Seven new species of Spathidexia Townsend (Diptera: Tachinidae) reared from caterpillars in Area de Conservación Guanacaste, Costa Rica

AJ Fleming; D Monty Wood; Daniel Janzen; Winnie Hallwachs; M Alex Smith

doi:10.3897/BDJ.3.e4597

. 2015 Mar 25;(3):e4597. doi: 10.3897/BDJ.3.e4597

Seven new species of Spathidexia Townsend (Diptera: Tachinidae) reared from caterpillars in Area de Conservación Guanacaste, Costa Rica

AJ Fleming ^‡,^✉, D Monty Wood ^‡, Daniel Janzen ^§, Winnie Hallwachs ^§, M Alex Smith ^|

PMCID: PMC4385903 PMID: 25859130

Abstract Abstract

We describe seven new species of Spathidexia (Diptera: Tachinidae) reared from Area de Conservación Guanacaste (ACG), northwestern Costa Rica. All were reared from various species of ACG caterpillars during an ongoing inventory of caterpillars, their food plants and their parasitoids. By coupling morphology, photographic documentation, life history and molecular data, we provide a clear and concise description of each species. All are known to be previously undescribed as a result of a comprehensive study of the genus by DMW. Spathidexia atripalpus sp. n., Spathidexia juanvialesi sp. n., Spathidexia marioburgosi sp. n., Spathidexia luisrobertogallegosi sp. n., Spathidexia luteola sp. n., Spathidexia hernanrodriguezi sp. n. and Spathidexia aurantiaca sp. n. are all authored and described by Fleming and Wood. Minthodexiopsis Townsend is proposed by Wood as a new synonym of Spathidexia. A new combination proposed by Wood as a result of the new synonymy is S. flavicornis (Brauer & Bergenstamm) comb. n.

Keywords: Spathidexia , Diptera , Tachinidae , tropical rain forest, tropical dry forest, parasitoid fly, host-specificity, caterpillars

Introduction

The tachinid genus Spathidexia Townsend 1912 is a small New World genus in the tribe Thelairini of the Dexiinae (Diptera, Tachinidae) (O’Hara and Wood 2004). Thelairini is classified as a small cosmopolitan tribe characterized by: an abdominal mid-dorsal depression that does not reach the hind margin of Tergite1+2, bare eyes, plumose antennae, and bearing 3 pairs of marginal scutellars of which the apicals are often crossed (Crosskey 1984, Mesnil 1939). The tribe Thelairini is known to occur from Hesperiidae, and Arctiidae (Arnaud 1978). The name Spathidexia is derived from the Latin term "spatha", in reference to the females' blade-like ovipositor. Males and females within this genus are sometimes strongly dimorphic with only the females possessing proclinate orbital bristles, or distinctive abdominal coloration and pattern. A complete description of the generic characters was given by Arnaud (1960) (we provide a diagnosis and description of the genus based on this work). The genus Spathidexia was erected for a female specimen caught at Melrose Highlands, Mass., in 1908, collected by Mr. D.H. Clemons. The type species Spathidexia clemonsi Townsend was named after the original collector of the specimen. The genus remained monotypic until Reinhard 1934 added Spathidexia cerussata Reinhard and Spathidexia rasilis Reinhard. Arnaud (1960) built on this and raised the number of species to nine, in addition to providing a hint on its biology and extended the generic distribution well into the Neotropics. Today we know that Spathidexia contains 17 nominal species, ranging throughout much of the New World, although specimens are still somewhat rare in collections. Wood and Zumbado (2010) attributed seven species to Spathidexia living north of Mexico and 12 represented in the Neotropics, with only minimal known overlap between their distributions.

This work aims to build on the existing knowledge and describes seven new species of Spathidexia, all reared from caterpillars collected in ACG. In fact, all species of Spathidexia reared in ACG have been found to be undescribed species. These species are recognized based on differences in external morphology, and COI (coxI or cytochrome oxidase I) gene sequences (a.k.a. “DNA barcodes”). By coupling COI data with morphological descriptions we are able to show that abdominal markings are not only different between males and females but are also consistent within a species. As such, they are ideal tools for visual species differentiation.

