This paper represents an update of the previous list of adult proteocephalidean tapeworms (Cestoda) parasitizing freshwater teleosts from the Peruvian Amazon, which was presented by de Chambrier et al. (2006a). Four new samplings made it possible to almost double the number of species found, all of them representing new geographical records from Peru. With 34 newly added species, a total of 63 proteocephalidean cestodes (46 named species of 27 genera) are now reported from Amazonia in Peru (compared to 54 named species of 28 genera from its Brazilian part). The genera previously unreported by de Chambrier et al. (2006a) are Ageneiella, Brayela, Endorchis, Ephedrocephalus, Gibsoniela, Harriscolex, Jauella, Lenhataenia, Manaosia, and Megathylacus. Four species, namely Jauella glandicephalus, Monticellia belavistensis, M. santafesina, and Proteocephalus hobergi, are reported from the Amazon River basin for the first time. Harriscolex piramutab (Woodland, 1934) n. comb. is proposed for specimens previously identified as Proteocephalus piramutab Woodland, 1934 from Brachyplatystoma vaillantii. The highest number of proteocephalidean cestodes is reported from Pseudoplatystoma fasciatum (a total of 10 cestode species), Zungaro zungaro (previously named Paulicea luetkeni; 9 species) and Phractocephalus hemioliopterus (6 species). A high number of unnamed species found in Peru (17), which most probably represent taxa new to science including at least two new genera, demonstrates that the species richness of proteocephalidean cestodes in Amazonia is still poorly known.
INTRODUCTION
The Amazon River basin is by far the largest river basin in the world and drains roughly 40 percent of the South American continent. This river basin hosts the most diverse fish fauna in planet, with about 2,500 species described and another 1,000 species estimated to be described (Junk et al., 2007). However, recent large-scale environmental degradation due to anthropogenic pressure such as deforestation, water pollution, overfishing and intensive farming has had negative effect on water ecosystems, including considerable decrease of population density of big pimelodid catfishes (Siluriformes) in the Brazilian part of Amazonia (Angelini et al., 2006; Pelicice & Agostinho, 2008; Boni et al., 2011; Reis, 2013).
These fishes serve as definitive hosts of a unique rich fauna of proteocephalidean tapeworms (Cestoda) that probably underwent explosive radiation and represent an interesting model for co-evolutionary studies because of strict host specificity of most taxa (de Chambrier & Vaucher, 1997, 1999; Zehnder & Mariaux, 1999; de Chambrier et al., 2004a; Hypša et al., 2005). Unlike most parts of the Brazilian Amazonia, in which population density of big catfish has declined (Angelini et al., 2006; Pelicice & Agostinho, 2008), numerous stocks of these fishes including pimelodids still inhabit the Peruvian part of the Amazon River basins.
Parasitological examination of 276 fishes of 73 species from the Amazon River and its tributaries around Iquitos, Loreto Region in Peru, carried out by the present authors and their co-workers in 2004 and 2005, revealed an extraordinary richness of proteocephalidean tapeworms, which were all reported from Peru for the first time (de Chambrier & Scholz, 2005; de Chambrier et al., 2006a). De Chambrier et al. (2006a) listed as many as 29 species of 17 genera found in 10 species of siluriform fishes and cichlids. New sampling in this region in 2006, 2008, 2009 and 2011 made it possible to obtain additional material that includes many cestodes not having been previously reported from Peru or from the Amazon River basin; some may even be new to science. To provide a robust baseline for forthcoming analyses of zoogeographical patterns and phylogenetic relationships of proteocephalideans in the Neotropical Region, updated information is presented on the species composition, host-parasite associations and geographical distribution of these cestodes, which represent an important component of the parasite fauna of Neotropical fishes (Thatcher, 2006).
MATERIAL AND METHODS
A total of 611 fish from the Amazon River and its tributaries around Iquitos (72°50′-73°40′W; 3°34′-4°53′S), Loreto Region, Peru, were examined for parasites in September 2006 and 2008, and in October 2009 and 2011. Intestines of freshly captured hosts as well as those sold on the market of Belén in Iquitos were transported in coolers to the provisional laboratory (courtesy of Acuario Río Momón in Iquitos), where they were immediately examined. For morphological evaluation, only specimens in good condition were used, but quantitative parameters such as intensity or abundance could not be reliable assessed.
Cestodes were gently washed in saline, fixed with hot (almost boiling) 4% formaldehyde solution and then processed using standard procedure used for fish tapeworms as described by de Chambrier et al. (2014). Fragments of strobila were also fixed with 96% molecular-grade ethanol for molecular analyses (DNA sequencing), which forms part of a large-scale study on the phylogenetic relationships of cestodes supported by the National Science Foundation project (programme Planetary Biodiversity Inventory; see www.tapeworm.uconn.edu). In the present paper, scanning electron micrographs (SEM) of the scoleces of five species are provided (Figs 1-5); these species were not studied using SEM or their SEM pictures were based on contracted or deformed specimens.
