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Research Article
Description of a Neotropical gall inducer on Araceae: Arastichus, gen. nov. (Hymenoptera, Eulophidae) and two new species
expand article infoY. Miles Zhang‡, Michael W. Gates‡, Paul E. Hanson§, Sergio Jansen-González§|
‡ National Museum of Natural History, Smithsonian Institution, Washington, United States of America
§ Universidad de Costa Rica, San José, Costa Rica
| Universidad Nacional, Guanacaste, Costa Rica
¶ Avenida Bandeirantes, Ribeirao Preto, Brazil

Corresponding author: Y. Miles Zhang ( yuanmeng.zhang@gmail.com )

Corresponding author: Michael W. Gates ( michael.gates@usda.gov )

Academic editor: Petr Janšta
© 2022 Y. Miles Zhang, Michael W. Gates, Paul E. Hanson, Sergio Jansen-González.
This is an open access article distributed under the terms of the CC0 Public Domain Dedication.
Citation: Zhang YM, Gates MW, Hanson PE, Jansen-González S (2022) Description of a Neotropical gall inducer on Araceae: Arastichus, gen. nov. (Hymenoptera, Eulophidae) and two new species. Journal of Hymenoptera Research 92: 145-171. https://doi.org/10.3897/jhr.92.85967
ZooBank: urn:lsid:zoobank.org:pub:3E9AD341-8B60-47AF-A14B-F8F2D885174B
Open Access

Abstract

A new genus of a Neotropical gall inducing tetrastichine eulophid on Araceae is described and confirmed using Ultraconserved Elements (UCE) phylogenomic data. Arastichus Gates, Hanson, Jansen-González & Zhang, gen. nov., includes two new species and one species transferred from Aprostocetus Westwood: A. capipunctata Gates, Hanson, Jansen-González & Zhang, sp. nov., A. gallicola (Ferrière), comb. nov., and A. gibernau, Gates, Hanson, Jansen-González & Zhang, sp. nov.

Keywords

Chalcidoidea, Philodendron, Phytophagy, Tetrastichinae, Thaumatophyllum

Introduction

The Chalcidoidea is a large and diverse superfamily with broad biological diversity (Heraty et al. 2013), and with estimates of over 500,000 species (Noyes 2019) on Earth. Although primarily entomophagous, many phytophagous forms are known, among these the gall inducers that deform plant tissue in order to complete their development. The biology of gall inducers and the evolution of gall induction in Chalcidoidea have been reviewed recently (LaSalle 2005). Gall induction has evolved in seven different families of Chalcidoidea, with at least 16 independent origins both from entomophagous and phytophagous ancestors (LaSalle 2005; Böhmová et al. 2022). This includes the Eulophidae, the largest and most diverse chalcidoid family including over 4,300 species in 332 genera (Noyes 2019; Rasplus et al. 2020). The diversity of gall inducing eulophids is highest in the Australian Opheliminae and the cosmopolitan Tetrastichinae, the latter is a large and diverse subfamily with 15 genera recorded as phytophagous species (Kim et al. 2004, 2005; Mendel et al. 2004; LaSalle 2005; Kim and LaSalle 2008; Rasplus et al. 2011; Fisher et al. 2014). Overall, knowledge of the specific biology of gall associated tetrastichines is minimal but falls into three categories: parasitoid of gall inducer, inquiline, or gall inducer. LaSalle (2005) divides gall-associated tetrastichines into two groups: (1) the Australian inducers that gall Myrtaceae, and (2) mostly Neotropical groups that are often larger and more heavily sclerotized.

LaSalle (1994) records seven plant families serving as hosts for gall inducing Tetrastichinae: Araceae, Chenopodiaceae, Euphorbiaceae, Fabaceae, Myrtaceae, Myrsinaceae, and Solanaceae. Additionally, tetrastichines have also been recorded as gall inducers from Casuarinaceae (Fisher et al. 2014), Sapotaceae (Singh et al 2022), and Smilacaceae (Gates et al. 2020). In evaluating the gall-inducers associated with the Araceae (Alismatales) in general, focusing specifically on Hymenoptera, we note that very few taxa are known to be associated with this family, particularly as suspected phytophages (Table 1).

Table 1.
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Hymenoptera associated with Araceae.