The treatments reported here is focused on placing names on the species reared from ACG, thereby preparing them for later detailed ecological and behavioral accounts and studies that will normally extend across ACG ecological groups, whole ecosystems, and taxonomic assemblages much larger than a genus. However, all ACG Spathidexia reared to date in ACG are parasitoids of monocot-eating caterpillars in the Nymphalidae (Satyrinae) or Hesperiidae (Hesperiinae).

Materials and methods

Acronyms for depositories

BMNH The Natural History Museum, London, United Kingdom

CNC Canadian National Collection of Insects, Arachnids and Nematodes, Ottawa, Canada

USNM National Museum of Natural History, Washington, D.C., USA

INBio Instituto Nacional de Biodiversidad, Santo Domingo de Heredia, Costa Rica

NHMW Naturhistorisches Museum, Wien, Austria

MZUT Musei di Zoologia, Università di Torino, Torino, Italia

CAS California Academy of Sciences, San Francisco, CA, USA

Geographic area of the study and rearing intensity

All flies and rearing information described here were found by the 35+ year-old ongoing inventory of the caterpillars, their food plants and their parasitoids of the dry forest, rain forest, cloud forest, and intergrades, in the 125,000+ ha terrestrial portion of Area de Conservación Guanacaste (ACG) in northwestern Costa Rica (Fleming et al. 2014a, Fleming et al. 2014b,Fernandez-Triana et al. 2014, Janzen and Hallwachs 2011, Janzen et al. 2009, Janzen et al. 2011, Rodriguez et al. 2012, Smith et al. 2012, Smith et al. 2006, Smith et al. 2007, Smith et al. 2008). The tachinid rearing methods are described at http://janzen.bio.upenn.edu/caterpillars/methodology/how/parasitoid_husbandry.htm. The data collected through this initiative contains copious information on parasitoid biology and associated hosts. Among the fly parasitoids encountered, the most species-rich, represented by hundreds of species is the family Tachinidae.

In brief, caterpillars at all instars (and sometimes pupae) are found in the wild by a wide variety of search methods, and reared in captivity on the food plant species on which they were found, until they produce an adult, a parasitoid, or die of other causes. Each caterpillar is documented as an individual, as are the adult parasitic flies.

This inventory has reared about 600,000 wild-caught caterpillars since 1978. All frequencies of parasitism reported here need to be considered against this background inventory. Equally, it is patently obvious that the inventory searches some kinds of vegetation and height off the ground much more thoroughly than others, and it also searches throughout the year. Comparison of reared species of parasitoids with those collected by net or Malaise traps demonstrates that, to date, the caterpillar inventory has encountered well less than half the species of caterpillar parasitoids present in ACG. The largest unsampled void is the upper foliage of the canopy above about 3–4 m above the ground.

Imaging and dissections

Our descriptions of new species are deliberately brief and only include some differentiating descriptions of body parts and colors that are commonly used in tachinid identification. These brief descriptions are complemented with an extensive series of color photos of every species to illustrate the readily-observed differences among these species.

Habitus photographs were taken using a Canon T3i digital SLR, using a 65mm Macro Photo Lens 1:2.8 (MP–E 65mm), mounted on a microscope track stand (AmScope, Model: TS200) modified to accept a Manfrotto QR 200PL–14 quick release plate. Images were shot in aperture priority, allowing the camera to control shutter speed at f/4.5. Stacks of 40 images were taken at equal distance increments. Illumination was provided with a homemade reflective dome (instruction for dome creation can be found at: http://www.cdfa.ca.gov/plant/ppd/entomology/Dome/kd–200.html) placed over a 144 LED ringlight (AmScope, Model: LED–144–YK).

The photographic series were processed using Photoshop CS6, and digitally stacked with Zerene Stacker Software v1.04. This produced a final composite image maximizing image quality and depth of field.

The terminology used for components of the terminalia (which refers here only to the sclerotized parts of the genitalia, and not to the soft internal structures) and other body parts, follows Cumming and Wood (2009).

All specimens listed as examined are considered paratypes, except for the holotype which is noted separately.

Wherever a specimen label has been cited, the information is presented using the following symbols: /, indicates the end of a line; //, indicates the end of a label. Labels are presented from top (closest to the specimen) to bottom, with any comments about the label being given in square brackets.

