Key to the Species of Cosmetidae (Arachnida, Opiliones) of Central America, with Notes on Penis Morphology and Sexual Dimorphisms

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VICTOR R. TOWNSEND, JR.1,5, CARLOS VÍQUEZ2, PETER A. VANZANDT3, & DANIEL N. PROUD4 1Department of Biology, Virginia Wesleyan College, 1584 Wesleyan Drive, Norfolk, Virginia 23502 USA. E-mail: [email protected] 2INBio, Apdo. 22-3100, Santo Domingo, Heredia, Costa Rica. E-mail: [email protected] 3Department of Biology, Birmingham-Southern College, 900 Arkadelphia Road, Birmingham, Alabama 35254 USA. E-mail: [email protected] 4Department of Biology, University of Louisiana at Lafayette, Box 42451, Lafayette, Louisiana 70504–2451 USA. E-mail: [email protected] 5Corresponding author

Abstract

To facilitate identification of harvestmen of the family Cosmetidae in Central America, we developed dichotomous keys that distinguish the 33 known genera and the 133 described species for this region. Couplets are based upon characters found in the literature and examinations of museum specimens. Important characters include the number of tarsomeres on leg I, armature of the dorsal scutum, free tergites and legs, as well as the coloration and relative length of the body and legs. In addition, we provide a summary of sexually dimorphic features and comment on the potential usefulness of penis morphology and coloration as characters for distinguishing taxa.

Key words: Arachnida, Central America, Cosmetidae, Laniatores, Opiliones, taxonomic key

Resumen

Para facilitar la identificación de Opiliones de la familia Cosmetidae en Centroamérica, nosotros desarrollamos una clave dicotómica que distingue los 33 géneros conocidos y las 133 especies descritas para esta región. Cada par de opciones esta basadas en caracteres que se encontraron en la literatura y revisión de especímenes de museo. Entre los caracteres de importancia están el número de tarsómeros de la pata I, armadura de el escudo dorsal, tergitos libres y patas, así como la coloración, tamaño relativo del cuerpo y patas. Además, nosotros suministramos un resumen de caracteres sexuales dimorficos y comentarios en la utilidad potencial de la morfología del pene y su coloración como caracter para distinguir taxones.

Palabras clave: Arachnida, Centroamérica, Cosmetidae, Laniatores, Opiliones, clave taxonómica

Introduction

In Neotropical forests, harvestmen (Arachnida, Opiliones) are among the most commonly encountered arthropods, particularly after dusk, when individuals are frequently seen in the leaf litter or climbing tree buttresses, lianas and other vegetation (Acosta & Machado 2007; Townsend et al. 2008). Most species are generalist predators, feeding upon a diverse array of invertebrates (Acosta & Machado 2007), but their diets may also include fungi, flowers, or fruits (Machado & Pizo 2000). In contrast to insects and spiders (for a review see Bragagnolo et al. 2007), harvestmen have seldom been used to assess the impact of forest management practices. In the Atlantic forests of Brazil, the abundance and presence of rare species of harvestmen from the families Gonyleptidae and Sclerosomatidae were strongly affected by the absolute size

