M. Alma Solis

Integration of DNA barcoding into an ongoing inventory of complex tropical biodiversity

Inventory of the caterpillars, their food plants and parasitoids began in 1978 for todays Area de Conservacion Guanacaste (ACG), in northwestern Costa Rica. This complex mosaic of 120 000 ha of conserved and regenerating dry, cloud and rain forest over 0–2000 m elevation contains at least 10 000 species of non‐leaf‐mining caterpillars used by more than 5000 species of parasitoids. Several hundred thousand specimens of ACG‐reared adult Lepidoptera and parasitoids have been intensively and extensively studied morphologically by many taxonomists, including most of the co‐authors. DNA barcoding — the use of a standardized short mitochondrial DNA sequence to identify specimens and flush out undisclosed species — was added to the taxonomic identification process in 2003. Barcoding has been found to be extremely accurate during the identification of about 100 000 specimens of about 3500 morphologically defined species of adult moths, butterflies, tachinid flies, and parasitoid wasps. Less than 1% of the species have such similar barcodes that a molecularly based taxonomic identification is impossible. No specimen with a full barcode was misidentified when its barcode was compared with the barcode library. Also as expected from early trials, barcoding a series from all morphologically defined species, and correlating the morphological, ecological and barcode traits, has revealed many hundreds of overlooked presumptive species. Many but not all of these cryptic species can now be distinguished by subtle morphological and/or ecological traits previously ascribed to ‘variation’ or thought to be insignificant for species‐level recognition. Adding DNA barcoding to the inventory has substantially improved the quality and depth of the inventory, and greatly multiplied the number of situations requiring further taxonomic work for resolution.

Review of Apanteles sensu stricto (Hymenoptera, Braconidae, Microgastrinae) from Area de Conservación Guanacaste, northwestern Costa Rica, with keys to all described species from Mesoamerica.