Voucher specimen management

All caterpillars reared from the ACG efforts receive a unique voucher code in the format of yy–SRNP–xxxxx. Any parasitoid emerging from this caterpillar receives the same voucher code, and then if/when later the parasitoid is dealt with individually, it receives a second voucher code unique to it, in the format of DHJPARxxxxxxx. The voucher codes and collateral data assigned to both host and emergent parasitoids are available at http://janzen.bio.upenn.edu/caterpillars/database.lasso. To date, all DHJPARxxxxxxx coded tachinids have had one leg removed for attempted DNA barcoding at the Biodiversity Institute of Ontario (BIO) at the University of Guelph, with all collateral data and all successful barcodes permanently and publically deposited in the Barcode of Life Data System (BOLD, www.boldsystems.org) (Ratnasingham and Hebert 2007), and later migrated to GenBank as well. A neighbor–joining (NJ) tree (Saitou and Nei 1987) for all Spathidexia reared and DNA barcoded by this inventory through 2013 is included as Supplemental Appendix 1. The inventory grows continually and new specimens can be found by searching the genus Spathidexia in BOLD. Each barcoded specimen also has an accession code, all information for the sequences associated with each individual specimen (including GenBank and BOLD accession) can be retrieved from the Barcode of Life Data System (BOLD) (Ratnasingham and Hebert 2007) via the publicly available dataset: dx.doi.org/10.5883/DS-ASSPATHI.

Inventoried Tachinidae were collected under Costa Rican government research permits issued to DHJ since 1978, and likewise exported under permit by DHJ from Costa Rica to Philadelphia, and then to the final depository in the Canadian National Insect collection in Ottawa, Canada. Tachinid identifications for the inventory were done by DHJ in coordination with a) visual inspection by AJF and DMW, b) DNA barcoding by BIO, MAS, and BOLD, and c) correlation with host caterpillar identifications by DHJ and WH through the inventory itself. Dates of capture of each reared fly in the inventory are the dates of eclosion of the fly, and not the date of capture of the caterpillar. This is because the fly eclosion date is much more representative of the time when that fly species is on the wing than is the time of capture of the caterpillar or (rarely) finding a parasitized pupa. However, the collector listed is the parataxonomist who found the caterpillar, rather than the person who retrieved the newly eclosed fly from its rearing bag or bottle, and processed it by freezing, pinning, labeling and oven–drying. Fly biology and degrees of parasitization by these flies will be the detailed subject of later papers.

DNA barcoding

DNA barcodes (standardised 5’ region of the mitochondrial cytochrome c oxidase I (COI) gene) for all ACG inventory specimens were obtained using DNA extracts prepared from single legs using a glass fibre protocol (Ivanova et al. 2006). Total genomic DNA was re-suspended in 30 μl of dH₂O, and a 658-bp region near the 5’ terminus of the COI gene was amplified using standard primers (LepF1–LepR1 (Hebert et al. 2004)) following established protocols (Smith et al. 2006, Smith et al. 2007, Smith et al. 2008).

Generic synonyms of Spathidexia

Spathidexia Townsend 1912: 110. Type species: Spathidexia clemonsi Townsend 1912, by original designation.

Gymnopalpus Townsend 1919b: 172. Type species: Gymnopalpus setipennis Townsend 1919b, by original designation. Synonymy by Wood 1987: 1265 & O’Hara and Wood 1998: 755.

Minthodexiopsis Townsend 1927: 221. Type species: Minthodexia flavicornis Brauer and Bergenstamm 1891, by original designation. Syn. nov.

Minthohoughia Townsend 1919a: 581. Type species: Minthohoughia cylindrica Townsend 1919a, by original designation. Synonymy by Guimarães 1971: 95.

Stenaulacodoria Townsend 1928: 161. Type species: Stenaulacodoria spatulata Townsend 1928, by original designation. Synonymy by Thompson 1963: 494.

