Simulium (Inaequalium) inaequale ( Paterson & Shannon, 1927 )

HERNÁNDEZ, LUIS MIGUEL, SHELLEY, ANTHONY JOHN, DE LUNA DIAS, ANTONIO PAULINO ANDRADE & MAIA-HERZOG, MARILZA, 2007, New specific synonymies and taxonomic notes on Neotropical black flies (Diptera: Simuliidae) belonging to the subgenera Chirostilbia Enderlein, Hemicnetha Enderlein, Inaequalium Coscarón & Wygodzinsky, Psaroniocompsa Enderlein and Psilopelmia Enderlein, Zootaxa 1506 (1), pp. 1-80 : 12-16

Simulium (Inaequalium) inaequale ( Paterson & Shannon, 1927)

( Figs. 15, 16 , 19–26 , 61, 62 , 127–135 , 174–179 , 211 )

Eusimulium inaequale Paterson & Shannon, 1927: 738 . NEOTYPE ♀ (pinned, not associated with pupal exuviae), ARGENTINA: Cerro San Jávier , Tucumán, 1200 m; 7.iv.1960, (Wygodzinsky) (MLP). New type designation.

Simulium baiensis Pinto, 1932: 685 . HOLOTYPE ♂, BRAZIL: Bahía State, Nazaré; 1931, (A. Lutz) (IOC). [Examined.] [Synonymy by Coscarón, 1991: 157.]

Trichodagmia manicata Enderlein, 1934a: 291 . LECTOTYPE ♀, PARAGUAY: Hohenau, 250 m; 15.x.1907, [Without collector’s name.] (SMT). [Examined.] [Synonymized with doubt by Coscarón & Wygodzinsky, 1984: 80; confirmed synonymy in this paper.] [Lectotype designation by Werner, 1996b: 296.]

Thyrsopelma argentata Enderlein, 1936: 125 . HOLOTYPE ♀, PERU: Hoch. [=Alto]; [Without date or collector’s name.] (ZMUH). [Examined.] [Synonymy by Coscarón & Miranda-Esquivel, 1998: 337.]

Simulium clarki Fairchild, 1940: 703 . HOLOTYPE ♀ (reared), PANAMA: Summit, C.Z.; 9.i.1940, [Without collector’s name, but probably collected by Fairchild.] (MCZ, no. 25751). [Examined.] [Probable junior synonym of S. inaequale by Strieder & Py-Daniel, 1999: 63, 2000: 27.] New synonymy.

Simulium jundiaiensis D’Andretta & González B., 1964: 108 . HOLOTYPE ♀ (reared), BRAZIL: São Paulo State: Jundiaí, Bairro Caxambú ; 1.vii.1956, [Collector’s name not stated in the original description.] (MZUSP, no. 855). [Synonymy by Coscarón & Wygodzinsky, 1984: 80.]

Simulium pseudoexiguum Nunes de Mello & Barbosa de Almeida, 1974: 65 . HOLOTYPE ♀ (man-biting), BRAZIL: Roraima State, Boca da Mata, próximo à BR-174; xi.1972, (J.A. Nunes de Mello & Eduardo Vieira da Silva ) (INPA, no. 5041). New synonymy.

Simulium inaequale was described as Eusimulium inaequalis by Paterson & Shannon (1927) based on seven syntype man-biting females collected in Zapla, Jujuy Argentina in 1927. The authors also mentioned in the original description the occurrence of this species in Quebrada de Lules and Tucumán. The depository of the type of S. inaequale is unknown. However, Strieder & Py-Daniel (2000) stated that the type material of S. inaequale is deposited in the USNM, but they did not examine any specimens. Prior to this, the type material of S. inaequale could not be found in the USNM collection (R.W.Crosskey’s notes during his visit to USNM in 1982) nor in any institution in Argentina (Sixto Coscarón, pers. comm.); the latter correspondent considers all South American simuliid species described by Paterson & Shannon (1927) to be lost. Wygodzinsky (1953) redescribed S. inaequale (as S. inaequalis ) from specimens collected from localities in or near Tucumán in Argentina (see p: 309) and it is on this description that the modern concept of the species is based. We have examined several females and males housed in the MLP with identification labels by Wygodzinsky that agree with the description of S. inaequale . Therefore, under the provision of the International Code for Zoological Nomenclature (1999) we have selected a female as neotype and labelled it accordingly. The female is in good condition and is glued on a card point on the left side, together with a male (on a different card point, but on the same pin), and is deposited in the MLP (Material Examined) (Figs. 15,16).