Abstract More than half a million specimens of wild-caught Lepidoptera caterpillars have been reared for their parasitoids, identified, and DNA barcoded over a period of 34 years (and ongoing) from Area de Conservación de Guanacaste (ACG), northwestern Costa Rica. This provides the world’s best location-based dataset for studying the taxonomy and host relationships of caterpillar parasitoids. Among Hymenoptera, Microgastrinae (Braconidae) is the most diverse and commonly encountered parasitoid subfamily, with many hundreds of species delineated to date, almost all undescribed. Here, we reassess the limits of the genus Apanteles sensu stricto, describe 186 new species from 3,200+ parasitized caterpillars of hundreds of ACG Lepidoptera species, and provide keys to all 205 described Apanteles from Mesoamerica – including 19 previously described species in addition to the new species. The Mesoamerican Apanteles are assigned to 32 species-groups, all but two of which are newly defined. Taxonomic keys are presented in two formats: traditional dichotomous print versions and links to electronic interactive versions (software Lucid 3.5). Numerous illustrations, computer-generated descriptions, distributional information, wasp biology, and DNA barcodes (where available) are presented for every species. All morphological terms are detailed and linked to the Hymenoptera Anatomy Ontology website. DNA barcodes (a standard fragment of the cytochrome c oxidase I (COI) mitochondrial gene), information on wasp biology (host records, solitary/gregariousness of wasp larvae), ratios of morphological features, and wasp microecological distributions were used to help clarify boundaries between morphologically cryptic species within species-complexes. Because of the high accuracy of host identification for about 80% of the wasp species studied, it was possible to analyze host relationships at a regional level. The ACG species of Apanteles attack mainly species of Hesperiidae, Elachistidae and Crambidae (Lepidoptera). About 90% of the wasp species with known host records seem to be monophagous or oligophagous at some level, parasitizing just one host family and commonly, just one species of caterpillar. Only 15 species (9%) parasitize species in more than one family, and some of these cases are likely to be found to be species complexes. We have used several information sources and techniques (traditional taxonomy, molecular, software-based, biology, and geography) to accelerate the process of finding and describing these new species in a hyperdiverse group such as Apanteles. The following new taxonomic and nomenclatural acts are proposed. Four species previously considered to be Apanteles are transferred to other microgastrine genera: Dolichogenidea hedyleptae (Muesebeck, 1958), comb. n., Dolichogenidea politiventris (Muesebeck, 1958), comb. n., Rhygoplitis sanctivincenti (Ashmead, 1900), comb. n., and Illidops scutellaris (Muesebeck, 1921), comb. rev. One European species that is a secondary homonym to a Mesoamerican species is removed from Apanteles and transferred to another genus: Iconella albinervis (Tobias, 1964), stat. rev. The name Apanteles albinervican Shenefelt, 1972, is an invalid replacement name for Apanteles albinervis (Cameron, 1904), stat. rev., and thus the later name is reinstated as valid. The following 186 species, all in Apanteles and all authored by Fernández-Triana, are described as species nova: adelinamoralesae, adrianachavarriae, adrianaguilarae, adrianguadamuzi, aichagirardae, aidalopezae, albanjimenezi, alejandromasisi, alejandromorai, minorcarmonai, alvarougaldei, federicomatarritai, anabellecordobae, rostermoragai, anamarencoae, anamartinesae, anapiedrae, anariasae, andreacalvoae, angelsolisi, arielopezi, bernardoespinozai, bernyapui, bettymarchenae, bienvenidachavarriae, calixtomoragai, carloscastilloi, carlosguadamuzi, eliethcantillanoae, carlosrodriguezi, carlosviquezi, carloszunigai, carolinacanoae, christianzunigai, cinthiabarrantesae, ciriloumanai, cristianalemani, cynthiacorderoae, deifiliadavilae, dickyui, didiguadamuzi, diegoalpizari, diegotorresi, diniamartinezae, duniagarciae, duvalierbricenoi, edgarjimenezi, edithlopezae, eduardoramirezi, edwinapui, eldarayae, erickduartei, esthercentenoae, eugeniaphilipsae, eulogiosequeira, felipechavarriai, felixcarmonai, fernandochavarriai, flormoralesae, franciscopizarroi, franciscoramirezi, freddyquesadai, freddysalazari, gabrielagutierrezae, garygibsoni, gerardobandoi, gerardosandovali, gladysrojasae, glenriverai, gloriasihezarae, guadaluperodriguezae, guillermopereirai, juanmatai, harryramirezi, hectorsolisi, humbertolopezi, inesolisae, irenecarrilloae, isaacbermudezi, isidrochaconi, isidrovillegasi, ivonnetranae, jairomoyai, javiercontrerasi, javierobandoi, javiersihezari, jesusbrenesi, jesusugaldei, jimmychevezi, johanvargasi, jorgecortesi, jorgehernandezi, josecalvoi, josecortesi, josediazi, josejaramilloi, josemonteroi, joseperezi, joserasi, juanapui, juancarrilloi, juangazoi, juanhernandezi, juanlopezi, juanvictori, juliodiazi, juniorlopezi, keineraragoni, laurahuberae, laurenmoralesae, leninguadamuzi, leonelgarayi, lilliammenae, lisabearssae, luciariosae, luisbrizuelai, luiscanalesi, luiscantillanoi, luisgarciai, luisgaritai, luishernandezi, luislopezi, luisvargasi, manuelarayai, manuelpereirai, manuelriosi, manuelzumbadoi, marcobustosi, marcogonzalezi, marcovenicioi, mariachavarriae mariaguevarae, marialuisariasae, mariamendezae, marianopereirai, mariatorrentesae, sigifredomarini, marisolarroyoae, marisolnavarroae, marvinmendozai, mauriciogurdiani, milenagutierrezae, monicachavarriae, oscarchavesi, osvaldoespinozai, pablotranai, pabloumanai, pablovasquezi, paulaixcamparijae, luzmariaromeroae, petronariosae, randallgarciai, randallmartinezi, raulacevedoi, raulsolorsanoi, wadyobandoi, ricardocaleroi, robertmontanoi, robertoespinozai, robertovargasi, rodrigogamezi, rogerblancoi, rolandoramosi, rolandovegai, ronaldcastroi, ronaldgutierrezi, ronaldmurilloi, ronaldnavarroi, ronaldquirosi, ronaldzunigai, rosibelelizondoae, ruthfrancoae, sergiocascantei, sergioriosi, tiboshartae, vannesabrenesae, minornavarroi, victorbarrantesi, waldymedinai, wilbertharayai, williamcamposi, yeissonchavesi, yilbertalvaradoi, yolandarojasae, hazelcambroneroae, zeneidabolanosae.

A molecular phylogeny for the pyraloid moths (Lepidoptera: Pyraloidea) and its implications for higher‐level classification

