UNIVERSIDADE DE SÃO PAULO FFCLRP ‐ DEPARTAMENTO DE BIOLOGIA PROGRAMA DE PÓS‐GRADUAÇÃO EM ENTOMOLOGIA Revisão taxonômica de Thraulodes Ulmer 1919 (Ephemeroptera: Leptophlebiidae: Atalophlebiinae) Rodolfo Mariano Lopes da Silva Tese apresentada à Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto da USP, como parte das exigências para a obtenção do título de Doutor em Ciências, Área: Entomologia RIBEIRÃO PRETO ‐ SP 2009
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UNIVERSIDADE DE SÃO PAULO
FFCLRP ‐ DEPARTAMENTO DE BIOLOGIA
PROGRAMA DE PÓS‐GRADUAÇÃO EM ENTOMOLOGIA
Revisão taxonômica de Thraulodes Ulmer 1919
(Ephemeroptera: Leptophlebiidae: Atalophlebiinae)
Rodolfo Mariano Lopes da Silva
Tese apresentada à Faculdade de Filosofia, Ciências e
2.2. Situação atual do estudo dos Ephemeroptera no Brasil ............................................................................. 6 2.3. Histórico da Ordem ..................................................................................................................................... 8 2.4. Leptophlebiidae ......................................................................................................................................... 11 2.5. Thraulodes Ulmer 1919 ............................................................................................................................. 13 3. Objetivos ............................................................................................................................................ 19 4. Materiais e métodos ........................................................................................................................... 20 4.1.Coletas de ninfas ........................................................................................................................................ 20 4.2. Coleta de Adultos ...................................................................................................................................... 20 4.3. Identificação e depósito do material ......................................................................................................... 20 4.4. Lista onde os espécimes estão depositados .............................................................................................. 21 4.5. Metodologia cladística .............................................................................................................................. 22 5. Resultados .......................................................................................................................................... 24 5.1. Checklist de Leptophlebiidae para o Estado de São Paulo ........................................................................ 24 5.2. Chave preliminar para os gêneros de Leptophlebiidae que ocorrem no Brasil ........................................ 26 5.3.Taxonomia................................................................................................................................................... 32
5.3.1. Espécies de Thraulodes não incluidas na análise ............................................................................ 32 5.3.2. Espécies ........................................................................................................................................... 33 5.3.3. Sinonimias ....................................................................................................................................... 52 5.3.4. Descrições de novas espécies .......................................................................................................... 52
5.4. Análise Cladística ....................................................................................................................................... 60 5.4.1. Matriz e Lista de caracteres ............................................................................................................ 60
5.5. Cladogramas .............................................................................................................................................. 65 5.5.1. Pesagem igual dos caracteres ......................................................................................................... 65 5.5.2. Pesagem implícita dos caracteres ................................................................................................... 79
6. Hipóteses de parentesco ..................................................................................................................... 85 7. Considerações finais ........................................................................................................................... 88 8. Referências Bibliográficas ................................................................................................................... 89 9. Anexos ................................................................................................................................................ 98
1
1. Resumo
O gênero Thraulodes Ulmer 1920 apresenta 52 espécies neotropicais, sendo que destas
apenas 20 espécies possuem a ninfa descrita. Esta é uma problemática encontrada em
vários grupos, o que levado à escolha de apenas os machos adultos serem analisados.
No Brasil ocorrem sete espécies: T. daidaleus Thew 1960 (Santa Catarina), T. itatiajanus
Traver & Edmunds 1967 (Rio de Janeiro), T. limbatus Navás 1936 (Santa Catarina), T.
subfasciatus Navás 1924 (Rio de Janeiro), T. traverae Thew 1960 (Santa Catarina), T.
ulmeri Edmunds 1950 (Santa Catarina) and T. schlingeri Traver & Edmunds 1967 (São
Paulo). O presente estudo gerou a revisão taxonômica do gênero, uma chave de
identificação dos gêneros de Leptophlebiidae que ocorrem no Brasil e uma check list
atualizada para a família. Foi possível observar um aumento significativo no número de
espécies para o Estado, 18, quando anteriormente apenas 5 espécies de
Leptophlebiidae eram conhecidas. Dentro do trabalho de revisão foram descritas 4
novas espécies, três em material colecionado no Brasil e uma colecionada na Costa
Rica, e foi proposta uma topologia para as espécies de Thraulodes.
2
Abstract
There are 52 known species of Neotropical Thraulodes Ulmer (1920), but only 20 of
these species have the nymph described. This is a problem found in many groups,
leading to only adult males being selected for analysis. Seven species occur in Brazil: T.
daidaleus Thew 1960 (Santa Catarina), T. itatiajanus Traver & Edmunds 1967 (Rio de
Janeiro), T. limbatus Navás 1936 (Santa Catarina), T. subfasciatus Navás 1924 (Rio de
Janeiro), T. traverae Thew 1960 (Santa Catarina), T. edmundsi Ulmer 1950 (Santa
Catarina) and T. schlingeri Traver & Edmunds 1967 (São Paulo). The aim of this study is
the revision of the genus Thraulodes, the presentation of a key for genera of
Leptophlebiidae from Brazil and of an updated check list for the family. By the latter,
it´s possible to observe a significant increase in the number of species for the State of
São Paulo, 18 species, in contrast to the previously only 5 species known of
Leptophlebiidae. Here we describe 4 new species, three from Brazil and one from
Costa Rica, and a topology of the species of Thraulodes is proposed.
3
2. Introdução
Os Ephemeroptera constituem um dos mais importantes grupos da
entomofauna aquática, ao lado de Plecoptera e Trichoptera (EPT), além dos
Chironomidae (Diptera). Ocorrem em ambientes aquáticos lênticos e lóticos, sendo a
maior diversidade encontrada em rios de cabeceira, de segunda e terceira ordens, com
fundo rochoso e água oligotrófica a mesotrófica (Edmunds et al. 1976; Merritt &
Cummins 1996; Roldán‐Pérez 1988). Os Ephemeroptera são encontrados em todos os
continentes, exceto na Antártida, no extremo Ártico e em algumas ilhas oceânicas
(Edmunds et al. 1976).
A maior parte das ninfas de Ephemeroptera se alimenta basicamente de
material vegetal (algas unicelulares e coloniais do biofilme), além de detritos, incluindo
material vegetal alóctone (Edmunds et al. 1976; Needham et al. 1935; Williams &
Feltmate 1992). Também fazem parte da dieta, fungos, bactérias e restos animais. As
espécies verdadeiramente carnívoras são raras (Brittain 1982; Campbell 1985;
McCafferty & Provonsha 1986). Muitas espécies não se alimentam no primeiro estágio
ninfal, sobrevivendo a partir das células intestinais vitelínicas (Brittain 1982) e,
freqüentemente, o hábito alimentar varia durante o desenvolvimento da ninfa (Merritt
& Cummins 1996).
Vários fatores influenciam o ciclo de vida e a distribuição temporal e espacial
dos estágios imaturos e adultos de EPT. A influência de fatores bióticos e abióticos
sobre os organismos aquáticos sejam eles físicos ou químicos, tem sido bastante
estudada nas últimas décadas (cf. Anderson & Cummins 1979; Cummins et al. 1984;
Petersen & Eeckhaute 1992).
4
2.1. Morfologia
2.1.1. Ninfas
Figura 1. Esquema geral de ninfa (modificado de Traver e Edmunds, 1967)
5
2.1.2. Imagos
Figura 2. Esquema geral da imago.
Figura 3. Esquema geral das asas da imago.
6
Figura 4. Esquema geral da genitália com pênis em destaque (Imago).
2.2. Situação atual do estudo dos Ephemeroptera no Brasil
A ordem Ephemeroptera está composta atualmente por cerca de 4000 espécies
em 37 famílias. Na América do Sul são conhecidas 14 famílias e aproximadamente 450
espécies de Ephemeroptera (Domínguez et al. 2006). Para o Brasil há um total de 63
gêneros e 166 espécies representando 10 famílias: Leptophlebiidae, Baetidae,
A análise da matriz de dados utilizando pesagem igual dos caracteres resultou
em 10 topologias igualmente parcimoniosas (Figuras 76‐86) com comprimento de 138
passos, CI = 0.23, RI = 0.69 e RC = 0.16.