Most specimens found are deposited in the Natural History Museum, Geneva, Switzerland (MHNG-PLAT), which hosts one of the most comprehensive collections of proteocephalidean cestodes ( http://www.ville-ge.ch/ mhng/dpt_inve_coll_e.php#platyhelminthes). See Table 1 for more details. Classification of cestodes, including original descriptions of taxa, follows the Global Cestode Database (Caira et al., 2012). However, the recently erected order Onchoproteocephalidea, which groups the proteocephalideans and some ‘hooked’ tetraphyllidean cestodes (see Caira et al., 2014), is not considered herein for the reasons presented by Arredondo et al. (2014), especially because no morphological synapomorphies of the new order were provided by Caira et al. (2014). Field numbers correspond to the numbers of fish examined in field protocols (PI = Peru, Iquitos, Loreto Region, Peru; letters after host number distinguish different worm samples). Since 2008, every fish dissected was photographed together with its field number (PI); in 2009 and 2011, tissue samples, usually a small piece of musculature, of every infected fish were taken and fixed with 96% molecular-grade ethanol for future DNA sequencing to confirm host identification. Photographs of fishes and their tissue samples are available upon request from the authors. Names of teleosts follow those in FishBase (Froese & Pauly, 2014) and PlanetCatfish ( http://www.planetcatfish.com) except for Brachyplatystoma rousseauxii (Castelnau), which was erroneously reported as B. flavicans (Castelnau) by de Chambrier et al. (2006a) following Fishbase (see Lundberg and Akama, 2005; http://www.planetcatfish.com/). In addition, Zungaro zungaro (Humboldt) was wrongly reported as Paulicea luetkeni (Steindachner) (for current nomenclature, see Froese & Pauly, 2014; John Lundberg, pers. comm.).
RESULTS
Survey of species found
Species not reported by de Chambrier et al. (2006a) are marked by an asterisk (*); species reported by de Chambrier et al. (2006a), but not found in 2006-2011, are also listed herein to provide a complete list of cestodes found. Collection numbers refer to the Natural History Museum, Geneva, Switzerland – MHNG-PLAT, unless otherwise stated. Cestode taxa are listed alphabetically.
Ageneiella sp.*
Host: Ageneiosus inermis (L.) (1 fish infected of 16 fish examined, i.e. prevalence of 6%).
Remarks: Specimens found in A. inermis are partly decomposed and contracted, which impedes their reliable identification to the species level. However, they apparently belong to an undescribed species of Ageneiella de Chambrier & Vaucher, 1999, a hitherto monotypic genus proposed to accommodate A. brevifilis de Chambrier & Vaucher, 1999 from Ageneiosus brevifilis (L.) (synonym of A. inermis) from Paraguay by de Chambrier & Vaucher (1999). They possess biloculate suckers with a sphincter and lateral lobes of the ovary penetrating into the cortex (see de Chambrier & Vaucher, 1999).
Immature cestodes were found in two additional Ageneiosus sp., but their identification is not possible.
Amphoteromorphus ovalis Carfora, de Chambrier & Vaucher, 2003*
Host: Brachyplatystoma cf. filamentosum (Lichtenstein); 1/3, 33%).
Figs 1-5.
Scanning electron micrographs of representative scoleces of proteocephalidean cestodes found in the Peruvian Amazon. (1) Nomimoscolex lopesi from Pseudoplatystoma fasciatum (PI 708). (2) Proteocephalus sp. 2 from Pterodoras granulosus (PI 635). (3) Jauella glandicephalus from Zungaro zungaro. (4) Proteocephalus kuyukuyu from Megalodoras uranoscopus (PI 324). (5) Spatulifer rugosa from P. fasciatum (PI 708). 1, 3, 5 = lateral view; 2, 4 = dorsoventral view.
Amphoteromorphus parkamoo Woodland, 1935
Host: Zungaro zungaro (3/30, 10%).
Remarks: Redescribed by Carfora et al. (2003), who confirmed the validity of the species.
Amphoteromorphus peniculus Diesing, 1850* Host: Brachyplatystoma rousseauxii (1/3, 33%).
Amphoteromorphus piriformis Carfora, de Chambrier & Vaucher, 2003
Host: Brachyplatystoma rousseauxii (1/3, 33%).
Remarks: A. piriformis was described from B. rousseauxii collected in Itacoatiara, Brazil in September 1992 and October 1995 (Carfora et al., 2003).