Accepted by A. Perez-Gonzalez: 24 Feb. 2010; published: 30 Mar. 2010 1 TERMS OF USE This pdf is provided by Magnolia Press for private/research use. Commercial sale or deposition in a public library or website is prohibited. and relative quality of forested patches (Bragagnolo et al. 2007). In temperate spruce and fir forests of North America, the abundance of harvestmen of genus Leiobunum (Sclerosomatidae) was significantly reduced in clear-cut strips (Jennings et al. 1984). Field studies of harvestmen in Central America have the potential to provide important insights into the efficacy of management practices, particularly those aimed at maintaining or restoring forested habitats (Kremen et al. 1993; Bragagnolo et al. 2007). Potential advantages of using these arachnids as ecological indicators include the richness of species richness exhibited by the group (239 described species in Central America) and the high endemism exhibited by harvestmen in tropical forests (Pinto-da-Rocha et al. 2005). Presently, the known harvestmen fauna of Central America (Roewer 1953; Kury 2003) features representatives of the families Cosmetidae (33 genera, 133 species), Cranaidae (2 genera, 3 species), Gonyleptidae (4 genera, 11 species), Manaosbiidae (4 genera, 4 species), Samoidae (3 genera, 4 species), Sclerosomatidae (4 genera, 41 species), Stygnopsidae (1 genus, 2 species), Stygnommatidae (1 genus, 5 species) and Zalmoxidae (6 genera, 36 species). A significant challenge to the use of harvestmen assemblages as ecological indicators in Central America is the fact that relatively little or nothing is known about their natural history (but see Mora 1990; Donaldson and Grether 2007a, 2007b) or geographic ranges (Roewer 1953; Kury 2003). There is also a significant bias with respect to the number of species recorded for each country (Roewer 1953; Kury 2003). The harvestmen fauna of Costa Rica (121 species) is the best characterized, whereas the total numbers of species for Belize (30 species), Panama (48 species) and Guatemala (51 species) probably represent considerable underestimates of the actual number of species present. The faunas of El Salvador (15 species), Honduras (9 species), and Nicaragua (2 species) are poorly known. Although excellent guides for identifying families have recently been published (Cokendolpher et al. 2007; Pinto-da-Rocha 2007), there are still no published taxonomic keys that distinguish species of harvestmen for Central America. Therefore, we developed taxonomic keys for the Cosmetidae, the most diverse family in the region (Kury 2003). Cosmetid harvestmen are easily distinguished from species of other families on the basis of the morphology of the pedipalp (Kury & Pinto-da-Rocha 2007). In cosmetid harvestmen, the femur of the pedipalp is laterally compressed and the tibia is spoon-shaped (Fig. 1). The Cosmetidae is endemic to the Western Hemisphere, with species occurring from the southern U.S. to Argentina with the highest levels of diversity concentrated in Mexico, Central America, the Caribbean, and northern South America (Kury 2003; Kury & Pinto-da-Rocha 2007). The Cosmetidae has traditionally been divided into two subfamilies on the basis of the morphology of the tarsal claws on legs III and IV (Roewer 1912; Kury & Pinto-da-Rocha 2007). Members of the Discosomaticinae (10 genera, 29 species) have pectinate claws, Cosmetinae (116 genera, 681 species) have smooth claws (Kury, 2003). All described cosmetid species in Central America are members of the Cosmetinae (Kury 2003). In the keys, we used the number of tarsomeres on leg I (Table 1) and the armature on the dorsal scutum (Table 2) as major characters because these features have been extensively used in taxonomic studies of the Cosmetidae from Central America (Roewer 1912, 1923, 1927; Goodnight & Goodnight 1953a, 1953b). The segmentation of the tarsi to define genera has been criticized (e.g., Kury et al. 2007) because the numbers of tarsomeres for especially legs II–IV have been observed to exhibit considerable intraspecific variation. In our keys, we avoided using tarsomere numbers for legs II–IV as characters, but we included published reports (if known) for ranges for observed tarsal formulae (TF: denoted as the number of tarsomeres occurring on each leg, i.e., Leg I: Leg II: Leg III: Leg IV). We also used characters related to body and leg coloration as well as relative leg size and total body length for species identification. Although body shape has shown considerable potential for use as an informative character in evaluating monophyly in several Neotropical genera (Kury et al. 2007), we did not use this character in our key because most species from Central America exhibit α or β shapes and we had difficulty with reliably distinguishing these body shapes.

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TABLE 1. Number of tarsal segments on leg I for the known genera of Cosmetidae in Central America.