Pyraloidea, one of the largest superfamilies of Lepidoptera, comprise more than 15 684 described species worldwide, including important pests, biological control agents and experimental models. Understanding of pyraloid phylogeny, the basis for a predictive classification, is currently provisional. We present the most detailed molecular estimate of relationships to date across the subfamilies of Pyraloidea, and assess its concordance with previous morphology‐based hypotheses. We sequenced up to five nuclear genes, totalling 6633 bp, in each of 42 pyraloids spanning both families and 18 of the 21 subfamilies, plus up to 14 additional genes, for a total of 14 826 bp, in 21 of those pyraloids plus all 24 outgroups. Maximum likelihood analyses yield trees that, within Pyraloidea, differ little among datasets and character treatments and are strongly supported at all levels of divergence (83% of nodes with bootstrap ≥80%). Subfamily relationships within Pyralidae, all very strongly supported (>90% bootstrap), differ only slightly from a previous morphological analysis, and can be summarized as Galleriinae + Chrysauginae (Phycitinae (Pyralinae + Epipaschiinae)). The main remaining uncertainty involves Chrysauginae, of which the poorly studied Australian genera may constitute the basal elements of Galleriinae + Chrysauginae or even of Pyralidae. In Crambidae the molecular phylogeny is also strongly supported, but conflicts with most previous hypotheses. Among the newly proposed groupings are a ‘wet‐habitat clade’ comprising Acentropinae + Schoenobiinae + Midilinae, and a provisional ‘mustard oil clade’ containing Glaphyriinae, Evergestinae and Noordinae, in which the majority of described larvae feed on Brassicales. Within this clade a previous synonymy of Dichogaminae with the Glaphyriinae is supported. Evergestinae syn. n. and Noordinae syn. n. are here newly synonymized with Glaphyriinae, which appear to be paraphyletic with respect to both. Pyraustinae and Spilomelinae as sampled here are each monophyletic but form a sister group pair. Wurthiinae n. syn., comprising the single genus Niphopyralis Hampson, which lives in ant nests, are closely related to, apparently subordinate within, and here newly synonymized with, Spilomelinae syn. n.

DNA barcoding and morphology reveal three cryptic species of Anania (Lepidoptera: Crambidae: Pyraustinae) in North America, all distinct from their European counterpart

Anania coronata (Hufnagel), a Holarctic species of pyraustine crambid moth, has long been treated as having two geographically separated subspecies – the nominotypical Anania coronata in the Palaearctic Region and Anania coronata tertialis (Guenée) in the Nearctic Region. Maximum likelihood and Bayesian inference analysis of mitochondrial DNA barcodes both recover four well‐supported, reciprocally monophyletic groups within Anania coronata. Qualitative and quantitative analyses of genital structures reveal diagnostic differences that correspond to the four barcode lineages. On the basis of both molecular and morphological evidence, we conclude that Anania coronata is actually a complex of four species. Anania coronata (Hufnagel) is restricted to Europe, whereas three species occur in North America: Anania tertialis (Guenée), Anania plectilis (Grote & Robinson) and Anania tennesseensissp.n. Yang.

Austromusotima, a New Musotimine Genus (Lepidoptera: Crambidae) Feeding on Old World Climbing Fern, Lygodium microphyllum (Schizaeaceae)

Abstract During the search for natural enemies of Old World climbing fern, Lygodium microphyllum (Cav.) R. Br. (Schizaeaceae), in Australia and southeastern Asia, Cataclysta camptozonale (Hampson) was found to be highly specific to this aggressive vine and was tested as a biological control agent. This musotimine moth species has long been misplaced in a European acentropine genus; therefore, we propose Austromusotima, new genus, to accommodate Austromusotima camptozonale, new combination, as the type species. The syntype series of Oligostima camptozonale is a mixture of specimens of the former species (sensu stricto) and its sibling, Austromusotima metastictalis (Hampson), new combination. A lectotype is designated for A. camptozonale to stabilize the use of the name. The immature stages of A. camptozonale are described and compared with other known musotimine immatures. The immatures of Eugauria albidenta (Hampson) and Cataclysta angulata Moore are illustrated for the first time. Austromusotima is most closely related to Cataclysta seriopunctalis Hampson based on adult morphological characters, but immatures of C. seriopunctalis are unknown, and therefore, this species is not included in Austromusotima. The important, yet incongruent, results between immature and adult characters are discussed in the context of phylogenetic relationships of Austromusotima to other taxa.

Nomenclatural benchmarking: the roles of digital typification and telemicroscopy.

Abstract Nomenclatural benchmarking is the periodic realignment of species names with species theories and is necessary for the accurate and uniform use of Linnaean binominals in the face of changing species limits. Gaining access to types, often for little more than a cursory examination by an expert, is a major bottleneck in the advance and availability of biodiversity informatics. For the nearly two million described species it has been estimated that five to six million name-bearing type specimens exist, including those for synonymized binominals. Recognizing that examination of types in person will remain necessary in special cases, we propose a four-part strategy for opening access to types that relies heavily on digitization and that would eliminate much of the bottleneck: (1) modify codes of nomenclature to create registries of nomenclatural acts, such as the proposed ZooBank, that include a requirement for digital representations (e-types) for all newly described species to avoid adding to backlog; (2) an “r” strategy that would engineer and deploy a network of automated instruments capable of rapidly creating 3-D images of type specimens not requiring participation of taxon experts; (3) a “K” strategy using remotely operable microscopes to engage taxon experts in targeting and annotating informative characters of types to supplement and extend information content of rapidly acquired e-types, a process that can be done on an as-needed basis as in the normal course of revisionary taxonomy; and (4) creation of a global e-type archive associated with the commissions on nomenclature and species registries providing one-stop-shopping for e-types. We describe a first generation implementation of the “K” strategy that adapts current technology to create a network of Remotely Operable Benchmarkers Of Types (ROBOT) specifically engineered to handle the largest backlog of types, pinned insect specimens. The three initial instruments will be in the Smithsonian Institution(Washington, DC), Natural History Museum (London), and Museum National d’Histoire Naturelle (Paris), networking the three largest insect collections in the world with entomologists worldwide. These three instruments make possible remote examination, manipulation, and photography of types for more than 600,000 species. This is a cybertaxonomy demonstration project that we anticipate will lead to similar instruments for a wide range of museum specimens and objects as well as revolutionary changes in collaborative taxonomy and formal and public taxonomic education.