O consenso estrito resultante dessas 10 topologias (Figura 86) mostra a
estabilidade de alguns clados – (T. sp2, T. schlingeri) (T. telegraphicus, T. papilionis) (T.
speciosus, T. lunatus) (T. quevedoensis, T. mucuy) (T. hilaroides, T. consortis) (T. flint, T.
brunneus) (T. basimaculatus (T. sp4 (T. ephippiatus, T. conchunaensis))) (T. centralis (T.
paysandensis, (T. lepidus, T. cryptodrilus) (T. sp1 (T. marreroi (T. osíris, T. bolivianus)))))
– sendo que as demais espécies (T. zonalis, T. venezuelana, T. valens, T. ulmeri, T.
trijuncta, T. traverae, T. spangleri, T. regulus, T. prolongnatus, T. packeri, T. mexicanus,
T. liminaris, T. laetus, T. itatiajanus, T. hilaris, T. guanare, T. gonzalesi, T. furficulus, T.
daidaleus, T. bomplandi, T. sp3) são apresentadas em uma politomia. A monofilia do
gênero Thraulodes foi corroborada na análise com pesagem igual dos caracteres.
66
Figura 76. Topologia 1 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
67
Figura 77. Topologia 2 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
68
Figura 78. Topologia 3 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
69
Figura 79. Topologia 4 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
70
Figura 80. Topologia 5 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
71
Figura 81. Topologia 6 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
72
Figura 82. Topologia 7 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
73
Figura 83. Topologia 8 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
74
Figura 84. Topologia 9 resultante da análise com pesagem igual dos caracteres (a barra
indica o gênero Thraulodes).
75
Figura 85. Topologia 10 resultante da análise com pesagem igual dos caracteres (a
barra indica o gênero Thraulodes).
76
Figura 86. Consenso estrito das 10 topologias resultantes da análise com pesagem
igual dos caracteres (a barra indica o gênero Thraulodes).
77
5.5.1.2. “New Technology”
A análise com “New Technology” do TNT resultou em duas topologias
igualmente parcimoniosas, com 138 passos cada, com CI = 0.23, RI = 0.69 e RC = 0.16.
As duas árvores apresentaram a mesma relação entre as espécies com diferença nas
sinapomorfias do nó 02 (figuras 87), bolsa lateral e comprimento do pênis.
Dentro do gênero o clado ((T. telegraphicus, T. papilionis) (T.itatiajanus (T.
basimaculatus (T. sp4 (T. ephippiatus, T. conchunaensis))))) é apresentado como grupo
irmão dos demais congêneres. Outro grupo monofilético resultante (T. packeri (T.
trijuncta (T. bomplandi (T. furficulus (T. zonalis (T. liminaris (T. hilaris (T. venezuelana (T.
hilaroides, T. consortis))))))))) foi apresentado como grupo irmão de (T. traverae (T.
prolongnatus ((T. laetus, T. daidaleus) (T. mexicanus (T. centralis ((T. lepidus, T.
cryptodrilus) (T. paysandensis (T. sp1 (T. marreroi (T. osíris, T. bolivianus)))))))))). Estes
dois clados formam um grupo monofilético sendo grupo irmão as demais spécies de
Thaulodes.
78
Figura 87. Topologia resultante da análise com pesagem igual dos caracteres com New
Technology Search, mostrando a diferença.
79
5.5.2. Pesagem implícita dos caracteres
As análises utilizando pesagem implícita dos caracteres foram feitas com uso do
software TNT. As análises com valores de k nos valores 300, 350 e 800 (figuras 88‐91)
resultaram em topologias com menor número de passos, 138. Alguns pequenos clados
se mantiveram nas topologias supracitadas (Figura 91), enquanto que as demais
espécies oscilam nos cladogramas: (T. centralis ((T. paysandensis (T. lepidus, T.
cryptodrilus)) (T. sp1 (T. marreroi (T. osisris, T. bolivianus))))) (figura 91A); (T.
itatiajanus (T. basimaculatus (T. ephippiatus (T.sp4, T. conchuanensis)))) (figura 91B);
(T.sp3 (T. sp2, T. schilingeri)) (figura 91C); (T. trijuncta ((T. furficulus, T. bomplandi) (T.
zonalis (T. liminaris (T. hilaris, T. venezuelana (T. hilaroides, T. consortis)))))) (figura
91D).
80
Figura 88. topologia obtida a por Implied Weighting, K=300.
81
Figura 89. topologia obtida a por Implied Weighting, K=350.
82
Figura 90. topologia obtida a por Implied Weighting, K=800.
83
Figura 91. Clados formados em pesagem implícita de três topologias.
84
Tabela 2. Número de passos das topologias resultantes das análises com pesagem implícita utilizando os diferentes valores de k. (entre parênteses quando número de topologias é maior que 1)
Valores de k No de passos Valores de k No de passos
1 155 (2) 35 139
2 155 40 139
3 154 45 139
4 149 50 139
5 147 (2) 60 139
6 147 70 139
7 146 80 139
8 144 90 139
9 143 (2) 100 139
10 143 150 139
11 142 200 139
12 142 250 139 (2)
13 144 300 138
14 140 350 138
15 140 400 139
16 139 450 140 (2)
17 140 500 139
18 139 600 139
19 140 700 139 (2)
20 140 800 138
25 139 900 140
30 140 1000 140
85
6. Hipóteses de parentesco
Como demonstrado anteriormente, as diferentes metodologias de pesagem
das análises resultaram em várias árvores filogenéticas diferentes com 138 passos,
porém houve congruência em relação a alguns clados da filogenia das espécies de
Thraulodes. As análises com pesagem igual dos caracteres resultaram em 10 e 2
topologias igualmente parcimoniosas com buscas tradicional e nova tecnologia do TNT,
respectivamente; enquanto que o conjunto de análises utilizando pesagem implícita
resultou em 3 topologias, com 138 passos, com os valores de k 300, 350 e 800.
A monofilia do gênero foi corroborada em todas as análises, pesagem igual e
implícita, sendo os caracteres que sustentam a monofilia de Thraulodes os seguintes:
1. Forquilha da veia MP ausente (caráter 2)
2. Manchas no fêmur anterior presentes (caráter 10)
3. Padrão geral de coloração abdominal translúcida nos primeiros segmentos
(Caráter 13)
4. Soquetes dos fórceps fusionados (caráter 19)
5. Base do pênis abruptamente inchado (caráter 25)
Partindo para a análise das hipóteses de relações entre as espécies de
Thraulodes, na pesagem igual de caracteres há uma grande incerteza, como podemos
observar no consenso das topologias, pela politomia da maioria das espécies, com
exceção da resolução de alguns clados (Figura 86). As relações entre as espécies de
Thraulodes ainda não estão totalmente resolvidas, porém alguns clados foram
observados nas análises. Sendo assim não houve uma topologia escolhida, mas sim
estes clados monofiléticos encontrados em pesagem implícita (Figura 91).
O maior grupo encontrado foi: (T. trijuncta (T. furficulus, T. bomplandi (T.
zonalis (T. liminaris (T. hilaris, T. venezuelana, (T. hilaroides, T. consortis))))))
sustentado pelo do carater 23 (0), pênis totalmente dividido. A espécie T. trijuncta
aparece como grupo irmão das demais espécies, que são por sua vez são sustentadas
pelo caráter 4 (1) área C e Sc pigmentada; o clado formado pelas espécies T. furficulus
e T. bomplandi formam um politomia com o grupo (T. zonalis (T. liminaris (T. hilaris, T.