Tarsomeres Genera 5 Bokwina, Boneta, Holovonones, Kevonones, Metacynorta, Paravonones, Tajumulcia, Vonones, Vononesta, Vononula 6 Acromares, Cynorta, Cynortellana, Cynortoperna, Cynortula, Erginoides, Erginulus, Eucynorta, Eucynortella, Eucynortoides, Eucynortula, Eugnidia, Flirtea, Metarhaucus, Metavonones, Paracynorta, Reimoserius 7 or more Cosmetus, Eupoecilaema, Meterginus, Paecilaema, Paecilaemana, Poecilaemula TABLE 2. Armature of the abdominal scutum for the Cosmetinae from Central America. Cynorta, Eucynortula, and Paecilaema are not included because these genera exhibit more than one pattern of dorsal armature. -- = unarmed, vv = paired tubercles, V = single, median tubercle. Area I Area II Area III Area IV Taxa ------Erginoides, Eucynortella, Kevonones, Vononula -- -- vv -- Acromares, Bokwina, Boneta, Erginulus, Eucynorta, Metavonones, Paecilaemana, Paravonones, Poecilaemula, Vonones -- -- V -- Cosmetus vv -- vv -- Cynortellana, Cynortula, Eugnidia, Eupoecilaema, Flirtea, Meterginus, Taljumulcia vv vv vv -- Cynortoperna, Metarhaucus, Reimoserius vv -- vv vv Eucynortoides, Metacynorta, Paracynorta vv vv vv vv Holovonones, Vononesta

TABLE 3. Sexual dimorphisms exhibited by species of Cosmetidae from Central America. Males may possess an enlarged basitarsal segments on leg I, enlarged second cheliceral segments, or greater armature on leg IV. Many species exhibit multiple dimorphisms, but no species possesses a dimorphic leg IV without also having an enlarged basitarsus I or second cheliceral segment. Sexual Dimorphism Taxa Basitarsus I enlarged (only) Bokwina, Cynorta annulata, C. bifurcata, C. bromeliacia, C. circumbrosa, C. columbiana, C. flavornata, C. hondurensis, C. leucopyga, C. marginalis, C. posticata, Cynortellana, Cynortoperna, Cynortula brevipes, C. cingulata, C. koelpelii, C. pedalis, C. torquata, Erginoides tarsalis, Eucynorta albipustulata, E. areolata, E. biguttata, E. bipunctata, E. interposita, E. longispina, E. pictipes, E. puncticulata, E. transversalis, E. unicolor, E. vidua, Eucynortula albipunctata, E. tuberculata, E. lata, E. multilineata, Metacynorta, Paecilaema bifurca, P. limbatum, Paravonones, Reimoserius, Vonones, Vononula Chelicerae enlarged (only) Cosmetus, Cynorta limona, Eucynortula nannocornuta, Eupoecilaema, Holovonones, Paecilaema chiriquiense, P. e ut y pa , Paecilaemana quadripunctata, Paracynorta, Poecilaemula, Tajumulcia Basitarsus I enlarged AND Cynorta salvadorensis, Eucynorta quadripustulata, E. schmidti, Metarhaucus, Chelicerae enlarged Meterginus inermipes, Paecilaema lineatum Basitarsus I enlarged AND Cynorta astora, C. coxalis, C. dentipes, C. punctitergum, Cynortula longipes, C. Leg IV armed robusta, Erginulus arcuatus, E. biserratus, E. clavipes, E. crassescens, E. cristatus, E. erectispinus, E. figuratus, E. rectus, E. serratipes, E. simplicipes, E. sinuosus, E. subserialis, E. triangularis, Eucynorta bipectinata, E. picta, E. reimoseri, E. tenuipes, E. venosa, Eucynortella annulipes, Eucynortoides parvulus, Metavonones bisignatus, Meterginus apicalis, M. basalis, M. dorsalis, M. tibialis, Paecilaemana reimoseri Basitarsus I enlarged AND Acromares, Erginulus brevispinosus, E. clavotibialis, E. pectinigerus, E. serratifer, Chelicerae enlarged AND E. serratofemoralis, E. weyerensis, Eucynortula rugipes, Eugnidia, Flirtea, Leg IV armed Meterginus zilchi, Paecilaema inerme, P. forcipatum, P. gigas, P. pectiginerum

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For several genera (i.e., Erginulus, Meterginus), we used sexually dimorphic structures as characters. In many species of harvestmen, males possess chelicerae or leg segments that are enlarged or more heavily armed than the female. As an aid to future studies of the group, we provide a summary of the sexual dimorphisms exhibited by Central American taxa (Table 3), especially with respect to basitarsus I, the second segment of the chelicera, and the armature of leg IV. While the functional significance of these structures has not been assessed in the Cosmetidae, the armature of leg IV of males is used in intrasexual combat in the gonyleptid harvestmen Neosadocus maximus (Giltay 1928) and Acutisoma proximum Mello-Leitão 1922 (Willemart et al. 2008; Machado et al. 2009). In an effort to assess interspecific variation in genitalic structures for Central American Cosmetidae, we dissected penises of several taxa and examined them with the aid of scanning electron microscopy (SEM).