Brayela karuatayi (Woodland, 1934)*
Host: Platynematichthys notatus (Jardine) (5/13, 38%).
Remarks: This species, which had never been found since its original description by Woodland (1934a), has recently been redescribed by de Chambrier et al. (2014) on the basis of new material collected in Peru. The authors also described correctly its scolex morphology and provided the evidence that the actual fish host of this cestode is P. notatus, not ‘Glanidium sp.’ as reported in the original description (see de Chambrier et al., 2014).
Chambriella agostinhoi (Pavanelli & Machado dos Santos, 1992)
Host: Zungaro zungaro (11/30, i.e. 37%).
Chambriella paranaensis (Pavanelli & Rego, 1989)
Host: Hemisorubim platyrhynchos (1/12, 8%).
Remarks: de Chambrier et al. (2006a) designated this species erroneously as the type species of Chambriella Rego, Chubb & Pavanelli, 1999. Rego et al. (1999) actually did not explicitly mention the type species of the genus in its generic diagnosis on p. 314, but C. agostinhoi was mentioned as the type species of the genus in remarks to that species (Rego et al., 1999: 317).
Chambriella sp. 1*
Host: Brachyplatystoma vaillantii (Valenciennes) (4/39, 10%).
Remarks: This cestode is a rare parasite of B. vaillantii.
Chambriella sp. 2 (= Chambriella sp. of de Chambrier et al., 2006a)
Host: Phractocephalus hemioliopterus (Bloch & Schneider) (5/10, 50%).
Chambriella sp. 3*
Host: Pseudoplatystoma fasciatum (7/42, 17%).
Chambriella sp. 4*
Host: Sorubimichthys planiceps (Spix & Agassiz) (6/22, 27%).
Remarks: de Chambrier & Scholz (2008) reported but did not describe the morphology of this species, which may be new to science, similarly as the three species listed above (Chambriella spp. 1-3). Their taxonomic study is in preparation and will be presented in a separate account.
Choanoscolex abscisus (Riggenbach, 1896)
Host: Pseudoplatystoma fasciatum (14/42, 33%).
Remarks: Compared to de Chambrier et al. (2006a), new collections enabled us to obtain sufficient material of this cestode, which has been found in a wide spectrum of unrelated fish hosts (Rego, 1987, 1990; Rego & Pavanelli 1990; Rego et al., 1999).
In its strobilar morphology, the species closely resembles Spatulifer surubim Woodland, 1934 from the same fish host, differing only in a much less developed metascolex. However, some intermediate forms with a more developed metascolex were found, which indicates that differences between these taxa of two different genera should be critically assessed. Molecular data also indicate close relatedness of S. surubim and C. abscisus from P. fasciatum (A. Waeschenbach, unpubl. data).
Choanoscolex sp.*
Host: Sorubimichthys planiceps (3/22, 14%).
Remarks: de Chambrier & Scholz (2008) reported cestodes of the genus Choanoscolex La Rue, 1911 that differ from those of C. abscisus, the only species of the genus (see above).
Endorchis piraeeba Woodland, 1934*
Host: Brachyplatystoma cf. filamentosum (1/3, 33%).
Remarks: At present, the genus includes E. piraeeba from B. filamentosum and Endorchis auchenipteri de Chambrier & Vaucher, 1999 from Auchenipterus osteomystax (Miranda Ribeiro) from the Paraná River in Paraguay (de Chambrier & Vaucher, 1999). In addition, de Chambrier & Vaucher (1999) reported unidentified cestodes of Endorchis from Pimelodus cf. maculatus Lacépède and Trachelyopterus striatulus (Steindachner) from Paraguay.
An immature specimen with a similar scolex was found in Pseudoplatystoma fasciatum (1/42, i.e. 2%).
Endorchis sp.*
Host: Pimelodus altissimus Eigenmann & Pearson (1/1).
Remarks: These specimens resemble those of E. auchenipteri but their large-sized Mehlis gland is unique among the Proteocephalidea.
Euzetiella tetraphylliformis de Chambrier, Rego & Vaucher, 1999
Host: Zungaro zungaro (5/30, 17%).
Remarks: Worms collected in 2009 were immature, but are supposed to belong to the only known species of the genus, which was described from the same host in Itacoatiara, Brazil (de Chambrier et al., 1999). One immature specimen was also found in Pseudoplatystoma fasciatum.
Gibsoniela mandube (Woodland, 1935)*
Host: Ageneiosus inermis (2/16, 13%), Ageneiosus sp. (3/10, 30%).