Several names have fallen as junior synonyms of S. inaequale and these are discussed in chronological sequence. Simulium baiense [as baiensis ] was described by Pinto (1932) based on three slide preparations of a male collected in Nazaré, Bahía State, Brazil on 1931 by A. Lutz and deposited in the Pinto collection in the IOC. We have examined these slides that are labelled as S. baiensis . The slides bear the following handwritten labels “ ♂ Simulium baiensis Pinto 1931 Cotipo [confusing because this term, not acceptable under ICZN rules, was used to denote one in a series of specimens with the status of paratype or syntype]. Est. Bahía Nazaré A. Lutz leg.” (see also Material Examined). They contain a male hypopygium ( Figs. 174–176 ), one wing and two hind legs (one is damaged). The wing figured in Pinto (1932) appears to have been stained, which corresponds with the material that we have examined. As Pinto referred to a type (“tipo”) and a single specimen we are confident that this material represents the holotype of S. baiense and it has been labelled accordingly. Coscarón & Wygodzinsky (1984) regarded S. baiense as a species inquirenda in their 1984 review of the subgenus Inaequalium . In a later paper, Coscarón (1991) examined the type of this species and agreed that it belongs to the subgenus Inaequalium . He further explained that though he did not find S. baiense or any other Simulium (Inaequalium) species in Nazaré, he found S. inaequale in a nearby locality (Itabuna in Bahía State) in habitats very similar to that of the type locality. He then suggested “…because of the abundance of S. inaequale in other areas of the state we think that the material studied by Pinto corresponds to this species and regard both species as conspecific…”. We have compared the original description and the type material of S. baiense and accept that the genitalia, especially the gonostyle ( Figs. 175, 176 ), wing setation, and hind leg coloration are similar to most species of the subgenus Inaequalium , but also to many species of the subgenus Psaroniocompsa . However, in the absence of further material or other life stages of S. baiense we agree with Coscarón’s (1991) synonymy.

The synonymy of Trichodagmia manicata Enderlein with S. inaequale was first proposed with doubt by Coscarón & Wygodzinsky (1984). Trichodagmia manicata was described by Enderlein (1934a) based on two pinned females collected in Hohenau, Paraguay, which are deposited in the NMUH and SMT. Werner (1996b) studied the Enderlein material and designated the female from the SMT as lectotype and the other specimen in the ZMUH became a paralectotype (see also Werner, 1996a). We have examined both specimens and taken digital images prior to dissection of the head, wings, legs and genitalia, which are mounted on two slides. The thorax in both specimens remains pinned. The lectotype bears a white, original label in Enderlein’s and Werner’s hand stating its taxonomic status. The specimen at NMUH bears similar labels to the lectotype and a red label of “ Paralectotypus ” in Werner’s hand (Material Examined). The lectotype has been pinned through the posterior margin of the thorax, which has slightly damaged the scutellum. The thorax is completely devoid of hairs ( Figs. 19, 20 ). However, 1+1 sub-median, grey pruinose bands can be seen on this specimen, which falls within the variation found in S. inaequale . The paralectotype is also pinned through the right side of the thorax and the 1+1 grey pruinose bands are less conspicuous than in the lectotype. The morphology of the nudiocular area ( Fig. 83 ), cibarium ( Fig. 101 ) and female genitalia ( Figs. 127–129 ) fall within the variation found in S. inaequale . However, similar variation is also found in other species within the subgenus Inaequalium . Nevertheless, in the absence of further evidence we accept Coscarón & Wygodzinsky’s (1984) synonymy of T. manicata with S. inaequale .

Enderlein (1936) described Thyrsopelma argentata from a single female collected in Peru, Hoch [= Alto Peru]. This species was synonymized with S. inaequale by Coscarón & Miranda-Esquivel (1998), who also provided a brief description of the holotype and advocated the dissection of the head and examination of the morphology of the cibarium. We have examined the pinned female of T. argentata , which is deposited in the NMUH, and attached a holotype label. The specimen is in good condition and has been pinned through the posterior margin of the thorax. It bears original labels in Enderlein’s and Coscarón’s hands (see Material Examined). We have taken digital images of the holotype prior to dissecting the head, wings and legs, which are mounted on a slide. The thorax remains pinned. The genitalia were apparently dissected by Coscarón and are mounted under a small cover slip attached to the pin. The stem of the genital fork is partially broken. The thoracic pattern ( Figs. 21, 22 ) and the morphology of the nudiocular area ( Fig. 85 ), cibarium ( Fig. 102 ), leg coloration, wing setation and genitalia ( Figs. 130–132 ) fall within the morphological variation found in S. inaequale , but also in many other species of Inaequalium . Minor differences in the morphology of the cercus or paraproct? are due to the positioning of this structure in the slide preparation. In the absence of further material we maintain Coscarón & Miranda-Esquivel’s (1998) synonymy.