First record of Duponchelia fovealis (Lepidoptera: Crambidae) in South America

espanolEl primer reporte de Duponchelia fovealis Zeller (Lepidoptera:Crambidae) fue por danos a la fresa (Fragaria x ananassa) en America del Sur en el Estado del Parana, Brasil. Se encontraron tres enemigos naturales para controlar D. fovealis identificados como Apanteles sp. (Hymenoptera: Braconidae), Hyaliodocoris insignis (Heteroptera: Miridae) y el hongo entomopatogenico Beauveria bassiana. EnglishThe European pepper moth Duponcheliafovealis Zeller (Lepidoptera: Crambidae) is reported for the first time in South America, in the State of Parana, Brazil. D.fovealis causes damage to strawberries and weakens the plants. Three natural enemies controlling D.fovealis were found and identified as Apanteles sp. (Hymenoptera: Braconidae), Hyaliodocoris insignis (Heteroptera: Miridae) and the entomopathogenic fungus Beauveria bassiana.

A New Cryptic Species of Diatraea (Lepidoptera: Crambidae: Crambinae) Feeding on Eastern Gama Grass and a Novel Host Association with a Braconid (Hymenoptera) in the United States

ABSTRACT A new species, Diatraea mitteri Solis, that had been residing cryptically as Diatraea crambidoides (Grote), feeding on eastern gama grass (Tripsacum dactyloides (L.) L., is described. D. crambidoides occurs in the southern United States and Mexico and is an economic pest of corn (Zea mays L.). It has been reported to also feed on sorghum (Sorghum bicolor (L.) Moench), johnsongrass (Sorghum halepense (L.) Persoon), and sugar cane (Saccharum officinarum L.). We confirm that D. crambidoides also feeds on eastern gama grass. Morphological and molecular characters support the status of D. mitteri as a new species. Parsimony analysis resulted in two clades corresponding to D. crambidoides and D. mitteri. We confirm the distribution of D. mitteri from Kansas, Oklahoma, and Texas, but its distribution could be as broad as the remaining range of eastern gama grass in the eastern United States. All the life stages are described and illustrated. A novel host association, Alabagrus imitatus Cresson (Hymenoptera: Braconidae), as a parasitoid of D. mitteri is reported.

Checklist and key of New World species of Omiodes Guenée with descriptions of four new Costa Rican species (Lepidoptera: Crambidae).

Omiodes Guenee is redescribed based on all New World species, including the type species O. humeralis Guenee. Four new species from Costa Rica, O. janzeni sp. n., O. hallwachsae sp. n., O. sirena sp. n., O. ochracea sp. n., are described. Ten new synonymies are established : Phostria disciiridescens Hampson is =O. croeceiceps (Walker), Phostria cayennalis Schaus is =O. grandis (Druce), Omiodes ochrosoma Felder & Rogenhofer and Phryganodes gazalis Schaus are =O. pandaralis (Walker), Nacoleia lenticurvalis Hampson, Phryganodes anchoritalis Dyar, and Phostria duplicata Kaye are =O. confusalis (Dognin), O. cervinalis Amsel is =O. martvralis (Lederer), Nacoleia indicata ab. pigralis Dognin and Botis fortificalis Moschler are =O. metricalis (Moschler). One new combination is recognized: O. pandaralis (Walker) was transferred from Coelorhynchidia Hampson. A key and an updated checklist to the neotropical Omiodes species is provided, including O. indicata (Fabricius), a worldwide pest. Ten species that do not belong in Omiodes are retained until appropriate generic placements are identified.

Michaelshaffera gen. n. - a pyraloid taxon lacking an abdominal tympanal organ (Lepidoptera: Pyralidae)

Michaelshaffera gen. n. is comprised of two species, M. maidoa (Schaus), new combination, the type species, described from French Guiana, and a new species, M. beckeri, here described from South America. The assignment of taxa to the Pyraloidea is based primarily on characters of the tympanal organs and immature stages. Michaelshaffera lacks a tympanal organ and the immatures are unknown. The rationale for the placement of this genus in the Pyraloidea and lower hierarchical ranks is discussed based on other morphological characters.