Untangling convoluted taxonomy of Chambriella Rego, Chubb & Pavanelli, 1999 (Cestoda: Proteocephalidae), with erection of Riggenbachiella n. g. and the description of a new species from pimelodid catfishes in the Neotropical Region Author Philippe Vieira Alves Author Alain de Chambrier Author José Luis Luque Author Tomáš Scholz text Syst Parasitol 2017 2017-02-20 94 367 389 journal article 10.1007/s11230-017-9700-1 7c324801-2c22-439d-87c8-1bdb83e11827 925123 Riggenbachiella paranaense ( Pavanelli & Rego, 1989 ) n. comb. Syns Goezeella paranaensis Pavanelli & Rego, 1989 ; Chambriella paranaensis ( Pavanelli & Rego, 1989 ) Rego, Pavanelli & Chubb, 1999 Type- and only known host : Hemisorubim platyrhynchos (Valenciennes) ( Siluriformes : Pimelodidae ). Type-locality : River Paraná (upper reaches) near Porto Rico ( State of Paraná , Brazil ; 22 43 0S , 53 10 0W ) . Other localities : River Paraguay, San Antonio near Asunción ( Departamento Central , Paraguay ; 25 25 0S , 57 34 0W ) ; River Amazon , Iquitos (Region of Loreto , Peru ; 3 47 0S , 73 20 0W ) . Prevalence : 37% (29/79) and 8% (1/12) in H . platyrhynchos from the Paraná and Amazon basins, respectively ( Pavanelli & Santos, 1991 ; de Chambrier et al., 2015b ). Site in host : Anterior intestine. Material studied : (i) Goezeella paranaensis from Hemisorubim platyrhynchos : holotype (incomplete specimen without pregravid proglottides; CHIOC 32490), 4 paratypes (2 entire specimens and 2 slides with serial cross-sections, CHIOC 32491a, b, 32492a, b); (ii) Goezeella paranaensis from H . platyrhynchos : vouchers (6 entire specimens and 2 slides with serial cross-sections), River Paraguay, San Antonio, Central Paraguay, collected by C. Vaucher, S. Fisch-Muller and A. de Chambrier on 28.x.1989 and 27.xi.1993 (MHNG-PLAT 1951 4, 19519, host field nos. PY 6922/1, PY 8467); (iii) Chambriella paranaensis from H . platyrhynchos : vouchers (3 immature and pregravid fragments), River Amazon, Iquitos, Loreto. Peru) collected by T. Scholz on 22.iv.2004 (MHNG- PLAT 3643 0, 36431, host field nos. PI 95a, PI 95c). Redescription ( Figs. 2I , J, M–O , 5 ) [Based on 6 specimens (6 entire specimens and 2 slides with serial cross-sections).] Proteocephalidae , Monticelliinae . Testes, ovary, vitelline follicles and uterus cortical. Total body length 19–32 mm (n = 3), maximum width up to 1.2 mm (n = 4). Strobila acraspedote, anapolytic, consisting of 59–7 6 proglottids: 40–46 immature, 5–6 mature, 6–14 pregravid and 8–10 gravid. Immature proglottides wider than long (length: width ratio 0.13–0.43); mature proglottides wider than long (length: width ratio 0.35–0.86); pregravid proglottides wider than long to longer than wide (length: width ratio 0.50–1.32); gravid proglottids longer than wide (length: width ratio 1.12–2.01). Scolex 495–630 9 485–720 (n = 4), wider than proliferative zone (neck), 325–685 9 175–380, with conical apex, without apical organ. Suckers large, biloculate, 8-shaped, with both loculi similar in length; length of suckers represents up to 78% of scolex length. Anterior loculus 130–220 wide (n = 5), posterior