In 1940 S. clarki was described by Fairchild based on two reared females and four males collected in 1930 in a small stream, at Summit Experimental Gardens, Summit, Canal Zone [now Panamá]. He also examined five reared females and four males bred from pupae collected on water weed in a small stream at Coclé Province, El Valle on xii. 1939. All material was apparently collected by Fairchild himself and deposited in the MCZ. Several authors such as Wygodzinsky (1953) and Coscarón (1991) have suggested that S. clarki might be a synonym of S. inaequale , but refrained to synonymize them because of minor differences in the leg coloration and length of the paraproct and gonostyle. In addition, Coscarón & Coscarón-Arias (1997) regarded S. clarki and S. lurybayae Vargas as being closely related to S. inaequale . More recently, Strieder & Py-Daniel (1999) did not include S. clarki [as Inaequalium clarki ] in their taxonomic treatment or keys to immature stages of Inaequalium [as genus] “…because of its uncertain taxonomic status and/or lack of data…”. However, they stated without further explanation (p. 63) that “… I. clarki should be considered as a probable junior synonym of I. inaequale (with a wide distribution in Central America)…”. In a later paper, Strieder & Py-Daniel (2000) listed S. clarki as a valid species in the genus Inaequalium , but at this juncture suggested that “…further investigations were needed to obtain a better understanding of the characteristics of the larva in Central America before any synonymy between I. clarki with I. Inaequale could be established…”. Furthermore, this species was not included in the phylogenetic analysis of Strieder & Py-Daniel (2002) because of its uncertain taxonomic situation and/or the lack of sufficient data. In Coscarón & Coscarón-Arias (2007) S. clarki was maintained as a valid species. We have examined the pinned female holotype of S. clarki as well as eight pinned females, five pinned males, and one male and one female on a slide (all labelled as paratypes) housed in MCZ, and studied the pupal gill configuration given in Fairchild (1940). We have also compared this material with numerous link-reared specimens of S. inaequale deposited in the BMNH and IOC collections (see Material Examined). The morphological characters of the female and male thoracic patterns ( Figs. 23, 24 , 61, 62 ), female nudiocular area ( Fig. 85 ), female cibarium ( Fig. 103 ) and female ( Figs. 133–135 ) and male genitalia ( Figs. 177–179 ) of the type specimens of S. clarki , as well as the configuration and number of pupal gill filaments of specimens identified as this species by A.J.Shelley ( Fig. 217 ) fall within the variation found in S. inaequale . Therefore, we regard both species as conspecific, with the former becoming the junior synonym.

Simulium jundiaiense [as jundiaiensis ] was described by D’Andretta & González B. (1964) from a reared female collected in Jundiaí (Bairro Caxambú), São Paulo State by D’Andretta. It was synonymized with S. inaequale by Coscarón & Wygodzinsky (1984). The holotype of S. jundiaiense was deposited in the MZUSP, but we were unable to find this specimen within the Museum holdings. The illustrations and morphological description of S. jundiaiense fall within the variation of S. inaequale and we agree with Coscarón & Wygodzinsky (1984) that S. jundiaiense is a junior synonym of S. inaequale .

Another species that we are treating as a synonym of S. inaequale is S. pseudoexiguum Nunes de Mello & Barbosa de Almeida. This species was described by Nunes de Mello and Barbosa de Almeida (1974) from 28 man-biting females collected near the Venezuela border in Roraima State, Brazil. The holotype is said to be deposited in the INPA collection with no. 5041. Coscarón & Wygodzinsky (1984) stated that S. pseudoexiguum might be a synonym of S. beaupertuyi , but they did not make any taxonomic decisions due to the lack of reared material of both species. Simulium pseudoexiguum has also been regarded as a species inquirenda by several authors such as Coscarón (1987, 1991), Coscarón & Coscarón-Arias (2007), and Strieder & Py-Daniel (2000). We have studied the original description and the general morphology of the thoracic pattern ( Figs. 25, 26 ) of the paratypes of S. pseudoexiguum and compared them with the morphology of numerous link-reared and man-biting specimens identified either as S. pseudoexiguum or S. clarki from Guyana and Roraima State, Brazil deposited at the BMNH (for adult general morphology and gill filament configuration of this material see Shelley et al., 2004). Although, we were unable to obtain the holotype for study we examined six pinned females and six slides containing body parts of these pinned specimens all labelled as paratypes and deposited in INPA (Material Examined). An additional paratype has been recently found in the IOC collection. The specimen bears the following labels providing data that agree with those given in the original description: Rio Surumu, Próx. acamp; 2.xi.1972; PARATIPO/ S. pseudoexiguum , nos. 1004, 5944-7. A label with the IOC number “LSO-389” has been added to this paratype. We agree that S. pseudoexiguum falls within the morphological variation found in S. inaequale and consider S. pseudoexiguum as a junior synonym of S. inaequale . We have only found morphological differences on the leg coloration between populations of this species and S. inaequale , which we consider to be intraspecific variations. In specimens identified as S. clarki all legs are darker brown, while they are more yellowish in S. pseudoexiguum .