Remarks: The species was described as Anthobothrium mandube Woodland, 1935, (Phyllobothriidae) and transferred to Gibsoniela Rego, 1984 by Rego (1984). From the same host (A. inermis) and same locality (Amazon River in Brazil), Woodland (1935a) described Endorchis mandube, but Rego (1984) suggested that both species may be synonymous and de Chambrier (1990) confirmed this synonymy.
However, de Chambrier & Vaucher (1999) studied the type material and newly collected specimens of both taxa from the Amazon River and concluded that they represent two distinct species of the same genus. To avoid their homonymy, they proposed Gibsoniela meursaulti de Chambrier & Vaucher, 1999 to accommodate Endorchis mandube; tapeworms redescribed by Rego (1992) as G. mandube actually belonged to G. meursaulti (de Chambrier & Vaucher, 1999).
Harriscolex kaparari (Woodland, 1935)*
Host: Pseudoplatystoma fasciatum (3/42, 7%).
Remarks: Described as Nomimoscolex kaparari Woodland, 1935 by Woodland (1935a) from Pseudoplatystoma tigrinum (Valenciennes) in Brazil.
Harriscolex piramutab (Woodland, 1934) n. comb.
Host: Brachyplatystoma vaillantii (8/39, 20%).
Remarks: de Chambrier et al. (2006a) reported Proteocephalus piramutab Woodland, 1934 from Brachyplatystoma vaillantii. A detailed morphological study of newly collected specimens and material of Proteocephalus piramutab from museum collections, and their comparison with those of H. kaparari, revealed that the former species should be transferred to Harriscolex Rego, 1987, because it possesses a scolex with a dome-shaped anterior end and suckers with two triangular projections (see Rego, 1994). Therefore, a new combination, Harriscolex piramutab, is proposed for specimens previously identified as P. piramutab, including those reported from Peru by de Chambrier et al. (2006a).
Houssayela sudobim (Woodland, 1935)
Host: Pseudoplatystoma fasciatum (3/42, 7%).
Remarks: Described as Myzophorus sudobim Woodland, 1935 from P. fasciatum from the Amazon River in Brazil by Woodland (1935b) and found and redescribed by de Chambrier & Scholz (2005) for the first time since original description on the basis of a single specimen from P. fasciatum in Iquitos (PI 76a – 22. 4. 2004).
Jauella glandicephalus Rego & Pavanelli, 1985* Fig. 3
Host: Zungaro zungaro (9/30, 30%).
Remarks: Described from Zungaro jahu (Ihering) (as Paulicea luetkeni) from the Paraná River in Brazil by Rego & Pavanelli (1985). This is the first record of the parasite in the Amazon River basin.
Lenhataenia megacephala (Woodland, 1934)*
Host: Sorubimichthys planiceps (11/22, 50%).
Remarks: The genus was erected by de Chambrier & Scholz (2008) to accommodate Monticellia megacephala Woodland, 1934, which is a common, host-specific parasite of S. planiceps.
Manaosia bracodemoca Woodland, 1935*
Host: Sorubim lima (Bloch & Schneider) (3/29, 10%).
Remarks: The species was described by Woodland (1935a) from ‘Platysoma sp.’ (vernacular name ‘braço de moça’) in the Amazon River in Brazil. De Chambrier (2003) clarified the systematic position of this species, which is a rare parasite of S. lima. He considered Paramonticellia Pavanelli & Rego, 1991 to be a junior synonym of Manaosia Woodland, 1935.
Mariauxiella piscatorum de Chambrier & Vaucher, 1999
Host: Hemisorubim platyrhynchos (2/12, i.e. 17%).
Remarks: This species was found only in 2004 (de Chambrier et al., 2006a).
Megathylacus jandia Woodland, 1934*
Host: Zungaro zungaro (2/30, 7%).
Remarks: This species was originally identified as Megathylacus brooksi Rego & Pavanelli, 1985, but a detailed study of type and new material of Megathylacus cestodes from the Amazon and Paraná River basins (de Chambrier et al., 2014) has demonstrated conspecifity of this species with M. jandia, which was described by Woodland (1934a) from the Amazon River in Brazil.
Megathylacus sp.*
Host: Pseudoplatystoma fasciatum (4/42, 10%).
Remarks: These cestodes from P. fasciatum differ from Megathylacus travassosi by a few morphological characters and potentially belong to a new species. This species was collected also in 2004, but not reported by de Chambrier et al. (2006a).
Monticellia amazonica de Chambrier & Vaucher, 1997
Host: Calophysus macropterus (Lichtenstein) (5/33, 15%).
Remarks: Scholz et al. (2008) redescribed the species on the basis of specimens found in Iquitos, Peru in 2005.
Monticellia belavistensis Pavanelli, Machado dos Santos, Takemoto & dos Santos, 1994*
Host: Pterodoras granulosus (Valenciennes) (1/24, 4%).