loculus 130–205 wide (n = 5); sucker rims well developed; septum between loculi well developed ( Figs. 2I , J , 5A ). Apex of scolex covered with acicular filitriches, upper part of sucker rim and medium part between suckers with acicular filitriches interspersed with gladiate spinitriches of similar appearance and density ( Fig. 2M–O ). Inner longitudinal musculature inconspicuous ( Fig. 5F ). Osmoregulatory canals situated at different levels ( Fig. 5E, F ). Ventral canals thin-walled, wide, mediodorsal to ventral row of vitelline follicles and medioventral to lateralmost testes ( Fig. 5E, F ); dorsal canals thickwalled, dorsal to ventral row of vitelline follicles and almost lateral to lateralmost testes ( Fig. 5E, F ). Testes cortical, spherical, small, 40–70 in diameter, in 1 irregular layer, 100–174 in number ( Fig. 5B, C ), reaching to ventral row of vitelline follicles ( Fig. 5E ). Testes in 1 field, less numerous alongside median line of proglottides (uterine stem) and at level of cirrus-sac level ( Fig. 5B, C ). Vas deferens strongly coiled, with loops forming elongate field reaching and crossing median line of proglottis ( Fig. 5B, C ). Cirrus-sac sigmoid, 180–305 9 45–110 wide (n = 28), with voluminous, chambered internal seminal vesicle ( Fig. 5 B–D ); length of cirrus-sac represents 18–31% (n = 28) of proglottis width; middle part of cirrus-sac muscular, with sinuous ejaculatory duct. Cirrus short, containing inverted T-shaped ejaculatory duct in its proximal part ( Fig. 5D ); cirrus occupies up to 38% (n = 28) of cirrus-sac length. Genital pores alternating irregularly, markedly pre-equatorial, situated at 14–26% (n = 28) of proglottis length from anterior margin ( Fig. 5B, C ). Ovary cortical, bi-lobed, follicular ( Fig. 5B, C ); length representing 19–29% of proglottis length (n = 28), width representing 69–84% proglottis width (n = 28). Mehlis’ gland 6 0–96 in diameter, representing 6–7% of proglottis width (n = 15). Relative ovarian size (see de Chambrier et al., 2012 ) c .9–14% size of mature and pregravid proglottides. Vaginal canal almost straight, with terminal part ( pars copulatrix vaginae ) surrounded by chromophilic cells and welldeveloped vaginal sphincter ( Fig. 5C, D ). Vagina mainly anterior (89%) or posterior (11%, n = 28) to cirrus-sac. Vitelline follicles cortical, ventrally more numerous at ovary level, arranged in 2 wide lateral rows (usually 7 to 10 follicles at same level), reaching anterior margin of proglottis, dorsally uninterrupted ( Fig. 5B–D ). Length of bands represents 93–98% and 92–99% of proglottis length on poral and aporal side, respectively (n = 28) ( Fig. 5B, C ). Uterus cortical, with development of type 2 (see de Chambrier et al., 2004 , 2015a ). Uterus opens by elongate, slit-like pore; uterine stem appearing in mature proglottides, occupying 85–88% (n = 7) of length of pregravid proglottides. Eggs subspherical; embryophore bi-layered, 17–19 9 16 –18; oncosphere subspherical, 10–1 3 9 7–13 , embryonic hooks 6–7 long. Remarks This species was described by Pavanelli & Rego (1989) as Goezeella paranaensis