In his catalogue of South and Central American Simuliidae Pinto (1932) referred to Lutz’ work on S. subnigrum and presented a description and figure of the pupa that is actually S. inaequale . This material was provided by Prof. Lutz and Prof. Travassos and collected at Anhembí, São Paulo and Angra dos Reis, Rio de Janeiro [respectively removed]. Strieder & Py-Daniel (2000) later referred to this misidentification.

The thoracic pattern of females S. inaequale varies from indistinct (neotype Figs. 15, 16 ; specimen from São Paulo State, Brazil- see Figs. 17, 18 ) to more distinct in well-preserved specimens as in Shelley et al., 2004 [as S. clarki ]. Simulium inaequale is only reliably identified from other species of the subgenus Inaequalium by its six filamented pupal gill, in which all primary branches bifurcate near the base ( Fig. 211 ). Other simuliid species with a similar gill configuration are S. metallicum Bellardi (species complex) and S. cerradense Coscarón, Cerqueira, Schumaker & Salvia Filho , but they can easily be separated by the different morphology of the cibarium and structure of the male and female genitalia.

Simulium inaequale was included in the genus Simulium by Edwards (1931) as he regarded Eusimulium Roubaud as a subgenus of Simulium Latreille. Full descriptions of adults and immature stages of S. inaequale are found in Coscarón (1991), Coscarón & Wygodzinsky (1984), Strieder & Py-Daniel (1999; 2000) and Wygodzinsky (1953). Vargas & Díaz Nájera (1948) also provided a morphological description of the male genitalia of S. inaequale [as S. clarki ] based on specimens collected in Carrizales, Venezuela, which were previously identified by Briceño Iragorry (1946) as S. pertinax Kollar (see also D’Andretta & D’Andretta, 1950). Coscarón (1987), Coscarón & Coscarón-Arias (1997) and Strieder & Py-Daniel (2002), in their phylogenetic analysis of Inaequalium placed S. inaequale in the inaequale -species group related to S. leopoldense , S. nahimi and S. subnigrum .

Based on the synonymies here proposed, S. inaequale has now a widespread distribution in the Neotropical region. It has been recorded in Argentina (Jujuy, Missiones, Salta and Tucumán Provinces), Brazil (Amapá, Bahía, Espírito Santo, Minas Gerais, Mato Grosso, Paraná, Paraíba, Rio Grande do Sul, Rio de Janeiro, Roraima, São Paulo and Santa Catarina States), Bolivia, Costa Rica, Ecuador, Guyana, Panamá, Paraguay, Peru and Venezuela ( Coscarón et al., 1992; Crosskey & Howard, 1997, 2004; Gil-Azevedo & Maia-Herzog, 2004; Material Examined). The immature stages are found in small streams in Brazil and in 50 m wide rivers in Guyana ( Shelley et al., 2004). Coscarón & Wygodzinsky (1984) and Coscarón (1991) collected pupae in small, clear water streams in Argentina. The females are highly anthropophilic along its distribution range biting man voraciously in countries like Guyana [as S. clarki ] ( Shelley et al., 2004) and in the River Uiramutão in Roraima State, Brazil together with S. nigrimanum Macquart , S. oyapockense Floch and Abonnenc (s.l.) and S. spinibranchium (A.J. Shelley & A.P.A. Luna Dias, unpublished data). Coscarón (1991) recorded this species biting mules in Bolivia, and Eaton et al. (1998) recorded its presence in the focus of pemphigus foliaceus in Mato Grosso do Sul, Brazil. Pepinelli & Trivinho-Strixino (2002) suggested that the females showed a tendency to lay eggs on dark substrates.

Figures

PLATE 1. FIGURES 1–16. Colour patterns of the female thorax. For each species first figure is with anterior illumination and second figure with posterior illumination. 1, 2: Thyrsopelma striginotum holotype; 3, 4: S. pillosum holotype; 5, 6: S. pillosum paratype; 7, 8: S. dekeyseri holotype; 9, 10: S. guarani holotype; 11, 12: S. acarayense holotype; 13, 14: S. mutucuna holotype; 15, 16: S. inaequale neotype.