86
venezuelana, (T. hilaroides, T. consortis)))). O táxon T.zonalis, grupo irmão das demais
espécies deste clado é sustentado pelo presença de bolsa lateral. O clado que T.
liminaris forma grupo irmão com (T.hilaris, T. venezuelana, (T. hilaroides, T. consortis))
que são sustentados pelo caráter 23 (1) pênis parcialmente divididos. E o grupo (T.
hilaroides, T. consortis) é sustentado pelos caracteres: padrão da geral coloração
abdominal não translúcida e espinho do pênis robusto.
Outro clado monofilético é formado por 8 espécies: (T. centralis ((T.
paysandensis (T. lepidus, T. cryptodrilus)) (T. sp1 (T. marreroi (T. osisris, T.
bolivianus))))) sustentado pelo carater 20 (0) ausência de bolsa lateral, tendo T.
centralis como grupo mais externo. O clado (T. lepidus, T. cryptodrilus) é sustentado
pelo caráter 3 (0) veias transversais presentes e pelo caráter 4 (1) área C e Sc
pigmentada, como citado anteriormente T. cryptodrilus será sinonimizado com T.
lepidus. Este clado forma um grupo monofilético com T. paysandendsis, sendo grupo
irmão de (T. sp1 (T. marreroi (T. osisris, T. bolivianus))) que é por sua vez sustentado
pelo caráter 11 (1), duas manchas no fêmur anterior. Enquanto que o clado T. marreroi
(T. osisris, T. bolivianus) é sustentado pelo espinho do pênis longo.
Outros dois clados são T. itatiajanus (T. basimaculatus (T. ephippiatus (T.sp4,
T. conchunaensis)))); sendo este clado sustentado pelos carateres 22 (1) e 4 (1) (figura
91B). As espécies T. sp4 e T. conchuanensis formam um clado sustentado pela área C e
SC da asa anterior sem pigmentação e pela forma curva dos espinhos do pênis.
Enquanto que o outro clado formado por T.sp3, (T. sp2, T. schilingeri)) é sustentado
pelo caráter 3 (1), veias transversais ausentes até a bula na asa anterior (figura 91C).
Apesar dos progressos realizados por essas análises filogenéticas, nota‐se que
existem alguns problemas na matriz de dados em si. Os altos índices de homoplasia e
os baixos índices de consistência de todas as análises feitas são indicativos dos
problemas existentes, alguns deles podendo ser de codificação. Um dos motivos do
alto índice de homoplasias pode ser explicado pelo conjunto de caracteres de genitália
que diferem nas 46 espécies. As diferentes combinações destes fazem com que surjam
diversas vezes dentro das filogenias aumentando este índice. Porém a falta de
caracteres de ninfas na matriz de dados também pode ter uma influência direta na
resolução de alguns clados, sendo este um problema não só encontrado em
87
Thraulodes, mas em um grande número de gêneros de Leptophlebiidae devido à falta
de descrição dos imaturos. Mesmo que plotados os caracteres de ninfas na matriz o
número de “missing data” seria muito grande. Provavelmente as espécies iriam ser
divididas em dois clados, um das espécies com ninfas descritas e outro de espécies sem
as ninfas descritas.
Apesar de não ter sido escolhida nehuma topologia como resultado entre
todas as relações das espécies de Thraulodes, os clados anteriormente citados
esclarecem algumas relações. Apesar disso há muito que ser feito, sendo o principal a
descrição dos outros estágios das espécies. Porém isto em alguns casos é inviável
dependendo muito da dificuldade de acesso aos pontos de coleta.
88
7. Considerações finais
No presente trabalho são descritas e ilustradas cinco novas espécies. Em todas
as análises essas espécies apresentam proximidade filogenética com os demais
gêneros de Thraulodes, o que demonstra que elas devem ser inclusas no gênero;
Uma das espécies, Thraulodes cryptodrilus, foi sinonimizada com Thraulodes
lepidus após análise dos holótipos e como demonstrado em todas as análises feitas;
A monofilia do gênero foi corroborada em todas as análises;
O trabalho ressalta ainda que os imaturos da maioria das espécies ainda
continuam desconhecidos, exigindo um esforço especial para sua descrição;
Em paralelo a esta tese alguns trabalhos foram publicados (anexos).
89
8. Referências Bibliográficas
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North and Central America. Canadian Entomologist 110:413‐433.
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Editora e Sociedade Brasileira de Entomologia, Ribeirão Preto. 276 p.
ANDERSON, N.H. & CUMMINS, K.W. 1979. Influence of diet on the life histories of
aquatic insects. Journal of the Fisheries Research Board of Canada. 36: 335‐342
BANKS, N. 1918. New neuropteroid insects. Bulletin of the Museum of Comparative
Zoology 62(1):1‐22, pl. 1‐2
BISPO, P. C. ; OLIVEIRA, L. G. ; BINI, L. M. ; SOUSA, K. G. 2006. Ephemeroptera,
Plecoptera and Trichoptera assemblages from riffles in mountain streams of
Central Brazil: environmental factors influencing the distribution and
abundance. Revista Brasileira de Biologia, v. 66, n. 2B, p. 611‐622.
BISPO, P. C. ; OLIVEIRA, L. G. 2007. Diversity and structure of Ephemeroptera,
Plecoptera and Trichoptera assemblages from riffles in mountain streams of
Central Brazil. Revista Brasileira de Zoologia, v. 24(2), p. 283‐293.
BLANCHARD 1851. In Gay, Historia Fisica y Politica de Chile VI: 107, Atl. Nevropt. ii: 3.
BRITTAIN, J.E. 1982. Biology of Mayflies. Annual Review of Entomology. 27: 119‐147
CAMPBELL, I.C. 1985. Dietary habits of Australian siphlonurid and oligoneuriid
ephemeropteran nymphs. Ecology of aquatic organisms 22: 3250‐3259.
CHACÓN M.M.; SEGNINI S. & DOMÍNGUEZ. E. 1999. Three new species of Thraulodes
(Ephemeroptera: Leptophlebiidae: Atalophlebiinae) from Venezuela. Aquatic
Insects 21(4): 249–257.
CRISCI‐BISPO, V. L. ; BISPO, P. C. ; FROEHLICH, C. G. 2007a. Ephemeroptera, Plecoptera
ando Trichoptera assemblages in two Atlantic rainforest streams, Southeastern
Brazil. Revista Brasileira de Zoologia, v. 24 (2), p. 312‐318.
CRISCI‐BISPO, V. L. ; BISPO, P. C. ; FROEHLICH, C. G. 2007b. Ephemeroptera, Plecoptera
and Trichoptera assemblages in litter in a mountain stream of the Atlantic
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Rainforest , Southeastern Brazil. Revista Brasileira de Zoologia, v. 24(3), p. 545‐
Domínguez, E., Molineri, C., Pescador, M.L., Hubbard, M.D. & Nieto, C. (2006)
Ephemeroptera of South America. In: Adis, J., Arias, J.R., Rueda‐Delgado, G. &
K.M. Wantzen (Eds.), Aquatic Biodiversity in Latin America (ABLA). Vol. 2.
Pensoft, Sofia‐Moscow, 646 pp.
Kluge N.J. (2007) A new taxon Hermanellonota, or subtribe Hermanellini subtr.n.
(Ephemeroptera: Leptophlebiidae: Hagenulini), with description of three new
species from Peruvian Amazonia. Russian Entomological Journal, 16(4), 385‐
400.
Traver J.R. (1947) Notes on Neotropical mayflies. Part II. Family Baetidae, subfamily
Leptophlebiinae, Revista de Entomologia, 18, 149‐160.
