Apocreadiinae Skrjabin, 1942

Blend, Charles K., Karar, Yasser F. M. & Dronen, Norman O., 2017, Revision of the Megaperidae Manter, 1934 n. comb. (Syn. Apocreadiidae Skrjabin, 1942) including a reorganization of the Schistorchiinae Yamaguti, 1942, Zootaxa 4358 (1), pp. 1-44 : 6-8

Subfamily Apocreadiinae Skrjabin, 1942

(Syns. Anallocreadiinae Hunter & Bangham, 1932 ; Homalometrinae Cable & Hunninen, 1942 ; Myzotinae Yamaguti, 1958 ; Marsupioacetabulinae Skrjabin & Koval, 1960 ; Eocreadiinae Mehra, 1962 ; Microcreadiinae Mehra, 1962 )

Diagnosis. (Based on Cribb 2005) Tegument spinous or unarmed. Oral sucker subterminal, unspecialized, with or without papillae. Ventral sucker pre-equatorial, unspecialized, with or without lamellar lips or flaps. Prepharynx often very short, sometimes longer than pharynx. Esophagus short or long. Caeca end blindly or form cyclocoel. Testes two, tandem, oblique or opposite. Cirrus pouch absent. Genital pore median, immediately anterior to ventral sucker (some distance anterior in Pancreadium ). Ovary smooth or deeply lobed. Vitellarium follicular; follicles extensive, either restricted to hindbody or enter forebody. Excretory vesicle I-shaped, very short or extends anteriorly to posterior testis or to ovary; excretory pore terminal or dorsally or ventrally subterminal. Lymphatic vessels present or absent. Eggs unembryonated when laid, embryonate to produce miracidia which infect fresh- and brackish-water hydrobiid, amnicolid, viviparid and planorbid snails, undergo polyembrony to produce rediae that develop cercariae that are shed into environment and infect freshwater sphaeriid and unionid bivalves as well as marine venerid clams and small polychaetes, and form metacercariae infective to definitive host. Adults in intestine of marine and freshwater fishes; cosmopolitan.

Type genus. Homalometron Stafford, 1904 (Syn. Apocreadium Manter, 1937 —see Cribb 2005).

Remarks. Members of the Apocreadiinae are unique within the Megaperidae n. comb. in possessing a genital pore anterior to the ventral sucker, an oral sucker lacking a partial U-shaped sphincter encircling the aperture of the sucker, and caeca that either end blindly or form a cyclocoel. The main features used to distinguish apocreadiine genera include the appearance of the tegument, forebody, ventral and oral suckers, pharynx, ovary, testes and uterus, the terminal nature of the caeca (forming a cyclocoel or ending blindly) and their posterior extent, the anterior and posterior extent of the vitellarium, the exact location of the excretory and genital pores, the ratio of body length to width, the size of the post-testicular region and the anterior extent of the excretory vesicle ( Cribb 2005).