PLATE 2. FIGURES 17–32. Colour patterns of the female thorax. For each species first figure is with anterior illumination and second figure with posterior illumination. 17, 18: S. inaequale (indistinct bands); 19, 20: Trichodamia manicata lectotype. 21, 22: Thyrsopelma argentata holotype; 23, 24: S. clarki holotype; 25–26: S. pseudoexiguum paratype; 27, 28: S. mbarigui holotype; 29, 30: S. nahimi holotype; 31, 32: S. subnigrum (Brazil).

PLATE 5. FIGURES 59–78. Colour patterns of the male thorax. For each species first figure is with anterior illumination and second figure with posterior illumination. 59, 60: S. acarayense paratype; 61, 62: S. clarki paratype; 63, 64: S. nahimi paratype (as allotype); 65, 66: S. subnigrum (Brazil); 67, 68: S. jujuyense (Argentina); 69, 70: S. auripellitum (Brazil, with silver cunae]; 71, 72: Psaroniocompsa mendozoana holotype; 73, 74: S. bonaerense paratype; 75, 76: S. minuanum paratype; 77, 78: S. sicuani paralectotype.

PLATE 6. FIGURES 79–96. Female nudiocular area. 79: Thyrsopelma striginotum holotype; 80: S. pillosum holotype; 81: S. dekeyseri paratype; 82: S. acarayense paratype; 83: Trichodagmia manicata lectotype; 84: Thyrsopelma argentata holotype; 85: S. clarki paratype; 86: S. subnigrum (Brazil); 87: Psaroniocompsa opalinifrons holotype; 88: S. jujuyense (Argentina); 89: S. auripellitum holotype; 90: Pliodasina guttata holotype; 91: S. bonaerense paratype; 92: S. minuanum paratype; 93: S. costaricensis holotye; 94: S. spinifer holotype; 95: S. hoffmani lectotype; 96: S. sicuani lectotype.

PLATE 7. FIGURES 97–114. Female cibarium. 97: Thyrsopelma striginotum holotype; 98: S. pillosum holotype; 99: S. dekeyseri paratype; 100: S. acarayense paratype; 101: Trichodagmia manicata lectotype; 102: Thyrsopelma argentata holotype; 103: S. clarki paratype; 104: S. subnigrum (Brazil); 105: Psaroniocompsa opalinifrons holotype; 106: S. jujuyense (Argentina); 107: S. auripellitum holotype; 108: Pliodasina guttata holotype; 109: S. bonaerense paratype; 110: S. minuanum paratype; 111: S. costaricensis holotye; 112: S. spinifer holotype; 113: S. hoffmani lectotype; 114: S. sicuani lectotype.

PLATE 9. FIGURES 127–141. Female genitalia (cercus and pararprocts, eighth sternite and gonopophyses). 127–129: Trichodagmia manicata lectotype. 130–132: Thyrsopelma argentata holotype; 133–135: S. clarki paratype; 136–138: S. subnigrum (Brazil). 139–141: S. subnigrum (specimens previously identified as S. nahimi by L.M.Hernández).Arrow indicates a sclerotized artefact on the left lateral arm of the genital fork that resembles an anterior process.

PLATE 12. FIGURES 171–182. Male genitalia (ventral plate, gonocoxite and gonostyle, paramere). 171–173: S. acarayense paratype; 174–176: S. baiense holotype; 174: hypopygium in situ; 175: Gonocoxite and gonostyle left side; 176: Gonocoxite and gonostyle right side; 177–179: S. clarki paratype; 180–182: Specimen previously identified as S. nahimi by L.M.Hernández; 181: Topotype male deposited in INPA.

PLATE 14. FIGURES 202–216. Pupal gill filaments and frontoclypeus. 202: S. guerreroi (Venezuela); 203: S. guarani holotype; S. acarayense paratype; 205–207: S. oviedoi (Venezuela); 208–210: S. rivasi (Venezuela); 211: Specimen identified as S. clarki by A.J.Shelley (Brazil); 212: S. clavibranchium syntype; 213: S. clavibranchium variation (Brazil); 214: S. mbarigui holotype; 215: Topotype identified as S. nahimi by V.P.Py-Daneil at INPA; 216: S. subnigrum (Brazil). Arrows indicate a variation on the gill filaments apically.

PLATE 15. FIGURES 217–220. Pupal gill filaments. 217: S. jujuyense (Argentina); 218: S. bonaerense paratype; 219: S. bonaerense (gill variation, Argentina); 220: S. minuanum paratype. Arrow indicate the more apical bifurcation of the dorsal primary branch.