Remarks: This cestode, which was described by Pavanelli et al. (1994) from P. granulosus from the Paraná River basin in Brazil and then reported by de Chambrier & Vaucher (1999) from the Paraguay River in Paraguay, was found in Peru only once. It is the first record of this species from the Amazon River basin.
Monticellia lenha Woodland, 1933*
Host: Sorubimichthys planiceps (13/22, 59%).
Remarks: Originally described by Woodland (1933) from specimens found in S. planiceps, and redescribed by de Chambrier & Scholz (2008), who studied type specimens and new material from Iquitos collected in 2006 (see Table 2). It is a specific and the most frequent parasite of S. planiceps.
Monticellia santafesina Arredondo & Gil de Pertierra, 2010*
Host: Megalonema platycephalum Eigenmann (1/1).
Remarks: Described from Megalonema platanum (Günther) from the Paraná River basin in Argentina (Arredondo & Gil de Pertierra, 2010). This is the first geographical record of this cestode from the Amazon River basin. M. platycephalum represents a new definitive host of the parasite.
Monticellia ventrei de Chambrier & Vaucher, 1999*
Host: Pinirampus pirinampu (Spix & Agassiz) (4/30, 13%).
Remarks: Monticellia ventrei was described by de Chambrier & Vaucher (1999) from specimens found in P. pirinampu from the Paraguay River in Paraguay. Specimens found in Peru represent a new geographical record and expand the distribution area of the species to include the Amazon River basin.
Nomimoscolex admonticellia (Woodland, 1934)*
Host: Pinirampus pirinampu (11/30, 37%).
Remarks: This is a relatively common parasite specific of P. pirinampu, which was originally described by Woodland (1934b) from Pinirampus sp. from the Amazon River near Itacoatiara, Brazil.
Nomimoscolex lenha (Woodland, 1933)*
Host: Sorubimichthys planiceps (5/22, 23%).
Remarks: de Chambrier & Scholz (2008) redescribed the species based on 2 specimens they collected in Itacoatiara, Brazil in 1995 and 1 specimen from Iquitos, Peru in 2006. Interestingly, the prevalence of N. lenha in Brazil (22%, n = 9; see de Chambrier & Scholz, 2008) was almost identical to that in the same host from Peru.
Nomimoscolex lopesi Rego, 1989 Fig. 1
Host: Pseudoplatystoma fasciatum (11/42, 26%).
Remarks: This species was studied using scanning electron microscopy for the first time (Fig. 1).
Nomimoscolex sudobim Woodland, 1935
Host: Pseudoplatystoma fasciatum (10/42, 24%).
Remarks: Also found in P. tigrinum from Peru by de Chambrier et al. (2006a). The species was redescribed by de Chambrier et al. (2006b).
Nomimoscolex suspectus Zehnder, de Chambrier, Vaucher & Mariaux, 2000*
Host: Brachyplatystoma cf. filamentosum (1/3, 33%).
Remarks: Described from tapeworms found in Brachyplatystoma filamentosum (type host), B. flavicans (now B. rousseauxii) and B. vaillantii from the Amazon River in Brazil (Zehnder et al., 2000); it was found in Peru only once.
Nomimoscolex sp.*
Host: Pimelodus ornatus Kner (2/13, 15%).
Remarks: These cestodes differ from N. microacetabula Gil de Pertierra, 1995 by a few morphological characters and potentially belong to a new species.
Nupelia sp.
Host: Goeldiella eques (Müller & Troschel) (3/28, 11%).
Remarks: Despite great efforts to collect more material allowing for its description, only one additional specimen from this species was found since 2005 (see de Chambrier et al., 2006a). These tapeworms are mainly characterized by extraordinarily wide ventral osmoregulatory canals.
Peltidocotyle lenha (Woodland, 1933)
Hosts: Sorubimichthys planiceps (13/22, 59%); Zungaro zungaro (13/30, 43%).
Remarks: de Chambrier & Scholz (2008) reported the species from the type host, S. planiceps. Zungaro zungaro is another host of the tapeworm (Zehnder & de Chambrier, 2000).
Peltidocotyle rugosa Diesing, 1850*
Host: Pseudoplatystoma fasciatum (10/42, 24%).
Remarks: de Chambrier et al. (2006a) did not report this frequent parasite of P. fasciatum.
Proteocephalus gibsoni Rego & Pavanelli, 1991
Host: Astronotus ocellatus (1/4, 25%).
Proteocephalus hemioliopteri de Chambrier & Vaucher, 1997*
Host: Phractocephalus hemioliopterus (1/10, 10%).