Materials and methods

Information for specific characters used in the dichotomous key was derived from the taxonomic literature as well as from the examination of museum specimens. The specimens examined in this study (Appendix 1) were borrowed from the collections of the American Museum of Natural History (AMNH), Senckenberg Museum (SMF), and INBio (Heredia, Costa Rica) or collected in the field. Field samples of harvestmen were made on 23–28 February 2007 in Parque Nacional General Division Omar Torrijos H., El Cope, Cocle Province, Panama (849.2’80”N, 80 5’45.7”W), 30 June–15 August 2007 and 30 June–13 August 2008 at La Selva Biological Field Station, Costa Rica (1026’15.0354”N, 840’1.19”W), and 6 August 2008 at Poas Volcano, Costa Rica (1013’3.36”N, 8413’55.92”W). Individuals were captured by hand and preserved in 70% ethanol. In the laboratory, harvestmen were photographed with a Leica stereomicroscope and image capturing system and identified with the aid of original descriptions and illustrations (Appendix 2). Comparisons were also made with AMNH and SMF specimens (Appendix 1). For species represented by males, the penis was dissected for examination by SEM. Specimens were dehydrated in a graded ethanol series, dried using hexamethyldisilizane, sputter-coated with gold for 2 min, and examined at an accelerating voltage of 15 kv with a Hitachi S-3000N SEM. Penises of the following species were examined using this protocol: Cynorta annulata Roewer 1947, C. marginalis Banks 1909, Cynortula cingulata Roewer 1933, Erginulus figuratus (Roewer 1947), Eucynorta puncticulata Roewer 1947, Eupoecilaema magnum Roewer 1933, Eupoecilaema sp.n., Meterginus apicalis Pickard-Cambridge 1905, Meterginus sp.n., Paecilaema sp.n. 2, Paecilaema sp.n. 4, Paecilaema sp.n. 6, Paecilaema sp.n. 7, and Reimoserius albipictus Roewer 1947. The most common terms used in the key are defined in the glossary or illustrated (Figs. 2–5). In general, we followed the terminology used by Kury & Pinto-da-Rocha (2002) and Acosta et al. (2007).

Glossary of Terms (Figs. 2–5) Abdominal scutum: dorsal plate formed by the fusion of the first five segments of the opisthosoma; delineated from carapace by scutal groove; five areas referenced from anterior (I) to posterior margin (V) as scutal areas and defined by sulci or color patterns; granular or spiniform tubercles (singular or paired) may occur on each area. Body length: measured from the anterior edge of the carapace to the posterior edge of the free tergites. Carapace: prosomic part of the dorsal scutum, delineated from abdominal scutum by scutal groove. Dorsal scutum: formed by the fusion of the carapace with the abdominal scutum. Free Tergites: the three most posterior dorsal sclerites of the opisthosoma that are not fused to the dorsal scutum. Legs: four pairs (I–IV), referenced from anterior (I) to posterior (IV); each leg is composed of the following segments (from proximal to distal): coxa, trochanter, femur, patella, tibia, metatarsus and tarsus. Leg length: measured from the proximal edge of the trochanter to the distal tip of the tarsus. Median line: a mid-dorsal line on the abdominal scutum that is either solid or made up of several smaller lines or spots. Ocularium: eye mound on the carapace. Reticulate pattern: dorsal pattern consisting of a series of fine lines or spots located along the margins of the carapace or abdominal scutum; referred to as filagree pattern by Pickard-Cambridge (1904–1905).

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Tarsal formula (TF): summary of the number of tarsomeres occurring on the legs, reported in the following format: I:II:III:IV, in which intraspecific variation for a leg is denoted by a range (i.e., the TF for Vononula singularis Roewer is 5:9–10:7:8). Tarsomeres: the subdivisions or segments of the tarsus.