Previously described species included in Spathidexia

antillensis Arnaud 1960: 6 (Spathidexia). Holotype male (USNM) [examined by DMW]. Type locality: Puerto Rico, Mayaguez.

brasiliensis Arnaud 1960: 10 (Spathidexia). Holotype male (CAS) [examined by DMW]. Type locality: Brazil, Santa Catarina, Nova Teutonia.

cerussata Reinhard 1934: 152 (Spathidexia). Holotype male (CNC) [examined by DMW]. Type locality: USA, Ohio, Amherst.

cinereicollis van der Wulp 1891: 255 (Thelairodes). Syntypes, 1 headless male, and 1 female (BMNH) [examined by DMW]. Type localities: Female: Mexico, Guerrero, Amula 6000 feet; Male: Sierra de las Aguas Escondidas 9500 feet. Combination established by Townsend 1915: 366, also mentioned as new combination in Guimarães 1971: 95.

clemonsi Townsend 1912: 110 (Spathidexia). Holotype female (USNM) [examined by DMW]. Type locality: USA, Massachusetts, Melrose Highlands.

creolensis Reinhard 1955: 131 (Spathidexia). Holotype female (USNM) [examined by DMW]. Type locality: USA, Florida, Miami.

cylindrica Townsend 1919a: 581 (Minthohoughia). Holotype female (USNM) [examined by DMW]. Type locality: Peru, Lima. Combination established by Guimarães 1971: 95.

dicta Giglio-Tos 1893: 5 (Plagia). Holotype male, published as female (MZUT) [examined by DMW]. Type locality: Mexico.

dunningii Coquillett 1895: 54 (Thryptocera). Lectotype female by fixation of Coquillett 1897: 60 (statement “From the type specimen” is regarded as a lectotype fixation); also by designation of Arnaud 1960: 22. (USNM) [examined by DMW]. Type locality: USA, Illinois, Algonquin. Combination established by Townsend 1915: 366.

rasilis Reinhard 1934: 153 (Spathidexia). Holotype female (CNC) [examined by DMW]. Type locality: USA, Wisconsin, Madison. Synonymy with dunningii established by Arnaud 1960: 5, 18.

elegans Reinhard 1964: 37 (Minthodexiopsis). Holotype male (CNC) [examined by DMW]. Type locality: USA, Texas, Cameron Co.

flavicornis Brauer and Bergenstamm 1891: 376 (Minthodexia). Holotype female (NHMW) [not examined]. Type locality: Venezuela. N. comb. *

nexa Reinhard 1953: 94 (Spathidexia). Holotype female (CNC) [examined by DMW]. Type locality: Mexico, Distrito Federal, Ciudad de Mexico.

niveomarginata van der Wulp 1890: 200 (Anisia). Holotype female (BMNH) [examined by DMW]. Type locality: Mexico, Guerrero, Amula, 6000ft. Combination established by Guimarães 1971: 95.

pallida van der Wulp 1891: 255 (Thelairodes). Holotype female (BMNH) [examined by DMW]. Type locality: Mexico, Guerrero, Venta de Zopilote, 2800ft.

reinhardi Arnaud 1960: 26 (Spathidexia). Holotype male (USNM) [examined by DMW]. Type locality: USA, Texas, College Station.

setipennis Townsend 1919b: 172 (Gymnopalpus). Holotype female (USNM) [examined by DMW]. Type locality: Guatemala, Los Amates. Combination established by Wood 1987: 1265 & O’Hara and Wood 1998: 755.

spatulata Townsend 1928: 162 (Stenaulacodoria). Holotype female (USNM) [examined by DMW]. Type locality: Peru, Cañete. Combination by Thompson 1963: 494.

*The new combination is proposed by DMW and result from new generic synonymy and the examination of the type material of other nominal species. Type label information is included for those species.

Diagnosis of the genus Spathidexia

Arnaud 1960 provided a detailed description of the genus Spathidexia. The genus is characterized as follows: small to medium sized, with narrow parafacial, and bare to sparsely haired eyes, lower margin almost at level of vibrissa. Frons moderately wide in both sexes, with a pair of proclinate orbital bristles in both sexes in many species, some males with reclinate orbital bristles in line with frontal bristles. Frontal bristles reaching to middle of second antennal segment. The antennae descend to near the lower facial margin, with the third segment three times longer than the pedicel. First flagellomere in both sexes parallel sided. Parafacial bare or lightly haired along upper portion. Facial ridge strongly divergent, often posessing supravibrissal bristles along facial ridge. Usually with apical and subapical scutellars crossed at their tips, if subapicals not crossed then these are at least strongly convergent. Abdomen lacking discal bristles; female with flattened rectractile ovipositor which is either long and sharply pointed or short and blunt ended. Wing short and broad without unusual modification in tachinid veination. Vein R₁ may be bare or haired with vein R₄₊₅ haired up to at least crossvein r-m. It is different from its sister taxon Thelairodes by the presence of 3–4 meral bristles, with Thelairodes possessing 5 or more.