Remarks: de Chambrier & Vaucher (1997) proposed a new name, Proteocephalus hemioliopteri, for Myzophorus woodlandi Rego, 1984 [syn. Nomimoscolex woodlandi (Rego, 1984) Rego & Pavanelli, 1992]; de Chambrier et al. (2005) redescribed this species, which was found only once in Peru.
Proteocephalus hobergi de Chambrier & Vaucher, 1999*
Host: Oxydoras niger (Valenciennes) (1/16, 6%).
Remarks: de Chambrier & Vaucher (1999) described the species from Oxydoras kneri Bleeker from the Paraná and Paraguay rivers in Paraguay. The specimens found in Peru represent new host and geographical records and the first report of the species from the Amazon River basin.
Proteocephalus kuyukuyu Woodland, 1935* Fig. 4
Hosts: Megalodoras uranoscopus (Eigenmann & Eigenmann) (3/4, 75%); Pterodoras granulosus (2/24, 8%); Pterodoras sp. (1/1).
Remarks: This parasite of doradid catfishes was described by Woodland (1935c) from the kuyukuyu, vernacular name of Oxydoras niger (as Pseudodoras niger), from Codajaz, Brazil. Even though Woodland (1935c) found over 50 specimens, no one was mature. The same situation was observed in Peru and none of 347 cestodes found was fully mature. This may indicate hyperapolytic development, i.e. release of proglottids precociously before they contain any eggs, which then complete their development while free in the intestine of the host (see glossary in Khalil et al., 1994), but no free proglottids were found in hosts infected with immature cestodes.
Proteocephalus macrophallus (Diesing, 1850)
Host: Cichla monoculus (2/15, 13%).
Proteocephalus microscopicus Woodland, 1935
Host: Cichla monoculus (6/15, 40%).
Remarks: Both species, similarly as P. gibsoni from another cichlid (see above), were not found since 2005 because no other hosts, C. monoculus and A. ocellatus, were examined.
Proteocephalus sophiae de Chambrier & Rego, 1994*
Host: Zungaro zungaro (6/30, 20%).
Remarks: This is a host-specific parasite of the Z. zungaro, described from the Amazon River in Brazil by de Chambrier & Rego (1994).
Proteocephalus sp. 1 of de Chambrier et al. (2006a)
Host: Phractocephalus hemioliopterus (2/10, 20%).
Remarks: Only immature specimens have been found.
Host: Pterodoras granulosus (2/24, 8%).
Remarks: Additional immature specimens were found in 5 P. granulosus and possibly belong to the same taxon.
Proteocephalus sp. 3*
Host: Pimelodus blochii Valenciennes (2/8, 25%).
Remarks: All specimens are immature.
Rudolphiella piracatinga (Woodland, 1935)
Host: Calophysus macropterus (10/33, 30%).
Rudolphiella sp.*
Host: Pinirampus pirinampu (5/30, 17%).
Remarks: These cestodes differ from both R. myoides Woodland, 1934 and R. piranabu Woodland, 1934 from the same host in Brazilian Amazon and potentially belong to a new species.
Scholzia emarginata (Diesing, 1850)
Host: Phractocephalus hemioliopterus (10/10, 100%).
Remarks: This is the most frequent specific parasite of P. hemioliopterus.
Sciadocephalus megalodiscus Diesing, 1850
Host: Cichla monoculus (1/15, 7%).
Remarks: Woodland (1933b) redescribed this taxa established by Diesing (1850), based on his material collected in the Amazon River in 1931. Rego et al. (1999) reported this species from the Paraná River basin and amended a generic diagnosis.
Spasskyellina spinulifera (Woodland, 1935)
Hosts: Pseudoplatystoma fasciatum (12/42, 29%), P. tigrinum (Valenciennes) (2/13, 14%; no new material found since 2005).
Remarks: This species was originally described as Monticellia spinulifera by Woodland (1935b) from P. fasciatum from the Amazon River in Brazil. Freze (1965) proposed a new genus, Spasskyellina, to accommodate this species. De Chambrier & Vaucher (1999) synonymized the genus with Monticellia, but later de Chambrier et al. (2006a) listed Spasskyellina as a valid genus, ignoring the previous paper from 1999. Three species of Pseudoplatystoma, namely P. corruscans, P. fasciatum and P. tigrinum, from the Amazon and Paraná River basins in Peru, Brazil and Paraguay serve as definitive hosts of S. spinulifera (Woodland, 1935b; Rego, 1990; de Chambrier & Vaucher, 1999; de Chambrier et al., 2006a; present study).
Spatulifer maringaensis Pavanelli & Rego, 1989
Host: Hemisorubim platyrhynchos (Valenciennes) (2/12; 17%); Sorubim lima (3/29, 10%).