Family (Subfamily) Species Plant Reference
Eulophidae (Tetrastichinae) Arastichus gallicola (Ferrière) Philodendron sp. Schott DeSantis 1979
P. undulatum Engler Ferrière 1924
P. tweedieanum Schott (as P. dubium (Chodat and Vischer)) This study
Thaumatophyllum bipinnatifidum (Schott ex Endl.) (as P. petraeum Chodat and Vischer)
T. solimoesense (A.C.Sm.) Sakur., Calazans & Mayo
Eulophidae (Tetrastichinae) Arastichus capipunctata sp. n. Philodendron radiatum (Schott) This study
Eulophidae (Tetrastichinae) Arastichus gibernau sp. n. Philodendron hederaceum var. oxycardium Schott This study
Eulophidae (Entedoninae) Ametallon deanthurium Hansson Anthurium cuspidatum Mast. Hansson 2004
Eurytomidae (Eurytominae) Prodecatoma philodendri Ferrière Philodendron sp. DeSantis 1979
Philodendron hederaceum (Jacq.) (as P. oxycardium (Schott)) DeSantis 1980
P. tweedieanum (as P. dubium) DeSantis and Fidalgo 1994 Ferrière 1924
Gibernau et al. (2002)
T. solimosoense (A. C. Sm.) (as P. solimosoense) Lotfalizadeh et al. 2007 Perioto and Lara 2019
Eurytomidae (Eurytominae) Aranedra millsi Burks Philodendron sp. Burks 1971
DeSantis 1979
Braconidae (Doryctinae) Monitoriella elongata Hedqvist P. radiatum Infante et al. 1995
Shimbori et al. 2011

Here we describe a new genus of Neotropical tetrastichines inducing galls on Thaumatophyllum and Philodendron (Araceae), Arastichus Gates, Hanson, Jansen-González & Zhang, gen. nov. (Fig. 1). We describe two new species: A. capipunctata Gates, Hanson, Jansen-González & Zhang, sp. nov., and A. gibernau, Gates, Hanson, Jansen-González & Zhang, sp. nov. Additionally, we transfer Trichaporus gallicola Ferrière to Arastichus, comb. nov., from its current placement in Aprostocetus Westwood, and provide a redescription along with designation of lectotype.

Figure 1. 

Illustration of the lifecycle of Arastichus gallicola with its host plant, Thaumatophyllum solimoesense (Arecaceae). Illustrated by Taina Litwak.

Materials and methods

Collection and identification

Mature infrutescences of Thaumatophyllum bipinnatifidum and Philodendron radiatum were cut from the plant in the laboratory, or mass reared in bags hung on clothesline. As the spathe was still closed in most of the infrutescences, careful incisions with a knife were used to expose the fruits beneath. A few fruits were dissected under a stereomicroscope to ensure they had galls with pupae or adults inside. The selected infrutescences were then put in individual organdy bags (40 cm × 30 cm) for wasp emergence. Emerging wasps were collected and stored in 70% EtOH.

Ethanol-preserved specimens were dehydrated through increasing concentrations of ethanol and transferred to hexamethyldisilazane (HMDS) (Heraty and Hawks 1998) before point-mounting. A Nikon SMZ1500 stereomicroscope with 10× oculars (Nikon C-W10X/22) and a Chiu Technical Corporation Lumina 1 FO-150 fiber optic light source were used for point-mounted specimen observation. Mylar film was placed over the ends of the light source to reduce glare from the specimen. Scanning electron microscope (SEM) images were taken with a Hitachi TM3000 (Tungsten source). Body parts of a disarticulated specimen were affixed to 0.1 mm minuten pins with Loctite Ultra Gel super glue. These were then adhered to a 12.7×3.2 mm Leica/Cambridge aluminum SEM stub by a carbon adhesive tab (Electron Microscopy Sciences, #77825-12). Stub-mounted specimens were sputter coated with gold-palladium using a Cressington Scientific 108 Auto from at least three different angles to ensure complete coverage (~20–30nm coating). One set of wings was removed and slide-mounted in polyvinyl alcohol prior to imaging; wings were photographed with a Olympus SC-100 digital camera attached to a Olympus BX43 light microscope and processed using analySIS getIT 5.2 (Olympus Soft Imaging Solutions). The habitus image was captured using an EntoVision Imaging Suite, which includes a firewire JVC KY-75 3CCD digital camera mounted on a Leica M16 zoom lens via a Leica z-step microscope stand. The program Cartograph 5.6.0 (Microvision Instruments, France) was used to merge an image series into a single in-focus, composite image. Lighting was achieved using techniques summarized in Buffington et al. (2005), Kerr et al. (2008), and Buffington and Gates (2008).When possible, male and female genitalia were extracted, cleared with KOH 10% and temporarily mounted in glycerin for imaging. Genitalia were photographed using the same setup as for wings (indicated above). These and SEM images were used for the elaboration of schemes of each genitalia using GIMP 2.8.10.

