M, et al. Distribution and genetic diversity of Anisakis spp. in cetaceans from the Northeast Atlantic Ocean and the Mediterranean Sea. Sci Rep 2022; 12(1): 13664. http://dx.doi.org/10.1038/s41598-022-17710-1 PMid:35953527.
  » http://dx.doi.org/10.1038/s41598-022-17710-1
• Di Azevedo MIN, Carvalho VL, Iñiguez AM. Integrative taxonomy of anisakid nematodes in stranded cetaceans from Brazilian waters: an update on parasite’s hosts and geographical records. Parasitol Res 2017; 116(11): 3105-3116. http://dx.doi.org/10.1007/s00436-017-5622-8 PMid:28975458.
  » http://dx.doi.org/10.1007/s00436-017-5622-8
• Di Azevedo MIN, Knoff M, Carvalho VL, Mello WN, Lopes Torres EJ, Gomes DC, et al. Morphological and genetic identification of Anisakis paggiae (Nematoda: Anisakidae) in dwarf sperm whale Kogia sima from Brazilian waters. Dis Aquat Organ 2015; 113(2): 103-111. http://dx.doi.org/10.3354/dao02831 PMid:25751853.
  » http://dx.doi.org/10.3354/dao02831
• Klimpel S, Palm HW. Anisakid Nematode (Ascaridoidea) life cycles and distribution: increasing zoonotic potential in the time of climate change? In: Mehlhorn H, editor. Progress in parasitology: parasitology research monographs Berlin, Heidelberg: Springer; 2011. vol. 2, p. 201-222. http://dx.doi.org/10.1007/978-3-642-21396-0_11
  » http://dx.doi.org/10.1007/978-3-642-21396-0_11
• Kuhn T, Cunze S, Kochmann J, Klimpel S. Environmental variables and definitive host distribution: a habitat suitability modelling for endohelminth parasites in the marine realm. Sci Rep 2016; 6(1): 30246. http://dx.doi.org/10.1038/srep30246 PMid:27507328.
  » http://dx.doi.org/10.1038/srep30246
• Kuhn T, García-Màrquez J, Klimpel S. Adaptive radiation within marine anisakid nematodes: a zoogeographical modeling of cosmopolitan, zoonotic parasites. PLoS One 2011; 6(12): e28642. http://dx.doi.org/10.1371/journal.pone.0028642 PMid:22180787.
  » http://dx.doi.org/10.1371/journal.pone.0028642
• Lehnert K, Seibel H, Hasselmeier I, Wohlsein P, Iversen M, Nielsen NH, et al. Increase in parasite burden and associated pathology in harbour porpoises (Phocoena phocoena) in West Greenland. Polar Biol 2014; 37(3): 321-331. http://dx.doi.org/10.1007/s00300-013-1433-2
  » http://dx.doi.org/10.1007/s00300-013-1433-2
• Leidenberger S, Harding K, Härkönen T. Phocid seals, seal lice and heartworms: a terrestrial host–parasite system conveyed to the marine environment. Dis Aquat Organ 2007; 77(3): 235-253. http://dx.doi.org/10.3354/dao01823 PMid:18062474.
  » http://dx.doi.org/10.3354/dao01823
• Li L, Lü L, Nadler SA, Gibson DI, Zhang L-P, Chen H-X, et al. Molecular phylogeny and dating reveal a terrestrial origin in the early carboniferous for ascaridoid nematodes. Syst Biol 2018; 67(5): 888-900. http://dx.doi.org/10.1093/sysbio/syy018 PMid:29528459.
  » http://dx.doi.org/10.1093/sysbio/syy018
• Luque JL, Muniz-Pereira LC, Siciliano S, Siqueira LR, Oliveira MS, Vieira FM. Checklist of helminth parasites of cetaceans from Brazil. Zootaxa 2010; 2548(1): 57-68. http://dx.doi.org/10.11646/zootaxa.2548.14
  » http://dx.doi.org/10.11646/zootaxa.2548.14
• Marcogliese DJ, Pietrock M. Combined effects of parasites and contaminants on animal health: parasites do matter. Trends Parasitol 2011; 27(3): 123-130. http://dx.doi.org/10.1016/j.pt.2010.11.002 PMid:21144800.
  » http://dx.doi.org/10.1016/j.pt.2010.11.002
• Mattiucci S, Cipriani P, Webb SC, Paoletti M, Marcer F, Bellisario B, et al. Genetic and morphological approaches distinguish the three sibling species of the Anisakis simplex species complex, with a species designation as Anisakis berlandi n. sp. for A. simplex sp. C (Nematoda: Anisakidae). J Parasitol 2014; 100(2): 199-214. http://dx.doi.org/10.1645/12-120.1 PMid:24224764.
  » http://dx.doi.org/10.1645/12-120.1
• Mattiucci S, Nascetti G, Bullini L, Orecchia P, Paggi L. Genetic structure of Anisakis physeteris, and its differentiation from the Anisakis simplex complex (Ascaridida: anisakidae). Parasitology 1986; 93(Pt 2): 383-387. http://dx.doi.org/10.1017/S0031182000051544 PMid:3785976.