Remarks: Originally described from H. platyrhynchos and found by de Chambrier et al. (2006a) in the same host from Peru. Arredondo & Gil de Pertierra (2008) confirmed that tapeworms from this catfish and S. lima from the Paraná River basin are conspecific, which was supported by the present study.
Spatulifer rugosa (Woodland, 1935) Fig. 5
Host: Pseudoplatystoma fasciatum (14/42, 33%).
Remarks: Described as Monticellia rugosa from P. fasciatum from the Amazon River, Brazil by Woodland (1935a), who reported prevalence of 55%.
Spatulifer sp. (probably S. surubim Woodland, 1934)
Host: Pseudoplatystoma tigrinum (1/13, 8%).
Remarks: Only immature specimens were found; see de Chambrier et al. (2006a).
Travassiella jandia (Woodland, 1934)
Host: Zungaro zungaro (1/30, 3%).
Remarks: de Chambrier et al. (2014) synonymized Travassiella avitellina Rego & Pavanelli, 1987 described from Zungaro zungaro (in fact Zungaro jahu, see Lundberg & Littmann, 2003) with Proteocephalus jandia Woodland, 1934 described from Z. zungaro from the Amazon River in Brazil and proposed a new combination, T. jandia (Woodland, 1934). This is the rarest species found in Z. zungaro in Peru.
No new specimens were found since 2004 (see de Chambrier et al., 2006a).
Zygobothrium megacephalum Diesing, 1850
Host: Phractocephalus hemioliopterus (1/10, 10%).
Monticelliinae gen. sp.*
Host: Phractocephalus hemioliopterus (1/10, 10%).
Remarks: This material differs from all known species of the Monticelliinae and potentially belong to a new species and genus.
Proteocephalidea gen. sp.*
Host: Cichlasoma amazonarum Kullander (3/29, 10%).
Remarks: This material differs from all known species of the Proteocephalidae and potentially belong to a new species and genus.
DISCUSSION
Our four recent sampling trips in the Peruvian Amazon enable us to double the number of proteocephalidean cestodes reported in 25 species of fishes of the upper part of the Amazon River around Iquitos. Besides the 29 proteocephalidean species found in 8 species of pimelodid, 1 heptapterid and 1 doradid catfishes, and 2 species of cichlids, the present account adds another 34 species, thus providing evidence of the occurrence of as many as 63 species of these cestodes in Peru. Out of them, 46 species could be identified to the species level and represent already known taxa. This is only slightly less than the known fauna of the Brazilian part of Amazonia, from which 54 species have been reported (Table 1). However, more than a dozen species found only in Peru are probably new taxa awaiting formal description. In total, as many as 64 named species of proteocephalidean cestodes are now known from the Amazon River basin (Table 1).
Unlike Peru, with almost no history of studies on cestode parasites of freshwater teleosts, research on fish parasites in the Brazilian part of the Amazon River basin started as early as in the 19th century, when Diesing (1850) described several taxa based on material collected by an Austrian naturalist and explorer Johann Natterer, who spent 18 years in Brazil from 1817 to 1835. More systematic studies on proteocephalidean cestodes started in the early 1930's when W.N.F. Woodland published 9 papers with descriptions of 32 species and 8 genera of proteocephalidean cestodes from catfishes and other teleost fishes in the Amazon River in Brazil (de Chambrier et al., 2014). After a couple of decades since Woodland's pioneer studies, Brazilian authors, especially A.A. Rego, studied the cestode fauna of fishes in Brazil (see Rego et al., 1999 for references), even though many of the studies were carried out in the Paraná River basin (Rego & Pavanelli, 1992; Fig. 6). Since the mid 1990's, the senior author with co-authors have also contributed considerably, with a number of papers dealing with proteocephalideans from the Brazilian Amazon (see de Chambrier et al., 2006a, 2014 and references therein). From the Amazon River basin in Peru, de Chambrier et al. (2006a) reported 5 species of proteocephalideans from Pseudoplatystoma fasciatum and Paulicea luetkeni (= Zungaro zungaro) each, and 4 species in Phractocephalus hemioliopterus and Pseudoplatystoma tigrinum. In the present study, much higher numbers of cestodes were found in these hosts: 10 (and juveniles of 2 other species) in P. fasciatum (plus one unidentified species; 7 of these species were also reported from Brazilian Amazonia), 9 in Z. zungaro (1 unidentified species) and 6 in P. hemioliopterus (1 unidentified species). As typical for proteocephalidean cestodes in the Neotropical Region (e.g., de Chambrier & Vaucher, 1999), most species are specific to a single fish host, more rarely to congeneric host species. In the present study, 9 species were found in more than one fish host and only 2 species, namely Proteocephalus kuyukuyu and Spatulifer maringaensis, occur in fish of more than one genus (Table 2). However, there could be a sampling bias, considering that the number of dissected hosts per species varied considerably, from 1 to 42 specimens (Table 2). Pseudoplatystoma fasciatum was the most frequently examined host and also harboured the highest number of species of proteocephalideans.