FIGURE 1. General morphology of the pedipalp of a cosmetid harvestman, SEM. A, Right pedipalp of Eupoecilaema magnum; B, Right pedipalp of Cynorta marginalis. Scale bars = 1 mm. c = tarsal claw, f = femur, p = patella, ta = tarsus, ti = tibia.

FIGURE 2. Armature on abdominal scutum, lateral perspective. A, Unarmed (Eucynortella sexpunctata); B, Paired spiniform tubercles on scutal area III (Eucynorta albipustulata); C, Paired granular tubercles on scutal areas I–II, paired spiniform tubercles on area III (Reimoserius albipictus); D, Paired granular tubercles on scutal areas I and II and paired spiniform tubercles on area IV (Paracynorta confluens). Arrows indicate tubercles.

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FIGURE 3. Dorsal patterns. A, V-pattern on scutal groove (sg) with complete longitudinal median line on dosum (Paecilaema sp.n. 1 from Panama); B, V-pattern on scutal groove with broken median line and transverse line (tl) on grooves between scutal areas III and IV (Eucynorta sp.n. 5); C, Reticulate pattern (rp) on margins of carapace (Meterginus sp.n. 2). Arrows indicate median line on dorsum. as = abdominal scutum, c = carapace.

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FIGURE 4. Coloration. A, Reticulate pattern on margins of carapace (c) and abdominal scutum (as) (Cynorta marginalis); B, Dorsal pattern formed by spots (Paecilaema chiriquiense); C, Borders of scutal areas I-IV outlined in white (Paracynorta confluens); D, Black patches (bp) on abdominal scutum (Cynortula cingulata); E, Free tergites (ft) and anal operculum (ao) with spots (Flirtea lateralis); F, Annulate legs (Cynorta annulata); G, White rings encircling of tubercles on scutal areas I and III (Cynortellana oculata); H, Fine lines on margins of abdominal scutum (Eucynorta sp.n. 3). i = scutal area I, ii = scutal area II, iii = scutal area III, iv = scutal area IV, f = femur, arrow indicates the coxa, as = abdominal scutum, c = carapace.

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FIGURE 5. Sexually dimorphic characters. A, Lateral (ectal) view of femur (f) of male with large spiniform tubercle (t) and smaller granular tubercle (Cynorta dentipes); B, Dorsal view of patella (p) and tibia (ti) IV of male with prolateral and retrolateral rows of tubercles (Acromares vittatum); C, Ventral view of femur of male with two rows of tubercles (Eucynorta tenuipes); D, Lateral view of metatarsus (m) with row of tubercles (Cynortula sp.n.); E, Tarsus I of male with enlarged basitarsal segments (bt) (Kevonones irazus); F, Tarsus I of female with basitarsal (bt) and distitarsal (dt) of similar size (Cynorta marginalis); G, Female with cheliceral segments (ch) not enlarged (Eugnidia clavifemur); H, Male with enlarged second cheliceral segment (Eugnidia clavifemur).

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FIGURE 6. Undescribed species. A, Cynorta sp.n. 1 (Costa Rica; INBio); B, Cynorta sp.n. 2 (Costa Rica, Limon; INBio); C, Cynorta sp.n. 3 (Costa Rica, Limon; INBio); D, Cynortellana sp.n. (Costa Rica; INBio); E, Cynortula sp.n. (Costa Rica, Parque Nacional Corcouado; INBio 49518); F, Erginoides sp.n. (Costa Rica, Volcan Poas; MIUP).

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FIGURE 7. Undescribed species and unidentified genera. A, Flirtea sp.n. (Costa Rica, Limon; INBio); B, Paecilaema sp.n. 1. (Panama, El Cope; AMNH); C, Paecilaema sp.n. 2 (Panama, El Cope; AMNH); D, Paecilaema sp.n. 3 (Panama, El Cope; AMNH); E, Meterginus sp.n. 1 (Panama, Parque Nacional Soberania; AMNH); F, Paecilaema sp.n. 4 (Costa Rica, La Selva; AMNH); G, Unidentified g.sp.n. 1 (Costa Rica, Guanacaste; INBio 47154). H. Unidentified g.sp.n. 2 (Guatemala, Biotopo del Quetzal Baja Verapaz; INBio).