from decomposed material as evidenced by the poor quality of the illustrations (see figures 6–11 in Pavanelli & Rego, 1989 ; the poor quality of the type-material was confirmed by observations of the present authors). Nevertheless, the most important genus-specific characteristics, i.e. the presence of a sigmoid cirrus-sac with three markedly different parts including a chambered internal seminal vesicle, and bi-loculate suckers could be observed in the holotype as well as in two paratypes studied ( Fig. 5D ). A new material of R. paranaense from Paraguay enabled us to redescribe this poorly known species. Riggenbachiella paranaense n. comb. differs from R. amazonense n. sp. in the following morphological characteristics: (i) the composition and anterior extent of the bands of vitelline follicles, which are narrower and composed from a fewer follicles in R. amazonense (compare Fig. 4B and Fig. 5B ), almost always absent preporally (only exceptionally, 2–4 follicles anterior to the cirrus-sac can be present in some specimens of R. amazonense vs extensive follicles always present pre-porally in R. paranaense ; compare Fig. 4B, C and Fig. 5B, C ), and usually not reaching up to the anterior margin of proglottides in R. amazonense ( vs reaching the anterior margin in R. paranaense ; compare Fig. 4B and Fig. 5B, C ); (ii) the mutual position of osmoregulatory canals, with both pairs of canals at the same level in R. amazonense ( vs dorsal canal more lateral than ventral ones in R. paranaense ; compare Fig. 4G–I and Fig. 5 E , F ); (iii) the extent of the testicular fields which may reach almost to the lateral margin of proglottides in their anterior part, both on the poral and aporal sides in R . amazonense ( vs testes reaching laterally only to the level of dorsal osmoregulatory canals, never to the lateral margin of proglottides in R . paranaense ; compare Fig. 4 B , C and Fig. 5 B , C ); and (iv) the less developed musculature of the suckers in R . amazonense , with the posterior loculus always wider than the anterior one ( vs suckers with more prominent rims and a conspicuous interlocular septum in R . paranaense ; the anterior loculus can be as wide as, or even wider than, the posterior one in R . paranaense ; compare Figs. 2E , 4A and Figs. 2I , 5A ). Table 1 List of taxa with sequences of the large subunit nuclear ribosomal RNA gene ( lsr DNA) included in the analyses

Species	Host species	Voucher accession no.	GenBank accession no.	Reference
Ageneiella brevifilis de Chambrier & Vaucher, 1999	Ageneiosus inermis (Linnaeus)	MHNG-PLAT 21841 (h)	AJ388 600	Zehnder & Mariaux (1999)
Amphoteromorphus ninoi Carfora, de Chambrier & Vaucher, 2003	Brachyplatystoma filamentosum (Lichtenstein)	MHNG-PLAT 22239 (h)	AJ388 624	de Chambrier et al. (2004)
Amphoteromorphus peniculus Diesing, 1850	Brachyplatystoma rousseauxii (Castelnau)	MHNG-PLAT 60052 (h)	KP729410	de Chambrier et al. (2015a)
Amphoteromorphus piraeeba Woodland, 1934	Brachyplatystoma filamentosum	MHNG-PLAT 22227	KP729407	de Chambrier et al. (2015a)