  » http://dx.doi.org/10.1017/S0031182000051544
• Mattiucci S, Nascetti G, Clanchi R, Paggi L, Arduino P, Margolis L, et al. Genetic and ecological data on the Anisakis simplex complex with evidence for a new species (Nematoda, Ascaridoidea, Anisakidae). J Parasitol 1997; 83(3): 401-416. http://dx.doi.org/10.2307/3284402 PMid:9194819.
  » http://dx.doi.org/10.2307/3284402
• Mattiucci S, Nascetti G, Dailey M, Webb SC, Barros NB, Cianchi R, et al. Evidence for a new species of Anisakis Dujardin, 1845: morphological description and genetic relationships between congeners (Nematoda: Anisakidae). Syst Parasitol 2005; 61(3): 157-171. http://dx.doi.org/10.1007/s11230-005-3158-2 PMid:16025205.
  » http://dx.doi.org/10.1007/s11230-005-3158-2
• Mattiucci S, Nascetti G. Advances and trends in the molecular systematics of anisakid nematodes, with implications for their evolutionary ecology and host-parasite co-evolutionary processes. Adv Parasitol 2008; 66: 47-148. http://dx.doi.org/10.1016/S0065-308X(08)00202-9 PMid:18486689.
  » http://dx.doi.org/10.1016/S0065-308X(08)00202-9
• Mattiucci S, Nascetti G. Molecular systematics, phylogeny and ecology of anisakid nematodes of the genus Anisakis Dujardin, 1845: an update. Parasite 2006; 13(2): 99-113. http://dx.doi.org/10.1051/parasite/2006132099 PMid:16800118.
  » http://dx.doi.org/10.1051/parasite/2006132099
• Mattiucci S, Paggi L, Nascetti G, Abollo E, Webb SC, Pascual S, et al. Genetic divergence and reproductive isolation between Anisakis brevispiculata and Anisakis physeteris (Nematoda: Anisakidae)s. Int J Parasitol 2001; 31(1): 9-14. http://dx.doi.org/10.1016/S0020-7519(00)00125-9 PMid:11165265.
  » http://dx.doi.org/10.1016/S0020-7519(00)00125-9
• Mattiucci S, Paoletti M, Webb SC. Anisakis nascettii n. sp. (Nematoda: Anisakidae) from beaked whales of the southern hemisphere: morphological description, genetic relationships between congeners and ecological data. Syst Parasitol 2009; 74(3): 199-217. http://dx.doi.org/10.1007/s11230-009-9212-8 PMid:19790000.
  » http://dx.doi.org/10.1007/s11230-009-9212-8
• Mostafa E, Omar M, Hassan SS, Samir M. Occurrence and molecular identification of Anisakis larval type 1 (Nematoda: Anisakidae) in marketed fish in Egypt. J Parasit Dis 2020; 44(3): 536-545. http://dx.doi.org/10.1007/s12639-020-01222-8 PMid:32801505.
  » http://dx.doi.org/10.1007/s12639-020-01222-8
• Muniz-Pereira LC, Vicente JJ, Noronha D. Helminths parasites of whales in Brazil. Rev Bras Zool 1999; 16(Suppl 2): 249-252. http://dx.doi.org/10.1590/S0101-81751999000600025
  » http://dx.doi.org/10.1590/S0101-81751999000600025
• Muniz-Pereira LC, Vieira FM, Luque JL. Checklist of helminth parasites of threatened vertebrate species from Brazil. Zootaxa 2009; 2123(1): 1-45. http://dx.doi.org/10.11646/zootaxa.2123.1.1
  » http://dx.doi.org/10.11646/zootaxa.2123.1.1
• Nemys – World Database of Nematodes. Anisakidae Railliet & Henry, 1912. [online] 2023 [cited 2023 Aug 11]. Available from: https://www.marinespecies.org/aphia.php?p=taxdetails&id=19961
  » https://www.marinespecies.org/aphia.php?p=taxdetails&id=19961
• Paggi L, Nascetti G, Webb SC, Mattiucci S, Cianchi R, Bullini L. A new species of Anisakis Dujardin, 1845 (Nematoda, Anisakidae) from beaked whales (Ziphiidae): allozyme and morphological evidence. Syst Parasitol 1998; 40(3): 161-174. http://dx.doi.org/10.1023/A:1006093201920
  » http://dx.doi.org/10.1023/A:1006093201920
• Pinheiro RHS, Santana RLS, Monks S, Santos JN, Giese EG. Cucullanus marajoara n. sp. (Nematoda: Cucullanidae), a parasite of Colomesus psittacus (Osteichthyes: Tetraodontiformes) in the Marajó, Brazil. Rev Bras Parasitol Vet 2018; 27(4): 521-530. http://dx.doi.org/10.1590/s1984-296120180072 PMid:30427526.