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9.2. Anexo 2
Aquatic Insects (no prelo) Description of the imago of Traverella longifrons Lugo‐Ortiz & McCafferty, 1996
(Ephemeroptera: Leptophlebiidae)
Rodolfo Marianoa*, Janice Petersb & R. Wills Flowersb a ‐ Universidade de São Paulo, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto. Departamento
de Biologia, Laboratório de Entomologia Aquática. Av. dos Bandeirantes, 3900, Monte Alegre. CEP‐
14040‐901. Ribeirão Preto, SP, Brazil. b‐ Entomology, CESTA, Florida A&M University, Tallahassee, FL 32307, USA
Revision of the South American species of Hagenulopsis Ulmer and Askola Peters (Ephemeroptera: Leptophlebiidae) with description of six new species
EDUARDO DOMÍNGUEZ1, CARLOS MOLINERI1 & RODOLFO MARIANO2
1CONICET-Facultad de Ciencias Naturales e IML, Universidad Nacional de Tucumán, Argentina2Universidade de São Paulo, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Departamento de Biologia, Laboratório de Entomologia Aquática, Ribeirão Preto, Brasil
Abstract
The South American species of the genera Askola and Hagenulopsis are revised. Three new species of Askola from Brazil are described based on male imagos. Askola emmerichi sp. nov. and A. paprockii sp. nov. present spotted wings, but differ in general coloration and details of genitalia; Askola cipoensis sp. nov. is easily distinguished because the male eyes being widely separated on meson of head. Three new species of Hagenulopsis are also described: H. lipeo (from Argentina and Bolivia) and H. zunigae (from Colombia), both described from imagos and nymphs, can be recognized by details of coloration and male genitalia. H. esmeralda sp. nov. from Ecuador, described from imagos, shows a distinct male genitalia and translucent male abdomen. A key to species for the the male and female imagos of Askola and Hagenulopsis species is provided.
Key words: Atalophlebiinae, Neotropics, taxonomy, new species, mayflies
Introduction
Askola Peters and Hagenulopsis Ulmer are two of the four dipterous (with no hind wings) leptophlebiids known to South America. The monotypic Bessierus Thomas & Orth and Perissophlebioides Savage, are the two other dipterous genera, but are not closely related to the sister taxa Askola and Hagenulopsis (Domínguez, 2009).
The genus Askola was established by Peters (1969) from male and female imagos and nymphs for A. froehlichi, and no other species was described since then. We are describing here three new species, based on male imagos.
The genus Hagenulopsis was established by Ulmer (1920) and is currently known from all the stages. Five species have been described, three from adults and nymphs: H. diptera Ulmer, H. minuta Spieth and H. traverae (Peters), and two only from nymphs: H. ingens and H. ramosa Lugo-Ortiz & McCafferty.
We are describing three new species of Hagenulopsis, two based on male and female imagos and nymphs, and the third from male and female imagos.
We are also including a key to separate the male and female imagos of all the known species of Askola and Hagenulopsis. The aspect and coloration of the nymphs of Hagenulopsis is very similar, and we found it very difficult to separate them. As we did not have specimens of all the species, we prefer not to include a key to separate them.
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Material and methods
The material used in this study is preserved in ethyl alcohol 75%. Male legs and genitalia and nymphal parts were dissected and mounted in Canada Balsam. Wings were mounted dry. Female descriptions only list those characters that differ from male (excluding those related to sexual dimorphism). The material is deposited in the following institutions: Instituto-Fundación Miguel Lillo, Tucumán, Argentina (IFML); Museu de Zoologia, Universidad de São Paulo, Brazil (MZSP); Museo de Entomología, Universidad del Valle, Cali-Colombia (MUSENUV), Museo Ecuatoriano de Ciencias Naturales, Quito, Ecuador (MECN).
Key to separate the imagos of Askola and Hagenulopsis
Males
1. Vein ICu1 of fore wings joined at base to CuA (Figs. 25–27); penis lobes without ventral spines (Figs. 28, 31, 34) .................................................................................................................................................................. 2 (Askola)
1’. Vein ICu1 of fore wings joined at base to CuP (Figs. 37–39); each penis lobe with a ventral spine (Figs. 40, 42–44) ........................................................................................................................................................ 5 (Hagenulopsis)
2(1). Cross veins of fore wings not surrounded with dark clouds (Fig 27)...................................................................... 32’. Cross veins of fore wings surrounded with dark clouds (Figs. 25–26) ................................................................... 43(2). Fore wing length approximately 7 mm; eyes meeting on meson of head (Figs. 11–12); penes not extending
beyond posterior margin of styliger plate (similar to Fig. 31); basal 1/3 of forceps brown, remainder paler; general coloration as in Fig. 10 .......................................................................................................................... A. froehlichi
3’. Fore wing length 4.5–5.3 mm; eyes separated on meson of head (Figs. 8–9); penes extending beyond posterior margin of styliger plate (Figs. 34–35); forceps light yellow washed with gray, lighter toward apex; general color-ation as in Fig. 7........................................................................................................................ A. cipoensis sp. nov.
4(2). Forceps yellowish-brown, except inner margins whitish; penes extending well beyond the posterior margin of styliger plate (Figs. 28–29); general coloration as in Figs. 1–3...............................................A. emmerichi sp. nov.
4’. Forceps whitish, except basal articulation orangeish; penes not extending beyond posterior margin of styliger plate (Figs. 31–32); general coloration as in Figs. 4–6 ............................................................ A. paprockii sp. nov.
5(1). Cross veins of fore wings blackish brown surrounded with dark clouds; dorsal portion of eyes yellowish white (Figs. 23–24); general coloration as in Fig. 22 ........................................................................................ H. diptera
5’. Cross veins of fore wings not surrounded with dark clouds (Figs. 37–39); dorsal portion of eyes darker (Figs. 14–15, 17–18, 20–21); general coloration not as above .......................................................................................... 6
6(5). Well developed bridge between stalks of upper portion of male eyes (Fig. 47) ....................................... H. minuta6’. Without well developed bridge between stalks of upper portion of male eyes ....................................................... 77(6). Upper portion of male eyes separated on meson of head by a length equal to maximum width of lateral ocellus
(distribution: Dominica and St. Lucia) .................................................................................................. H. traverae 7’. Upper portion of male eyes meeting on meson of head (Figs. 14, 17, 20, 23) ....................................................... 88(7). Light colored species, with abdominal segments II–VI translucent white, with black posterolateral spot (Figs.
16–18); first forceps segment long, three times length of styliger plate and straight (Fig. 41) ................................................................................................................................................................................. H. esmeralda sp. nov.
8’. Dark colored species, with abdominal segments II–VI heavily washed with black or blackish brown (Figs. 13, 19); first forceps segment short—not more than 2.3 times length of styliger plate, and curved medially (Figs. 41–42, 44) ................................................................................................................................................................ 9
9(8). Hind femora yellowish washed with black, heavier on apical 1/4, with a longitudinal lighter line; cerci dark brown ......................................................................................................................................................... H. lipeo sp. nov.
9’. Hind femora yellowish with black shading restricted to apical ¼; cerci yellowish ....................H. zunigae sp. nov.
Females 1
1. Cross veins of fore wings blackish brown surrounded with dark clouds; general coloration similar to Fig. 22 .......
1. Askola froehlichi, the only species known from females for the genus, can be separated from the species of Hagenulopsis by the wing characters included in the male key.
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.....................................................................................................................................................................H. diptera1’. Cross veins of fore wings not surrounded with dark clouds (Figs. 37–39); general coloration not as above ........ 22(1). Small species, body length 4.0 mm or less; cerci with darker annulations at articulation of three most basal seg-
ments .......................................................................................................................................................... H. minuta2’. Larger species, body length 5 mm or more; cerci without annulations as above ..................................................... 33(2). Abdominal sterna much paler than terga .................................................................................................................. 43’. Abdominal sterna concolorous with terga ................................................................................................................ 54(3). Abdominal terga II–VII with a paler, medial line (only subimago known, distribution: Dominica and St. Lucia) ..
.................................................................................................................................................................. H. traverae4’. Abdominal terga II–VII with a pair of paler submedial dots on anterior margin (similar to Fig. 16) .......................
................................................................................................................................................. H. esmeralda sp. nov.5(3). Hind femora yellowish washed with black, heavier on apical ¼, with a longitudinal lighter line .............................
......................................................................................................................................................... H. lipeo sp. nov.5’. Hind femora yellowish with black shading restricted to apical ¼ ............................................. H. zunigae sp. nov.