Extensive material of proteocephalidean cestodes was collected in a wide spectrum of teleosts during six visits by the present authors and their co-workers to the Peruvian Amazonia. This material will make it possible to compare the species composition of the cestode fauna and host-parasite associations in the Amazon River basin with those in the Paraná River basin (Fig. 6). Some proteocephalideans occur in closely related hosts from different river basins, such as Proteocephalus macrophallus and P. microscopicus in species of Cichla Bloch & Schneider, 1801, or in recently separated ‘couples’ of fish hosts that occur only in one of the two principal river basins in South America, i.e. Amazon and Paraná, such as Zungaro zungaro in the former river basin and Z. jahu in the latter one.
Table 1.
List of species of proteocephalidean cestodes found in fishes from the Amazon River basin.
Table 2.
List of fish hosts and their proteocephalidean cestodes found in the Peruvian Amazonia, with values of prevalence. Cestode species found in 2006-2011, but not reported by de Chambrier et al. (2006a), in bold.
In the present study, we focused on adult cestodes and thus only very few proteocephalidean larvae (merocercoids, see Chervy, 2002) were found. The identification of the latter based on morphological characteristics is impossible, but their molecular analysis will enable us to match their DNA sequences with those of adults, which were obtained in the framework of a NSF-PBI project “A Survey of the Tapeworms (Cestoda: Platyhelminthes) from the Vertebrate Bowels of the Earth” ( www.tapeworms.uconn.edu). This approach (see also Jensen & Bullard, 2010) is the most feasible way to elucidate life cycles of Neotropical proteocephalideans, which are almost completely unknown. Based on the fact that large catfishes are predatory (piscivorous) and do not consume plankton, it is reasonable to assume that life cycles of many, if not most, proteocephalidean cestodes that mature in large catfishes in South America include two intermediate (or one intermediate and one paratenic) hosts, the second host being small planktonophagous fish similarly to the developmental cycles of Proteocephalus ambloplitis in North America (Hunter, 1928; Freze, 1965; Scholz, 1999; Scholz & de Chambrier, 2003). To summarize, the present study enriched considerably the current knowledge of the species composition and distribution areas of members of one of the dominant groups of metazoan parasites of freshwater teleosts in the Neotropical Region. However, there are still many fish hosts that have never been examined for parasites and thus a number of new taxa probably remain to be discovered. This will depend on sampling effort and time dedicated to future collecting trips and taxonomic evaluation of newly collected cestodes, using combined morphological and molecular approaches. A recent discovery of a new genus from the little known auchenopterid catfish Tocantinsia piresi from the Xingú River in Brazil (Alves et al., 2015) as well as the number of unidentified species found in Peru, which may represent new species, supports the argument that we are just at the very beginning of a long path towards representative mapping the species diversity, host-parasite relationships and zoogeography of the parasites of teleost fishes in one of the hottest spots of fish parasite diversity on the Earth. Since the existence of cryptic species among proteocephalidean cestodes cannot be excluded, it is impossible to provide a reliable estimate of the species richness of these parasites. However, it is reasonable to assume that the actual number of extant species would be at least twice as high as the number of the species currently considered to be valid.
ACKNOWLEDGEMENTS
The authors are deeply indebted to Jean Mariaux, Florian Reyda and Amilcar Arandas Rego for helpful suggestions, to Martin Mortenthaler and his family, Acuario Río Momon, Iquitos, Peru, for providing facilities for fish examination and supplying fish from Santa Clara, Río Nanay. Sophie de Chambrier, Sandrine C. Coquille and Carlos A. Mendoza-Palmero helped with fish examination in 2009 and 2011. Thanks are due to John G. Lundberg, Department of Ichthyology, The Academy of Natural Sciences, Philadelphia, Pennsylvania, USA, for valuable remarks on the identification of some fish hosts, and to Andrea Waeschenbach, Natural History Museum, London, UK, for providing unpublished data on the molecular phylogeny of proteocephalidean cestodes. Support of authorities of the Czech Embassy in Lima, Peru and Peruvian Embassy in Prague, Czech Republic, in particular of Marina Landaveri, Ambassador of Peru in the Czech Republic, is also greatly appreciated. The stays of the present authors in Peru were financially supported by the National Science Foundation, USA (PBI award Nos. 0818696 and 0818823), Czech Science Foundation (project No. P505/12/G112) and the Institute of Parasitology, AS CR, České Budějovice (RVO: 60077344).