Apocreadiinae is the largest subfamily within the Megaperidae n. comb. with 14 recognized genera. Callohelmis Cribb & Bray, 1999 was erected by Cribb & Bray (1999) with the type and only species, Callohelmis pichelinae Cribb & Bray, 1999 , found parasitizing the intestine of the blackeye thicklip, Hemigymnus melapterus (Bloch) , the barred thicklip, Hemigymnus fasciatus (Bloch) , the red shoulder wrasse, Stethojulis bandanensis (Bleeker) and the venus tuskfish, Choerodon venustus (De Vis) ( Perciformes : Labridae ), from off Heron Island, southern Great Barrier Reef, Australia. Choanodera Manter, 1940 was erected by Manter (1940) with the description of Choanodera caulolatili Manter, 1940 infecting the intestine of the bighead filefish, Caulolatilus affinis Gill (= Caulolatilus anomalus Gill ) and Caulolatilus sp. ( Perciformes : Malacanthidae ), from off Cerros Island, Mexico, and Santiago (=James) Island, Galapagos. Crassicutis Manter, 1936 (Syn. Eocreadium Szidat, 1954 ) was erected by Manter (1936) when he described Crassicutis cichlasomae Manter, 1936 from the stomach of the cichlid Mayaheros mayorum (Hubbs) (= Cichlasoma mayorum Hubbs ) ( Perciformes : Cichlidae ) from off Yucatan, Mexico. Dactylotrema Bravo-Hollis & Manter, 1957 is a monotypic genus with its only member, Dactylotrema squamatum Bravo-Hollis & Manter, 1957 , obtained from the intestine of an unidentified mojarra, Gerres sp. ( Perciformes : Gerreidae ), found off Zihuatanejo, Guerrero, Mexico ( Bravo-Hollis & Manter 1957). Homalometron Stafford, 1904 (Syns. Anallocreadium Simer, 1929 ; Apocreadium Manter, 1937 ; Austrocreadium Szidat, 1956 ; Barbulostomum Ramsey, 1965 ) is a relatively large genus with the type species, Homalometron pallidum Stafford, 1904 , published by Stafford (1904) based on “ Distomum sp.” of Linton (1901, Fig. 354) collected from the stomach and duodenum of the mummichog, Fundulus heteroclitus ( Cyprinodontiformes : Fundulidae ), found in Canadian waters. Marsupioacetabulum marinum Yamaguti, 1952 was described by Yamaguti (1952) as the type species of Marsupioacetabulum Yamaguti, 1952 from a single specimen found in the intestine of the whipfin silver-biddy, Gerres filamentosus Cuvier (= Gerres punctatus Cuvier ) ( Perciformes : Gerreidae ), off Makassar, Sulawesi (formerly known as Celebes), Indonesia. Microcreadium Simer, 1929 was established by Simer (1929) with the description of Microcreadium parvum Simer, 1929 from the intestine of the freshwater drum, Aplodinotus grunniens Rafinesque ( Perciformes : Sciaenidae ), secured from the lower Tallahatchie River in Mississippi. Manter (1940) erected the monotypic genus Myzotus Manter, 1940 with the description of Myzotus vitellosus Manter, 1940 obtained from the intestine of the ocean whitefish, Caulolatilus princeps (Jenyns) ( Perciformes : Malacanthidae ), collected off Tagus Cove, Isabela (=Albemarle) Island, Galapagos. Sogandares-Bernal (1959), while studying the digenetic trematodes of marine fishes from the Gulf of Panama and off Bimini, Bahamas, British West Indies, described Apocreadium angustum Sogandares-Bernal, 1959 from the intestine of the buffalo trunkfish, Lactophrys trigonus (Linnaeus) ( Tetraodontiformes : Ostraciidae ). Siddiqi & Cable (1960), after collecting additional specimens of this digenean from the intestine of the spotted trunkfish, Lactophrys bicaudalis (Linnaeus) ( Tetraodontiformes : Ostraciidae ), from off Cabo Rojo, Puerto Rico, then erected Neoapocreadium Siddiqi & Cable, 1960 with Neoapocreadium angustum (Sogandares-Bernal, 1959) Siddiqi & Cable, 1960 as type species. They distinguished species of Neoapocreadium from Apocreadium (= Homalometron ) by the former possessing a longitudinal slit-like mouth, a massive pharynx, wide caeca, and confluent vitellarium in the forebody. Neomegasolena Siddiqi & Cable, 1960 is a monotypic genus with its type and only species, Neomegasolena chaetodipteri Siddiqi & Cable, 1960 described from the caeca and intestine of the Atlantic spadefish, Chaetodipterus faber (Broussonet) ( Perciformes : Ephippidae ), from off Isla Ratones, Puerto Rico ( Siddiqi & Cable 1960). Pancreadium Manter, 1954 is another monotypic genus with its type and only species, Pancreadium otagoensis Manter, 1954 described from the intestine, stomach and gall bladder of the New Zealand blue cod, Parapercis colias (Forster) ( Perciformes : Pinguipedidae ), from off Wellington and from the aquarium at the Portobello Marine Laboratory in New Zealand ( Manter 1954). Posterotestes Ostrowski de Núñez, Brugni & Flores, 2003 is monotypic with the type species, Posterotestes unelen Ostrowski de Núñez, Brugni & Flores, 2003 found infecting the posterior intestine of the creole perch, Percichthys trucha (Valenciennes) ( Perciformes : Percichthydidae), from Lake Epuyén, Chubut Province, Argentina ( Ostrowski de Núñez et al. 2003). Procaudotestis uruguayensis Szidat, 1954 was described by Szidat (1954) from the digestive tract of the armored catfish Paraloricaria vetula (Valenciennes) (= Loricaria vetula Valenciennes ) ( Siluriformes : Loricariidae ) from the Uruguay River, South America; it is the type species of Procaudotestis Szidat, 1954 . Finally, Trematobrien Dollfus, 1950 was erected—indeed, an entire new family, Trematobrienidae Dollfus, 1950 —with the description of Trematobrien haplochromios Dollfus, 1950 from the intestine of the southern mouthbrooder, Pseudocrenilabrus philander (Weber) (= Haplochromis moffati [non Castelnau]) ( Perciformes : Cichlidae ), from the Belgian Congo (now recognized as the Democratic Republic of the Congo) in Africa ( Dollfus 1950). With this review, we note that megaperines, postporines and schistorchiines are known from marine hosts only; whereas, apocreadiines infect fish from marine to freshwater environments. To our knowledge at least six, and perhaps more, apocreadiine genera are also monotypic. As alluded to by Cribb (2005, p. 624), the Apocreadiinae is a large, generalized “catch-all group” likely to be divided and redefined following further study.