Amphoteromorphus piriformis Carfora, de Chambrier & Vaucher, 2003	Brachyplatystoma rousseauxii	MHNG-PLAT 22211 (h)	AJ275 231	de Chambrier et al. (2004)
Brayela karuatayi (Woodland, 1934)	Platynematichthys notatus (Jardine)	MHNG-PLAT 63128 (h)	KP729406	de Chambrier et al. (2015a)
Chambriella megacephala n. comb.	Zungaru jahu (Ihering)	MHNG-PLAT 34745 (h)	KY207447	This study
Chambriella megacephala n. comb.	Zungaro zungaro (Humboldt)	CHIOC 38484 (h)	KY207448	This study
Chambriella megacephala n. comb.	Sorubimichthys planiceps (Spix & Agassiz)	MHNG-PLAT 91863-65, 67-68, 69568, 72973 (h)	KY207449 (7 replicates)	This study
Choanoscolex abscisus (Riggenbach, 1895)	Pseudoplatystoma corruscans (Agassiz)	MHNG-PLAT 17905 (h)	AJ388 630	Zehnder & Mariaux (1999)
Choanoscolex sp.	Pseudoplatystoma fasciatum (Linnaeus)	MHNG-PLAT 25102 (h)	AJ275 0 64	de Chambrier et al. (2004)
Endorchis piraeeba Woodland, 1934	Brachyplatystoma filamentosum	MHNG-PLAT 21738 (h)	AJ388 603	Zehnder & Mariaux (1999)
Gibsoniela mandube (Woodland, 1935) Gibsoniela meursaulti de Chambrier & Vaucher, 1999	Ageneiosus sp. Ageneiosus inermis	MHNG-PLAT 63119 (h) MHNG-PLAT 21839 (h)	KP729412 AJ388 631	de Chambrier et al. (2015a) Zehnder & Mariaux (1999)
Goezeella siluri Fuhrmann , 1916	Pinirampus pirinampu (Spix & Agassiz)	MHNG-PLAT 21877 (h)	AJ388 612	Zehnder & Mariaux (1999)
Harriscolex kaparari (Woodland, 1935)	Pseudoplatystoma tigrinum (Valenciennes)	MHNG-PLAT 22018 (h)	AJ275 227	Zehnder et al. (2000)
Manaosia bracodemoca Woodland , 1935	Sorubim lima (Bloch & Schneider)	MHNG-PLAT 34186 (h)	KP729414	de Chambrier et al. (2015a)
Megathylacus jandia Woodland , 1934	Zungaro zungaro	MHNG-PLAT 21874 (h)	AJ388 596	Zehnder & Mariaux (1999)
Monticellia coryphicephala (Monticelli, 1891)	Salminus brasiliensis (Cuvier)	MHNG-PLAT 17984 (h)	AJ238 832	Zehnder & Mariaux (1999)
Nomimoscolex admonticellia (Woodland, 1934)	Pinirampus pirinampu	MHNG-PLAT 21870 (h)	AJ388 628	Zehnder & Mariaux (1999)
Nomimoscolex chubbi (Pavanelli & Takemoto, 1995)	Gymnotus carapo Linnaeus	MHNG-PLAT 20351 (h)	AJ388 625	Zehnder & Mariaux (1999)

Table 1 continued

Species	Host species	Voucher accession no.	GenBank accession no.	Reference
Nomimoscolex lenha (Woodland, 1933)	Sorubimichthys planiceps	MHNG-PLAT 21740 (h)	AJ388 611	Zehnder & Mariaux (1999)
Nomimoscolex lopesi Rego , 1989	Pseudoplatystoma fasciatum	MHNG-PLAT 21963 (h)	AJ388 618	Zehnder & Mariaux (1999)
Nomimoscolex matogrossensis Rego & Pavanelli , 1990	Hoplias malabaricus (Bloch)	MHNG-PLAT 17913 (h)	AJ388 614	Zehnder & Mariaux (1999)
Nomimoscolex sudobim Woodland , 1935	Pseudoplatystoma fasciatum	MHNG-PLAT 21969 (h)	AJ388 597	Zehnder & Mariaux (1999)
Nupelia portoriquensis Pavanelli & Rego , 1991	Sorubim lima	MHNG-PLAT 34185 (h)	KP729401	de Chambrier et al. (2015a)
Ophiotaenia europaea Odening , 1963	Natrix maura (Linnaeus)	MHNG-PLAT 18407 (h)	AJ388 598	Zehnder & Mariaux (1999)
Ophiotaenia filaroides (La Rue, 1909)	Ambystoma tigrinum (Green)	MHNG-PLAT 63372 (h)	KP729416	de Chambrier et al. (2015a)
Ophiotaenia paraguayensis (Rudin, 1917)	Hydrodynastes gigas (Duméril, Bibron & Duméril)	MHNG-PLAT 16927 (h)	AJ388 629	Zehnder & Mariaux (1999)