Discussion: Askola can be distinguished from the other genera of Leptophlebiidae by the following combination of characters, in the imago: 1) hind wings absent; 2) MA fork slightly asymmetrical, MP fork symmetrical; 3) vein ICu1 of fore wings joined at base to vein CuA; 4) claws of a pair dissimilar, one apically hooked and the other blunt; 5) penes divided, tubular, slender, apically pointed, and without appendages or spines (Figs. 28–36 ); and 6) female with egg guide prolonged to middle of abdominal sternum IX and 7) female sternum IX deeply cleft apically. In the nymph: 1) hind wing pads absent; 2) anteromedian emargination of labrum with two small denticles; 3) denticles of tarsal claws progressively larger apically; 4) dorsal and ventral portions of abdominal gills I–VII equal and plate-like, with the apical half of each plate bordered with finger-like processes; 5) posterolateral spines present on abdominal segments V–IX or VI–IX.The generic description of the male imago needs to be emended with the following characters to include the variations reported for the new species: 1) eyes separated (Fig 8) or meeting (Figs. 2, 6 and 11) on meson of head; 2) wings hyaline (Fig 27) or spotted (Figs. 1, 25, 26), costal cross veins basad to bullae absent (Fig. 27) or present (Figs. 25–26); 3) penes extending (Figs. 28, 34) or not (Fig 31) beyond posterior margin of styliger plate.
Male imago. Length: body, 5.0–5.2 mm; fore wing, 4.8–5.0 mm. General coloration (Fig. 1) thorax yellowish orange, abdomen translucent, blackish marks on thorax and abdomen forming a pair of sublateral longitudinal lines; wings with blackish marks. Head (Figs. 2–3). Dorsal portion of eyes grayish, lower portion black; eyes widely meeting dorsally on meson of head; head yellowish with black stripes between eyes and ocelli. Antennae whitish. Thorax. Pronotum yellowish white with blackish lateral third. Mesonotum orange yellow with lateral margin of scutum, scutellum and central line on scutellum blackish. Metanotum yellowish with lateral and posterior margins blackish. Pleurae and sterna yellowish white except sclerites close to base of legs II and III darker. Legs. Leg I yellowish white except tarsi whitish, black bands on apex of femur, subapex of tibia and base of tarsal segments III and IV; tarsal bands occupying ¾ of respective segment; claws grayish [legs II and III broken off and lost]. Wings (Figs. 1, 25). Membrane hyaline except base of C area yellowish and grayish spots mainly around cross veins as in Figs. 1, 25; longitudinal veins yellowish, cross veins blackish bordered with grayish; 4 costal cross veins from bulla to costal brace. Abdomen translucent white except segments VIII–X yellowish white. Terga with characteristic black pattern of marks and dots (Fig.1), sterna without marks. Genitalia (Figs. 28–30): styliger plate yellowish white darker on margins, forceps and
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penes light gray, paler towards apex. Terminal filament whitish with a black band on the base of each segment [cerci broken off and lost].
Material: 1 male imago from Colombia-Brazil, Amazonas, Reserva Natural Palmarí, quebrada Natividad, cuenca rio Yabarí, 150 m, N 04º 17' 28"- W 70º 17' 42", 28-V-2002, light trap, M.C. Zúñiga, D. Emmerich, A.J. Cardozo & R.J. Cardozo cols.; 1 male imago from Colombia-Brazil, Amazonas, Reserva Natural Palmarí, rio Yabarí, muelle Centro Administrativo, 120 m, N 04º 17' 10"- W 70º 17' 49", 29-V-2002, light trap, same collectors. Holotype deposited at MUSENUV, paratype at IFML.
Etymology: We dedicate this species to our friend and colleague Daniel Emmerich, one of the collectors of the type material.
Discussion: Askola emmerichi can be separated from the other species of the genus by the following combination of characters. Imago: 1) blackish marks on thorax and abdomen forming a pair of sublateral longitudinal lines (Fig. 1), wings with blackish marks (Figs. 1, 25); 2) dorsal portion of eyes grayish and widely meeting dorsally on meson of head (Figs. 2–3); 3) forceps yellowish-brown, except inner margins whitish; 4) penes extending well beyond posterior margin of styliger plate (Figs. 28–29).
Male imago. Length: body, 6.5–6.8 mm; fore wing, 6.5–6.7 mm. General coloration (Figs. 4–5) thorax yellowish white, wings and abdomen hyaline, with grayish marks. Head (Fig. 6). Dorsal portion of eyes grayish black, lower portion black; eyes widely meeting dorsally on meson of head; head yellowish white with two black stripes from eyes and ocelli to fore margin. Antennae whitish. Thorax yellowish white darker on meso and metanotum. Pronotum with blackish marks on lateral margins and two pairs of black sublateral spots. Mesonotum with a small black spot at base of wings and diffuse black marks from wing base to anterior margin. Metanotum with a pair of broad sublateral black marks. Pleurae with distinct black marks especially around coxae, sterna with central area washed with black. Legs yellowish white with slightly darker femora; trochanters II–III with black spots; subapical black band on tibia I; black medial mark on femora II–III. Wings (Fig. 26). Membrane hyaline except base of C area yellowish and grayish spots mainly around cross veins as in Fig. 26; longitudinal veins yellowish gray lighter towards hind margin, cross veins blackish bordered with grayish; 4 costal cross veins from bulla to costal brace. Abdomen (Figs. 4–5) translucent white except segments IX–X yellowish heavily washed with black. Tergum I completely washed with black, terga II–VIII with a black band on lateral and hind margins, except medial line; terga VII–VIII with a pair of submedian blackish spots near fore margin. Abdominal sternum I with anteromedian black mark and a pair of blackish wide diagonal stripes, sterna II–VII with small anterolateral spot and thin and short oblique blackish stripe ending on spiracles, sterna VIII–IX with lateral margins blackish. Genitalia: styliger plate whitish uniformly washed with gray, forceps whitish except basal half washed with gray, penes yellowish washed with gray. [Caudal filaments broken of and lost].
Material: Holotype and 1 paratype male imagos from Brazil, Minas Gerais, rio Peixe/rio Itambé confluence, S 19º 17.525'- W 43º 15.457', 500 m, 4-II-1998, Holzenthal & Paprocki Cols. Holotype deposited at MZSP, paratype at IFML.
Etymology: We dedicate this species to H. Paprocki, Trichoptera specialist, one of the collectors of the type material.
Discussion: The male imago of Askola paprockii sp. nov. can be distinguished by the following combination of characters: 1) General coloration yellowish white with grayish marks (Figs. 4–5), wings with grayish spots (Fig. 26); 2) dorsal portion of eyes grayish black, eyes widely meeting dorsally on meson of head (Fig. 6); 3) 4 costal cross veins from bulla to costal brace (Fig. 26); 4) forceps whitish except basal half washed with gray (Fig. 5); 5) penes not extending beyond posterior margin of styliger plate (Figs. 31–32).
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Male imago. Length: body and fore wing, 4.5–5.3 mm. General coloration (Fig. 7) yellowish, abdomen washed with gray. Head (Figs. 8–9). Dorsal portion of eyes yellowish brown, lower portion black; eyes widely separated dorsally on meson of head by ca. twice width of lateral ocelli; head yellowish washed with black between ocelli. Antennae: scape yellowish brown, pedicel yellowish white with a grayish band on apical half, flagellum whitish. Thorax yellowish with carinae and sutures slightly darker. Legs yellowish paler toward apex and with narrow subapical blackish band on tibiae, stronger on tibia I, and subapical blackish band on femora III. Wings (Fig. 27). Membrane hyaline with longitudinal and cross veins yellowish gray lighter towards hind margin; no costal cross veins basad to bulla. Abdomen (Fig. 7) translucent yellowish white except segments VIII–X whitish, segments I–II and VIII–X heavily washed with black; segments III–VII with a transversal blackish band, narrower at center. Terga I–IX with a transparent medial line. Genitalia (Figs. 34–36): styliger plate yellowish with hind margin orangeish; forceps light yellow washed with gray lighter toward apex, penes yellowish orange washed with gray. Caudal filaments yellowish white with every other intersegmental union with a narrow black band.