Key to genera of Apocreadiinae Skrjabin, 1942 (based on Cribb 2005)

1a. Margins of forebody folded ventrally and converging to meet at posterior margin of ventral sucker..................................................................................................... Choanodera Manter, 1940 .

1b. Forebody not specialized as above....................................................................... 2.

2a. Caeca unite to form cyclocoel..................................................... Trematobrien Dollfus, 1950 .

2b. Caeca terminate blindly................................................................................ 3.

3a. Ventral sucker specialized with flaps or lamellar lips......................................................... 4.

3b. Ventral sucker not specialized (may be retracted or deeply embedded in body).................................... 5.

4a. Ventral sucker with circular lamellar lips embedded in aperture................... Marsupioacetabulum Yamaguti, 1952 .

4b. Ventral sucker with conspicuous bilobed flap on each lateral margin........................... Myzotus Manter, 1940 .

5a. Oral sucker with several pairs of elongate pointed processes embedded in wall of outer margin dorsally and ventrally........................................................................ Dactylotrema Bravo-Hollis & Manter, 1957 .

5b. Oral sucker not specialized as above (may possess small papillae, see Homalometron Stafford, 1904 ).................. 6.

6a. Pharynx massive, larger than ventral sucker.................................. Neomegasolena Siddiqi & Cable, 1960 .

6b. Pharynx smaller than ventral sucker..................................................................... 7.

7a. Vitelline follicles extend into forebody................................................................... 8.

7b. Vitelline follicles restricted to hindbody.................................................................. 11.

8a. Tegument unarmed; excretory pore distinctly dorso-subterminal; body length <3 times body width........................................................................... Crassicutis Manter, 1936 (Syn. Eocreadium Szidat, 1954 ).

8b. Tegument spinous (occasionally unarmed); excretory pore terminal or ventroterminal; body length usually> 3 times body width.............................................................................................. 9.

9a. Genital pore immediately anterior to ventral sucker; ovary smooth............................................. 10.

9b. Genital pore well anterior to ventral sucker; ovary deeply lobed........................... Pancreadium Manter, 1954 .

10a. Testes well separated from posterior end of body; vitelline follicles extend posteriorly beyond testes........................................................................................ Neoapocreadium Siddiqi & Cable, 1960 .

10b. Testes at posterior end of body; vitelline follicles not extending posteriorly past testes...................................................................................... Posterotestes Ostrowski de Núñez, Brugni & Flores, 2003 .

11a. Testes symmetrical; vitelline follicles restricted to post-testicular zone.................... Microcreadium Simer, 1929 .

11b. Testes tandem to oblique; vitelline follicles extend as far anteriorly as testes..................................... 12.

12a. Vitelline follicles restricted to posterior half of hindbody; uterus extensive, fills most of hindbody; testes near posterior extremity............................................................................ Procaudotestis Szidat, 1954 .

12b. Vitelline follicles extend to region of ventral sucker; uterus not extensive; testes in mid-hindbody.................... 13.

13a. Excretory vesicle short, not reaching posterior testis, opens posteroventrally; tegumental spines absent; caeca terminate midway between testes and posterior end of body; ventral sucker enclosed in tegumental pouch..................................................................................................... Callohelmis Cribb & Bray, 1999 .

13b. Excretory vesicle usually long, opens terminally; tegument usually spinous; caeca terminate near posterior end of body; ventral sucker not in pouch.................................................................................... Homalometron Stafford, 1904 (Syns. Anallocreadium Simer, 1929 ; Apocreadium Manter, 1937 ; Austrocreadium Szidat, 1956 ; Barbulostomum Ramsey, 1965 ).