Ophiotaenia cf. perspicua La Rue, 1911	Nerodia rhombifer (Hallowell)	MHNG-PLAT 35370 (h)	KP729415	de Chambrier et al. (2015a)
Ophiotaenia sanbernardinensis Rudin , 1917	Helicops leopardinus (Schlegel)	MHNG-PLAT 18251 (h)	AJ388 637	Zehnder & Mariaux (1999)
Ophiotaenia saphena Osler , 1931 Peltidocotyle lenha (Woodland, 1933)	Lithobates pipiens (Schreber) Zungaro zungaro	MHNG-PLAT 32851 (h) MHNG-PLAT 22373 (h)	KP729402 AJ238 837	de Chambrier et al. (2015a) Zehnder & Mariaux (1999)
Peltidocotyle rugosa Diesing , 1850	Pseudoplatystoma reticulatum Eigenmann & Eigenmann	MHNG-PLAT 22374 (h)	AJ238 835	Zehnder & Mariaux (1999)
Proteocephalidae gen. sp.	Amia calva Linnaeus	MHNG-PLAT 35548 (h)	FM956088	de Chambrier et al. (2009)
Proteocephalus perplexus La Rue, 1911	Amia calva	MHNG-PLAT 35366 (h)	FM956089	de Chambrier et al. (2009)
Proteocephalus sp.	Ictalurus punctatus (Rafinesque)	MHNG-PLAT 36278 (h)	FM956085	de Chambrier et al. (2009)
Regoella brevis Arredondo , Gil de Pertierra & de Chambrier , 2013	Pseudoplatystoma reticulatum	MHNG-PLAT 79184 (h)	KP729389	de Chambrier et al. (2015a)
Riggenbachiella amazonense n. sp.	Phractocephalus hemioliopterus (Schneider)	MHNG-PLAT 67054, 67060 (h)	KY207450 (2 replicates)	This study
Riggenbachiella amazonense n. sp.	Sorubimichthys planiceps	MHNG-PLAT 60046, 60048, 91866 (h)	KY207451 (3 replicates)	This study
Spasskyellina lenha (Woodland, 1933)	Sorubimichthys planiceps	MHNG-PLAT 69600 (h)	KP729413	de Chambrier et al. (2015a)
Spasskyellina spinulifera (Woodland, 1935)	Pseudoplatystoma corruscans	MHNG-PLAT 34216 (h)	KP729417	de Chambrier et al. (2015a)

Table 1 continued

Species	Host species	Voucher accession no.	GenBank accession no.	Reference
Spatulifer maringaensis Pavanelli & Rego , 1989	Sorubim lima	MHNG-PLAT 21986 (h)	AJ388 634	de Chambrier et al. (2004)
Testudotaenia testudo (Magath, 1924)	Apalone spinifera (Le Sueur)	MHNG-PLAT 35320 (h)	FM956082	de Chambrier et al. (2009)
Jauella glandicephalus Rego & Pavanelli , 1985 (out)	Zungaro jahu	MHNG-PLAT 31179 (h)	KP729399	de Chambrier et al. (2015a)
Nomimoscolex dorad (Woodland, 1935) (out)	Brachyplatystoma rousseauxii	MHNG-PLAT 22269 (h)	AJ388 613	Zehnder & Mariaux (1999)
Nomimoscolex piraeeba Woodland , 1934 (out)	Brachyplatystoma capapretum Lundberg & Akama	MHNG-PLAT 22284 (h)	AJ388 608	Zehnder & Mariaux (1999)
Nomimoscolex suspectus Zehnder, de Chambrier, Vaucher & Mariaux , 2000 (out)	Brachyplatystoma vaillanti (Valenciennes)	MHNG-PLAT 22298 (h)	AJ388 602	de Chambrier et al. (2004)

Abbreviations : out, outgroup; h, hologenophore sensu Pleijel et al. (2008) Ethanol-fixed material of R. paranaense from Paraguay has been lost and repeated attempts of the present authors to find new specimens in the typehost near the type-locality (River Paraná near Porto Rico ) failed. Therefore, no molecular data on this species are available. Brooks (1 9 9 5) transferred G . paranaensis to Spatulifer Woodland , 1 9 3 4 as S . paranensis [sic!] based on a cladistics analysis inferred from morphological characters, but this new combination was not accepted by subsequent authors.