Material: Holotype male imago and 14 paratypes male imagos from Brazil, Minas Gerais, Serra do Cipó, km 126, II-1973, P. Montouchet & I. Sazima. Holotype and 6 paratypes deposited at MZSP, 7 paratypes at IFML.
Etymology: cipoensis, from the type locality, Serra do Cipó.Discussion: male imago of Askola cipoensis sp. nov. can be distinguished by the following combination
of characters: 1) General coloration yellowish, abdomen washed with gray (Fig. 7); 2) dorsal portion of eyes yellowish brown, eyes widely separated dorsally on meson of head (Figs. 8–9); 3) no costal cross veins basad to bulla (Fig. 27); 4) forceps light yellow washed with gray; 5) penes extending slightly beyond posterior margin of styliger plate (Figs. 34–35).
Material: 1 male imago from Brazil, SP, Casa Grande, Rib. Coruja, 11-IV-1983, light, C. G. Froehlich col.; 1 male imago from Brazil, SP, Campos do Jordão, Parque Estadual Campos do Jordão, córrego Galharada, 16-X-1998, C. G. Froehlich & H. Paprocki cols.; 1 male imago from Brazil, SP, Campos do Jordão, Parque Estadual Campos do Jordão, rio Sapucaí e córrego Galharada, 7–8/I/1986, C. G. Froehlich & L. G. Oliveira cols.; 1 male imago, 6 male subimagos and 3 female subimagos from Brazil, SP, Campos do Jordão, Parque Estadual Campos do Jordão, 16-XII-1987, C. G. Froehlich & L. G. Oliveira cols.; 2 mature male nymphs from Brazil, SP, Campos do Jordão, Parque Estadual Campos do Jordão, 18-XI-1987, C. G. Froehlich & L. G. Oliveira cols.; 1 male and 1 female from Brazil, SP, Jundiaí, Serra do Japi, Trilha da cachoeira do Paraíso, riacho paraíso, S23°14 W46°57”, 1050 m, 18–20-XII-2007, Puçá, L. S. Lecci; R. A. Moretto & E. A. Nascimento cols.; 1 male and 1 female from Brazil, SP, Jundiaí, Serra do Japi, córrego Paraiso, 20-II-2008, Malaise trap, L. S. Lecci, R. A. Moretto & E. A. Nascimento cols. All material deposited at MZSP, except 1 male imago from Rib. Corujá, 1 male imago and one nymph from Campos do Jordão, 1 male and 1 female imagos from Serra do Japi.
Discussion: male imago of Askola froehlichi can be distinguished by the following combination of characters:1) General coloration yellowish, abdomen washed with gray (Fig. 10), wings hyaline; 2) dorsal portion of eyes blackish (Figs. 11–12); 3) 4 weak costal cross veins basad to and 1 on bulla; 4) basal 1/3 of forceps brown, remainder paler; 5) penes not extending beyond posterior margin of styliger plate.
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FIGURES 7–12. Askola. Figs 7–9, Askola cipoensis sp. nov., male imago. 7, general aspect, lateral view; 8, head, dorsal view; 9, head, lateral view. Figs 10–12, A. froehlichi, male imago. 10, general aspect, lateral view; 11, head, dorsal view; 12, head, lateral view.
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Discussion: Hagenulopsis Ulmer can be separated from the other genera of the family by the following combination of characters, in the adult: 1) hind wings absent; 2) MA fork symmetrical or asymmetrical, MP fork symmetrical; 3) vein ICu1 of fore wings attached at base to vein CuP (Figs. 37–39); 4) tarsal claws of a pair dissimilar, one apically pointed, other blunt; 5) penes divided, tubular, apically acute, with two small ventral spines located between 1/5–1/3 distance from apex; 6) inner angle of forceps segment I located about 1/2–1/3 distance from base; 7) female with well developed egg guide, which is prolonged to middle of abdominal sternum IX; and 8) female sternum IX deeply cleft apically. In the nymph: 1) labrum with rounded margins, and anteromedian emargination with 3–5 denticles; 2) mandible with few or no setae on apical third of outer margin; 3) apical 1/2 of segment III of labial palpi constricted; 4) denticles of tarsal claws progressively larger toward apex, except apical denticle much larger; 5) gills on abdominal segments I–VII lanceolate, narrow, dorsal and ventral portions similar; 6) posterolateral spines on abdominal segments VI–IX, larger posteriorly, only slightly developed in IV and V.
The generic description needs to be amended with the following characters to include the variations reported for the new species: In the imago, 1) penes divided, tubular, apically acute, with two small ventral spines located between 1/5–1/3 distance from apex; 2) inner angle of forceps segment I located about 1/2–1/3 distance from base. In the nymph, 1) labrum with rounded margins, and anteromedian emargination with 3–5 denticles.
Lugo-Ortiz & McCafferty (1996) separated one of the two species they described from nymphs, mainly on the presence of branched setae on the distal end of hind tibiae. The nymphs we are describing and H. diptera we studied (from Sao Paulo) have only simple setae on hind tibiae.
Hagenulopsis lipeo sp. nov. Domínguez, Molineri and Mariano
Male imago (Fig. 19). Length: body, 5.0–5.8 mm; fore wings, 5.0–5.6 mm. Eyes: upper portion grayish brown meeting dorsally, basally contiguous; facets small and numerous (Figs. 20–21). Facets of lower portion black, small. Head yellowish brown with black markings close to base of eyes. Ocelli whitish, lateral ocelli twice the size of the median one. Antennae: scape yellowish white, pedicel brownish [flagellum broken off and lost]. Thorax. Nota and pleurae reddish brown with carinae darker and whitish membranes; sterna yellowish brown with whitish membranes. Leg I yellowish heavily washed with black specially on femora, tarsi lighter; legs II–III with coxae and trochanter yellowish white, remainder segments yellowish washed with black specially at apex of femora; longitudinal lighter line on femora II–III; claws in all legs yellowish washed with black. Wings membrane hyaline uniformly tinted with light brown, veins brownish lighter toward apex, pterostigma clouded white (Fig. 37); no costal cross veins basad to bulla. Abdomen. Terga yellowish heavily washed with black except on two submedial and two sublateral paler areas close to anterior margin on each terga II to VI; sterna yellowish white washed with black except anterior margin and ganglia; posterior margin of sterna VII–VIII translucid. Genitalia (Figs. 43–46): styliger plate and forceps yellowish brown except inner margins of forceps whitish, penes yellowish white; short styliger plate (ratio maximum width/medial length: 1.95–2.17) with a similar width along its entire length, hind margin straight to slightly concave; first forceps segment curved medially (ratio length F1/styliger: 2.0–2.3) (Figs. 43–44). Caudal filaments, basal half of first segment yellowish brown; rest of filaments yellowish black basally, turning yellowish gradually toward apex.
Female imago. Length: body, 4.4–5.6 mm; fore wings, 5.0–5.8 mm. Head yellowish brown except base of ocelli blackish, and area between ocelli and eyes whitish. Eyes black. Thorax yellowish brown, sterna yellowish white except darker medially. Some females have lighter wing membranes than the males.
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Abdomen ventrally with lighter areas covering anterior ¾ of segments II–V; egg guide yellowish black lighter toward apex, apically acute.
FIGURES 13–18. Hagenulopsis. Figs 13–15, H. zunigae sp. nov. 13, male imago, general aspect, lateral view; 14, head, dorsal view; 15, head, lateral view. Figs 16–18, H. esmeralda sp. nov. 16, male imago, general aspect, lateral view; 17, head, dorsal view; 18, head, lateral view.
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FIGURES 19–24. Hagenulopsis. Figs 19–21, H. lipeo. 19, male imago, general aspect, lateral view; 20, head, dorsal view; 21, head, lateral view. Figs 22–24, H. diptera. 22, male imago, general aspect, lateral view; 23, head, dorsal view; 24, head, lateral view.