  » http://dx.doi.org/10.1590/s1984-296120180072
• Pinto RM, Knoff M, Gomes DC, Noronha D. Nematodes from Mammals in Brazil: an updating. Neotrop Helminthol 2011; 5(2): 139-183.
• Quiazon KMA, Santos MD, Yoshinaga T. Anisakis species (Nematoda: Anisakidae) of dwarf sperm whale Kogia sima (Owen, 1866) stranded off the Pacific coast of southern Philippine archipelago. Vet Parasitol 2013; 197(1−2): 221-230. http://dx.doi.org/10.1016/j.vetpar.2013.05.019 PMid:23786786.
  » http://dx.doi.org/10.1016/j.vetpar.2013.05.019
• Quiazon KMA. Anisakis Dujardin, 1845 infection (Nematoda: Anisakidae) in Pygmy Sperm Whale Kogia breviceps Blainville, 1838 from west Pacific region off the coast of Philippine archipelago. Parasitol Res 2016; 115(9): 3663-3668. http://dx.doi.org/10.1007/s00436-016-5169-0 PMid:27300704.
  » http://dx.doi.org/10.1007/s00436-016-5169-0
• Safonova AE, Voronova AN, Vainutis KS. First report on molecular identification of Anisakis simplex in Oncorhynchus nerka from the fish market, with taxonomical issues within Anisakidae. J Nematol 2021; 53(1): e2021-e2023. http://dx.doi.org/10.21307/jofnem-2021-023 PMid:33860240.
  » http://dx.doi.org/10.21307/jofnem-2021-023
• Shamsi S, Sprohnle-Barrera C, Shafaet Hossen M. Occurrence of Anisakis spp. (Nematoda: Anisakidae) in a pygmy sperm whale Kogia breviceps (Cetacea: Kogiidae) in Australian waters. Dis Aquat Organ 2019; 134(1): 65-74. http://dx.doi.org/10.3354/dao03360 PMid:31020949.
  » http://dx.doi.org/10.3354/dao03360
• Shamsi S. The occurrence of Anisakis spp. in Australian waters: past, present, and future trends. Parasitol Res 2021; 120(9): 3007-3033. http://dx.doi.org/10.1007/s00436-021-07243-3 PMid:34341859.
  » http://dx.doi.org/10.1007/s00436-021-07243-3
• Takano T, Sata N. Multigene phylogenetic analysis reveals non-monophyly of Anisakis s. l. and Pseudoterranova (Nematoda: anisakidae). Parasitol Int 2022; 91: 102631. http://dx.doi.org/10.1016/j.parint.2022.102631 PMid:35863674.
  » http://dx.doi.org/10.1016/j.parint.2022.102631
• Travassos L, Freitas JFT, Kohn A. Trematódeos do Brasil. Mem Inst Oswaldo Cruz 1969; 67(1): 1-886. PMid:5397756.
• Travassos L. Contribuição para o Inventário Crítico da Zoologia no Brasil. Fauna Helmintológica: Considerações Preliminares – Cestódeos Rio de Janeiro: Universidade Federal do Rio de Janeiro; 1965. (Publicações Avulsas do Museu Nacional)
• Valentini A, Mattiucci S, Bondanelli P, Webb SC, Mignucci-Giannone AA, Colom-Llavina MM, et al. Genetic relationships among Anisakis species (Nematoda: Anisakidae) inferred from mitochondrial cox2 sequences, and comparison with allozyme data. J Parasitol 2006; 92(1): 156-166. http://dx.doi.org/10.1645/GE-3504.1 PMid:16629330.
  » http://dx.doi.org/10.1645/GE-3504.1
• Vicente JJ, Rodrigues HO, Gomes DC, Pinto RM. Nematóides do Brasil. Parte V: nematóides de mamíferos. Rev Bras Zool 1997; 14(Suppl 1): 1-452. http://dx.doi.org/10.1590/S0101-81751997000500001
  » http://dx.doi.org/10.1590/S0101-81751997000500001
• Vieira FM, Luque JL, Muniz-Pereira LC. Checklist of helminth parasites in wild carnivore mammals from Brazil. Zootaxa 2008; 1721(1): 1-23. http://dx.doi.org/10.11646/zootaxa.1721.1.1
  » http://dx.doi.org/10.11646/zootaxa.1721.1.1
• Yamaguti S. Synopsis of the digenetic trematodes of vertebrates. Tokyo: Keigaku Publishing Company; 1971.
• Yamaguti S. Systema Helminthum. Vol. II. The Cestodes of Vertebrates New York: Interscience Publishers; 1959.
• Yamaguti S. Systema Helminthum. Vol. V. The Acanthocephala of Vertebrates New York: Interscience Publishers; 1963.

Publication Dates

• Publication in this collection
  13 Nov 2023
• Date of issue
  2023

History

• Received
  18 Aug 2023
• Accepted
  14 Sept 2023