Taxon treatments

Spathidexia atripalpus

Fleming & Wood 2015 sp. n.

urn:lsid:zoobank.org:act:0D7D1AFF-015A-48E5-809E-EEA094A3319F

Materials

Type status: Holotype. Occurrence: occurrenceDetails: http://janzen.sas.upenn.edu; catalogNumber: DHJPAR0048611; recordedBy: D.H. Janzen & W. Hallwachs; individualID: DHJPAR0048611; individualCount: 1; sex: M; lifeStage: adult; preparations: pinned; otherCatalogNumbers: 12-SRNP-30227; Taxon: scientificName: Spathidexia atripalpus; phylum: Arthropoda; class: Insecta; order: Diptera; family: Tachinidae; genus: Spathidexia; specificEpithet: atripalpus; scientificNameAuthorship: Fleming & Wood, 2015; Location: continent: Central America; country: Costa Rica; countryCode: CR; stateProvince: Guanacaste; county: Area de Conservacion Guanacaste; locality: Sector Pitilla; verbatimLocality: Ingas; verbatimElevation: 580; verbatimLatitude: 11.00311; verbatimLongitude: -85.288; verbatimCoordinateSystem: Decimal; decimalLatitude: 11.00311; decimalLongitude: -85.288; Identification: identifiedBy: AJ Fleming; dateIdentified: 2014; Event: samplingProtocol: reared from caterpillar of Magneuptychia libye (Nymphalidae); verbatimEventDate: 19/Mar/12; Record Level: language: en; institutionCode: CNC; collectionCode: Insects; basisOfRecord: Pinned Specimen
Type status: Paratype. Occurrence: occurrenceDetails: http://janzen.sas.upenn.edu; catalogNumber: DHJPAR0018619; recordedBy: D.H. Janzen & W. Hallwachs; individualID: DHJPAR0018619; individualCount: 1; lifeStage: adult; preparations: pinned; otherCatalogNumbers: 99-SRNP-2997; Taxon: scientificName: Spathidexia atripalpus; phylum: Arthropoda; class: Insecta; order: Diptera; family: Tachinidae; genus: Spathidexia; specificEpithet: atripalpus; scientificNameAuthorship: Fleming & Wood, 2015; Location: continent: Central America; country: Costa Rica; countryCode: CR; stateProvince: Guanacaste; county: Area de Conservacion Guanacaste; locality: Sector El Hacha; verbatimLocality: Estacion Los Almendros; verbatimElevation: 290; verbatimLatitude: 11.03226; verbatimLongitude: -85.52776; verbatimCoordinateSystem: Decimal; decimalLatitude: 11.03226; decimalLongitude: -85.52776; Identification: identifiedBy: AJ Fleming; dateIdentified: 2014; Event: samplingProtocol: reared from caterpillar of Pierella pallida (Nymphalidae); verbatimEventDate: 24/Jul/99; Record Level: language: en; institutionCode: CNC; collectionCode: Insects; basisOfRecord: Pinned Specimen
Type status: Paratype. Occurrence: occurrenceDetails: http://janzen.sas.upenn.edu; catalogNumber: DHJPAR0048578; recordedBy: D.H. Janzen & W. Hallwachs; individualID: DHJPAR0048578; individualCount: 1; lifeStage: adult; preparations: pinned; otherCatalogNumbers: 12-SRNP-33263; Taxon: scientificName: Spathidexia atripalpus; phylum: Arthropoda; class: Insecta; order: Diptera; family: Tachinidae; genus: Spathidexia; specificEpithet: atripalpus; scientificNameAuthorship: Fleming & Wood, 2015; Location: continent: Central America; country: Costa Rica; countryCode: CR; stateProvince: Guanacaste; county: Area de Conservacion Guanacaste; locality: Sector Pitilla; verbatimLocality: Ingas; verbatimElevation: 580; verbatimLatitude: 11.00311; verbatimLongitude: -85.42041; verbatimCoordinateSystem: Decimal; decimalLatitude: 11.00311; decimalLongitude: -85.42041; Identification: identifiedBy: AJ Fleming; dateIdentified: 2014; Event: samplingProtocol: reared from caterpillar of Pareuptychia ocirrhoe (Nymphalidae); verbatimEventDate: 26/Jan/12; Record Level: language: en; institutionCode: CNC; collectionCode: Insects; basisOfRecord: Pinned Specimen