Mature nymphs. Female length: body, 5.4–5.6 mm, cerci 3.7–3.9 mm, terminal filament, 4.8–5.0 mm. Male length: body 5.3–5.6 mm, cerci 5.3 mm, terminal filament, 3.6 mm. Head. Eyes of male with reddish black upper portion and blackish lower portion; eyes of female black; ocelli whitish with inner half margin blackish. Antennae: scape yellowish, pedicel blackish, flagellum yellowish lighter toward apex. Dorsum of
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head yellowish brown stained with black in central area. Mouthparts yellowish stained with black at: base of labrum, basal half of mandibles, outer margin and palpi segment I of maxilla, posterior margin of superlinguae, and submentum; molae of mandible and apical row of setae of maxilla orange brown; anteromedian emargination of labrum with 3 denticles, the median smaller than lateral ones. Thorax. nota yellowish white with latero-medial and latero-posterior areas washed with black; pro- and mesosternum yellowish white with ganglia and margins stained with black, metasternum yellowish white almost completely washed with black except inner margin of articulation of coxae. Leg I light orange yellow with coxa and margins of trochanters washed with black, femur almost completely washed with black except lighter oblicuous line. Legs II and III yellowish with coxa and two longitudinal lateromedial areas on femora, and longitudinal stripe on tibiae blackish; tibiae and tarsi darker than femora, claws orange brown. Tarsal claws with 8–9 denticles. Abdomen dorsally yellowish orange washed heavily with black especially on latero-posterior areas of terga; sterna yellowish with central area tinged with black, lighter in central area. [Posterolateral projection as in minuta description]. Gills whitish with blackish tracheae. Cerci yellowish orange, few setae on each intersegmental union.
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Material: Holotype male imago from ARGENTINA: Salta, PN Baritu, Lipeo, estación 5, 13-XI-2004; 98 male and 8 female imagos same data as holotype. Paratypes: 18 nymphs from ARGENTINA: Salta, Parque Nacional Baritu, Lipeo, Aº Los Naranjos, 13-XI-2004, E. Domínguez col.; 2 nymphs, same data as holotype, except Aº Baritu, 17-XI-2004. Other material: Jujuy, El Carmen, Aº Las Lanzas, 3-III-2000, Domínguez & Molineri cols. BOLIVIA: Dpto. Santa Cruz, Ichilo Prov., 10 km NE Hierba Buena Militar, Quebrada El Bronce, 1100 m, 19-IV-1993, E. Domínguez & M. Paco cols. All material deposited at IFML, except 5 male imagos at MZSP and 5 male imagos at MUSENUV.
Etymology: Lipeo, name of the type locality. Biology: Hagenulopsis lipeo sp. nov. was collected in a small effluent of the Lipeo river, in Salta
Province, NW Argentina. The stream was about 3 m wide and between 20 cm to 60 cm deep. The bottom was covered with rocks, with some sandy areas. A mating flight was observed during the morning hours, 1 m above the water course, performing the typical up and down pattern of most leptophlebiid species. It is interesting to note that the pattern does not seem, at least on the main features, to be affected by the dipterous conditions of the specimens. The size of the swarm was approximately 5 m long and 1 m width, and extended for about an hour. A few females were caught among the flying males.
Discussion: This species seems to have a rather extended distribution from NW Argentina to central Bolivia. It has been observed certain variation in the shape of the apex of the male styliger plate (Figs. 45–46), that is due to the angle of observation. It can be separated from the other- species of the genus by the following combination of characters. Imago: 1) general coloration dark (yellowish, heavily washed with black), pattern as in Fig. 19; 2) eyes of male meeting on -meson of head (Figs. 20–21); 3) first forceps segment not more than 2.3 times length of styliger plate, and curved medially (Fig. 43); 4) hind femora yellowish washed with black, heavier on apical 1/4, with a longitudinal lighter line; 5) cerci dark brown.
Male imago (Fig. 16). Length: body, 4.8–5.2 mm; fore wings, 4.8–5.0 mm. Eyes: upper and lower portions black, meeting dorsally, in frontal view the eyes are contiguous except small basal and medio-apical openings; facets small and numerous. Head yellowish washed with black diffusely. Ocelli whitish, lateral ocelli twice the size of the median one. Antennae: scape yellowish white, pedicel brownish, flagellum yellowish lighter toward apex. Thorax. Pronotum yellowish white heavily washed with black except central area and two C-shaped submdian marks on posterior margin lighter; mesonotum orangish yellow with sutures and carinae darker, metanotum yellowish white with posterior and lateral margins washed with black; pleurae sclerites yellowish orange, membranes whitish heavily washed with black; sterna yellowish orange except central portions whitish. Legs yellowish white with brownish spot at apex of femora, hooked claw of a pair orange blunt claw grayish. Wings membrane hyaline except basal to costal brace brownish, veins yellowish brown, crossveins whitish, pterostigma clouded white (Fig. 38); bullae (better distinguishable in alcohol specimens) present on Sc, R1 , R4+5 and MP1 about ½ from base; 4 costal cross veins from bulla to costal brace. Abdomen.
Terga II–VI translucent white with black posterolateral angles; tergum VII whitish with sublateral circular areas and posterolateral angles washed with black; terga VIII–IX whitish heavily washed with black except narrow medial line; tergum X whitish with blackish anterolateral corners; abdominal sterna whitish. Genitalia (Figs. 41–42): whitish except basal articulation of forceps and posterior margin of styliger plate orangeish and penes light orange; long styliger plate (ratio maximum width/medial length: 1.66–1.95) wider at base becoming thinner toward apex, hind margin markedly concave; first forceps segment long and straight (ratio length forceps I/styliger plate: 3) (Fig. 41). Caudal filaments translucent white with black annulations, narrow near base of filaments and widening towards apex.
Female imago. Length: body, 5.0–5.5 mm; fore wings, 5.3–5.5 mm. Eyes black. Head yellowish white with two dark stripes between lateral ocelli and posterior margin. Antennae scape and pedicel yellowish washed with black, flagellum grayish lighter towards apex. Thorax. Pronotum whitish heavily washed with
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black; mesonotum yellowish orange margins darker; pleurael sclerites yellowish orange slightly washed with black, membranes whitish heavily washed with black; sterna yellowish except central parts whitish. Legs coxae and trochanter yellowish orange washed with black on coxae, femora whitish with black subapical band, tibiae and tarsi yellowish white, claws grayish. Wings. Membrane hyaline basally brown as in male, longitudinal and crossveins brownish, bullae as in male. Abdomen. Terga whitish, heavily washed with black from I to IX, except median area of tergum VII, and a pair of submedial dots on anterior margin of terga II–VII paler; sterna whitish except posterior margin of sternum VI and egg guide brownish, egg guide apically acute. Caudal filaments light yellowish brown with annulations as in male.
Material. Holotype male from ECUADOR: Esmeralda Prov., Canton Eloy Alfaro, Parroquia Telembí, Estero Arenales, N 0º 40' 06", W 78º 69' 26", 40 m, 15-IV-2002, E. Domínguez, F. Bersoza, M.C. Zuñiga coll. Allotype, and paratypes (42 males, 5 females) same data as Holotype; 6 male and 1 female imagos (paratypes) from ECUADOR: Esmeralda Prov., Canton Eloy Alfaro, Parroquia Telembí, Comunidad San Miguel, Estero Charco Vicente, N 0º 41' 36", W 78º 54' 33", 80 m, 14-IV-2002, E. Domínguez, F. Bersoza, M.C. Zuñiga coll. Imagos of both sexes were captured in the same nuptial flight. Holotype, Allotype and half of the partatypes deposited in MECN, rest of paratypes divided equally between IFML and MUSENUV.
Etymology: Esmeralda, from the name of the Ecuadorean province where the species was collected.Discussion: Hagenulopsis esmeralda sp. nov. can be separated from the other species of the genus by the
following combination of characters. Imago: 1) general coloration light, with abdominal segments II–VI translucent white, with black posterolateral angles (Figs. 16–18); 2) eyes of male meeting on dorsum of head (Figs. 17–18); 3) first forceps segment long (3 times length of styliger plate), and straight (Fig. 42); 4) hind femora yellowish white with brownish spot at apex; 5) cerci translucent white with black annulations, narrow near base of filaments and widening towards apex.