Description

Male (Fig. 1 a, b, c), head: Eye bare; frontal vitta dark black, narrowed apically to equal width of the ocellar triangle, face 3 times as wide as frontal vitta; frontal bristles arise no lower than level of pedicel; small black hairs lining the margin of the frontal vitta; antenna black; arista black and plumose, trichia at least 4 times as long as width of base of arista, tapering at apex of arista; proclinate orbital bristles absent; parafrontal entirely silver; parafacial silver; palpi black grey; short row of black supravibrissal hairs along facial margin. Thorax: greyish-gold when viewed dorsally with four longitudinal black vittae, these becoming fused post-suturally, appearing as two indistinct blotches covering more than 2/3rds of thorax; three post sutural dorsocentral bristles; scutellum bearing white or yellowish pruinosity over its entirety (occupying 1/2 or more of total area) darkened along its anterior edge; legs black with silvery sheen on anterior tibia. Wings: pale smoky greyish in color, vein R₄₊₅ setose from node up to r-m, R₁ bare. Abdomen: abdominal tergites dark shiny black, with bright gold bands covering 1/3^rd or more of the anterior margins of abdominal tergites T3 and T4, these bands wrapping around to the underside of the abdomen. When viewed laterally bright yellow blotches appear along tergites T1+2, T3 and the anterior margin of T4; T3, T4 and T5 possessing medial marginal bristles. Lateral marginal bristles on T1+2. Small black hairs visible over entire body, in particular visible extending from underside of T1+2.

Figure 1a. — *Spathidexia* *atripalpus* **sp. n.;** male DHJPAR0048611, female DHJPAR0048578

Figure 1b. — *Spathidexia* *atripalpus* **sp. n.;** male DHJPAR0048611, female DHJPAR0048578

Female (Fig. 1 d, e, f), head: Frontal vitta dark black, parallel sided apically equal to twice the width of the ocellar triangle, face 3 times as wide as frontal vitta; frontal bristles arise n o lower than level of pedicel; black hairs lining the margin of the frontal vitta; proclinate orbital bristles present; antenna black; arista black and plumose, trichia at least 4 times as long as width of base of arista, tapering at apex of arista; parafrontal entirely silver; parafacial silvery; palpi black, slightly haired along lower surface; short row of black supravibrissal hairs along facial margin. Thorax: greyish when viewed dorsally with four longitudinal black vittae, these becoming fused post-suturally, appearing as two indistinct blotches covering just more than 2/3 thorax postsuturally; three post sutural dorsocentral bristles; scutellum bearing white or yellowish pruinosity over its ½ of its entirety; legs black with silvery sheen on anterior femur. Wings: pale smoky greyish in color, vein R₄₊₅setose from node up to r-m, R₁ bare. Abdomen: abdominal tergites dark velvety black, bright grayish bands covering at up to 1/2 of tergal surface along anterior margin of T3 and T4; yellow abdominal band wrapping around the abdomen on the posterior margin of T1+2 visible only when viewed laterally; T3, T4 and T5 possessing medial marginal bristles. Lateral marginal bristles on T1+2. Small black hairs visible over entire body, not as hirsute as males but still present, in particular visible extending from anepimeron, and from underside of T1+2.

Diagnosis

The presence of black palpi is its strongest diagnostic character, differentiating it from almost all other species. This species differs from S. atypica, which also has black(ish) palpi, in having 3 postsutural dorsocentral bristles, bare eyes, and the presence of small black hairs covering entire body especially prominent extending from anepimeron and underside of T₁₊₂. Differs, from S. antillensis, which also bears two bold thoracic vittae but does not bear black palpi.

Etymology

From the Latin “ater”, color black, and the noun “palpus”, literally the palm of the hand, in reference to the black palpi present in both sexes of this species.

Distribution

Costa Rica, ACG, Prov. Guanacaste, rain forest and rain forest/dry forest ecotone, 290-580m elevation.

Ecology

Reared from four species of grass-eating rain forest satyrine Nymphalidae (4 records). One larva per host.