Hagenulopsis zunigae sp. nov. Domínguez, Molineri and Mariano
Male imago (Fig. 13). Length: body, 6.0–6.8 mm; fore wings, 6.0–6.5 mm. Eyes: upper portion dark reddish brown, lower portion black, meeting dorsally, in frontal view the eyes are contiguous; facets small and numerous. Head yellowish washed with black in median area delimited by eyes and ocelli. Ocelli whitish, median ocelli very small, lateral ocelli 4 times the size of the median one. Antennae: scape yellowish and pedicel yellowish brown, flagellum grayish, lighter towards apex. Thorax. Pronotum yellowish with margins and paramedian lines blackish; mesonotum yellowish orange with sutures and carinae darker, metanotum yellowish orange diffusely washed with black darker along margins; pleural sclerites yellowish orange, membranes whitish heavily washed with black; sterna yellowish orange except central portions whitish and margins of sclerites blackish. Legs. Leg I: coxa, trochanter and femur yellowish heavily washed with black, tibia light yellowish black, tarsi whitish except apical tarsomere washed with black, hooked claw grayish, blunt claw translucent white. Legs II and III similar to leg I, except femora shading restricted to apical ¼. Wings membrane hyaline tenuously tinged with brown; except basal to costal brace brownish, veins grayish brown, crossveins lighter, pterostigma clouded white; bullae (better distinguishable in alcohol specimens) present on Sc, R1 , R4+5 and MP1 about ½ from base (Fig. 37); 4 costal cross veins from bulla to costal brace.
Abdomen. Terga yellowish white heavily washed with blackish brown except terga III–VII with anterior margins with central area and corners not tinged; sterna yellowish white shaded with brownish black except ganglia and semicircular area close to posterior margin on sterna III–VIII, lighter. Genitalia (Fig. 40): styliger plate yellowish white with basal half and posterior margins washed with black; forceps yellowish white with segment I heavily washed with black; penes yellowish white; short styliger plate (ratio maximum width/medial length: 1.95–2.16) with a similar width along its entire length, hind margin straight to slightly concave; first forceps segment curved medially (ratio length F1/styliger: 2.2) (Fig. 40). Caudal filaments yellowish gray lighter towards apex.
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FIGURES 37–47. Hagenulopsis. Figs 37–39, male fore wing: 37, H. zunigae sp. nov.; 38, H. esmeralda sp. nov.; 39, H. lipeo. Fig. 40, H. zunigae sp. nov., genitalia, ventral view. Figs 41–42, H. esmeralda sp. nov.: 41, genitalia, ventral view; 42, penes, detail. Figs 43–46, H. lipeo: 43, genitalia, ventral view; 44, penes, detail; 45, apex of styliger plate, ventral view; 46, idem, variation. Fig. 47, H. diptera, male head, dorsal view.
Female imago. Length: body, 6.1–6.3 mm; fore wings, 6.5 mm. Head yellowish gray, with whitish area between eyes and center of head. Eyes black. Thorax yellowish brown, with pleural sclerites washed with black. Abdomen lighter than male; egg guide yellowish washed with black, apically acute.[Caudal filaments broken off and lost].
Mature male nymphs. Length: body 5.2–6.7 mm, cerci 3.5–4.0 mm, terminal filament, 5.0 mm. Head. Eyes of male with yellowish brown upper portion and blackish lower portion; eyes of female black; ocelli whitish with inner half margin blackish. Antennae whitish with blackish band occupying 2/3 of pedicel. Dorsum of head yellowish washed with black in central area. Mouthparts yellowish white with clypeus, labrum, base of mandibles, stipes of maxillae and postmentum of labium washed with black; molae of mandibles and crown of setae on maxillae orangeish; anteromedian emargination of labrum with 3 denticles of similar size. Thorax. Thoracic nota light yellow orange, pronotum and metanotum heavily washed with black, mesonotum with outer margin and base of wingbuds blackish; thoracic sterna yellowish heavily washed with black except basal part of prosternum and area between legs in mesosternum. Leg I yellowish with two subapical black spots on femora, tibiae and tarsi darker. Legs II and III with coxae, trochanters and femora yellowish white, trochanters washed with black, femora with subapical black band, tibiae and tarsi yellowish especially on leg III. Tarsal claws yellowish white, with 9–10 denticles. Abdomen light yellow orange, darker dorsally and with a blackish pattern similar to male imago but more diffuse. [Posterolateral
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projection as in minuta description]. Gills whitish with blackish tracheae. Caudal filaments yellowish orange lighter towards apex, with setae on each intersegmental union.
Material. Holotype male imago from COLOMBIA: P. N. Farallones de Cali, Peñas Blancas, río Pichinde, N 3º 25' 45", W 76º 39' 27", 2.000 m, 17-18-III-1999, E. Domínguez, M.C. Zuñiga & C. Molineri; allotype female imago, 7 male imagos and 1 male nymph paratypes, same data as holotype; 7 male and 1 female imagos and 2 male nymphs paratypes from COLOMBIA: Boyacá, Municipio de Arcabuco, Santuario de Flora y Fauna de Iguaque, quebrada Carrizal, N 5º 42' 37", W 73º 27' 43", 2720 m, 6-II-1997, E. Domínguez, M. Pescador & L. Baena cols. All material deposited at MUSENUV, except 4 male imagos from rio Pichinde, 3 male, 1 female imago and 2 nymphs from quebrada Carrizal, deposited at IFML.
Etymology: The species is dedicated to Maria del Carmen Zuñiga, friend and colleague for her enthusiasm and contributions to the knowledge of Colombian aquatic insects.
Discussion: H. zunigae sp. nov. can be separated from the other species of the genus by the following combination of characters. Imago: 1) General coloration dark (yellowish white heavily washed with blackish brown except terga III–VII with anterior margins with central area and corners not tinged), pattern as in Fig. 13; 2) eyes of male meeting on dorsum of head (Figs. 14–15); 3) first forceps segment around 2.2 times length of styliger plate, and curved medially (Figs. 41–42); 4) hind femora yellowish with black shading restricted to apical ¼; 5) cerci yellowish.
Material studied: One male imago from BRAZIL, São Paulo, Campos do Jordão, Parque Estadual, 16/XII/1987. C. G. Froehlich & L. G. Oliveira cols. Six nymphs, same data, except date: 18/XI/1987. Three nymphs deposited at MZSP, remainder at IFML.
Discussion: This species was recently redescribed (Peters & Domínguez, 2001), it can be separated from the other species of the genus by the following combination of characters. Imago: 1) general coloration yellowish brown, pattern as in Fig. 22, 2) cross veins surrounded with dark clouds; 3) dorsal portion of male eyes yellowish white, meeting on dorsum of head (Figs. 23–24); 4) first forceps segment around 1.5 times length of styliger plate, and curved medially (Figs. 41–42); 5) hind femora yellowish-white, with wide medial and narrower apical grayish black bands; 6) cerci yellowish-white, with basal 1/3 of each segment grayish.
Discussion: This is a very small species (body size 3–4 mm) as noted by Spieth (1943), in the species description. It is known from Surinam, Brazil and Venezuela. Peters & Dominguez (2001) detailed variations in size, and coloration. The Venezuelan specimens are larger and the color pattern is more pronounced than the others. H. minuta can be separated from the other species of the genus by the following combination of characters. Imago: 1) general coloration reddish brown, heavily washed with blackish brown; 2) upper portion of male eyes separated basally, meeting medially with well developed eye bridge on inner margin of upper portion; 3) first forceps segment around 2 times length of styliger plate, and curved medially; 4) hind femora yellowish, with wide subbasal and apical dark bands; 5) cerci pale, articulations of basal 3 segments darker.
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Akcnowledgments
We are grateful to María del Carmen Zúñiga, Daniel Emmerich, Lucas Lecci and Claudio Froehlich for material donation. Partial support was obtained from ANCYPT (PICT 528 and PICT 351) and CONICET (PIP 1484). The two first authors are member of the CONICET, which support is acknowledged.
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