Morphological terminology follows Gibson (1997), while the surface sculpture follows Harris (1979). Several measurements were taken, including: body length, in lateral view from the anterior projection of the face to the tip of the metasoma; head width through an imaginary line connecting the farthest lateral projection of the eyes; head height through an imaginary line from the vertex to the clypeal margin bisecting both the median ocellus and the distance between the toruli; malar space, in lateral view between the ventral margin of the eye and lateral margin of the oral fossa; eye height in anterior view; vertex bristle in anterior view; mesoscutum and scutellum, in dorsal view through imaginary, median transverse and longitudinal lines; marginal vein, the length coincident with the leading fore wing edge to the base of the stigmal vein; stigmal vein, the length between its base on the marginal vein (M) and its apex; postmarginal vein (PMV), the length from the base of the stigmal vein (S) to its apex on the leading fore wing edge. Metasomal sclerites were measured dorsally along the midline. Abbreviations used: A1–n (anellus), F1–n (funicular segment), LOL (lateral ocellar line), OOL (ocellocular line), POL (posterior ocellar line), SMV (submarginal vein), A (anellus), C (clava), F (funicle), MPS (multiporous mlate sensilla), Gt1–n (gastral tergites), Gs1-n (gastral sternites). The antennal formula consists of: scape, pedicel, anelli, funiculars, clava.

Specimens are deposited in the following collections: ANIC (Australia National Insect Collection, Canberra, Australia), BMNH (The Natural History Museum, London, England), CNCI (Canadian National Collection, Ottawa, Canada), CNIN (National Collection of Insects – The National Autonomous University of Mexico, Mexico City, Mexico), MNHN (The National Museum of Natural History, Paris, France), MZUCR (Museum of Zoology – University of Costa Rica, San José, Costa Rica), MZUSP (Museum of Zoology – University of São Paulo, São Paulo, Brazil), USNM (National Museum of Natural History, Smithsonian Institution, Washington, D.C., USA).

Molecular analysis

One specimen each of A. gallicola and A. capipunctata were extracted, amplified, and sequenced at the Laboratories of Analytical Biology (LAB) at the Smithsonian Institution’s National Museum of Natural History (NMNH, Washington, DC, USA). A modified Ultraconserved Elements (UCE) protocol was used (Faircloth et al. 2012; Branstetter et al. 2017) along with the HymV2P probe set to enrich the UCE loci, (Branstetter et al. 2017). The library was sent to Admera Health (South Plainfield, NJ) and sequenced on an Illumina HiSeq 4000 (150-bp paired-end, Illumina Inc., San Diego, CA, USA). Additional eulophid UCE sequences were supplemented from Cruaud et al. (2019) and Rasplus et al. (2020).

PHYLUCE v1.7.0 (Faircloth, 2015) was used for UCE processing. SPAdes v3.14.0 (Bankevich et al. 2012) was used to align the contigs, sequences were aligned using MAFFT v7.490 (Katoh and Toh 2008), and trimmed using Gblocks v0.91b (Castresana 2000) with the following settings: b1 = 0.5, b2 = 0.5, b3 = 12, b4 = 7. A 50% complete matrix was used for downstream phylogenomic analysis. Additionally, fragments of legacy markers (COI, 28S, and CytB) were extracted from the UCE contigs using PHYLUCE. Trimmed reads for the newly generated sequences in this study are available from the National Center for Biotechnology Sequence Read Archive (SRA; BioProject ID PRJNA827143), and Sanger markers are available on GenBank (Suppl. material 1).

Phylogenomic analysis was conducted under the maximum likelihood (ML) criterion with IQ-TREE v2.1.1 (Minh et al. 2020), partitioning based on loci and with the best models of nucleotide substitution selected in ModelFinder with “-m MFP” (Kalyaanamoorthy et al. 2017). To assess nodal support, we performed a Shimodaira-Hasegawa approximate likelihood-rate test (SH-aLRT, Guindon et al. 2010) with 1000 replicates using the “-alrt” flag, and 1000 ultrafast bootstrap replicates (UFBoot2; Hoang et al. 2017) using “-bb”. Only nodes with support values of SH-aLRT ≥ 80 and UFBoot2 ≥ 95 were considered robust.

Results

The 50% UCE matrix consisted of 567 loci, with A. capipunctata and A. gallicola having 1715 and 1802 UCE loci recovered, respectively. The topology recovered was largely identical to that of Rasplus et al. (2020). The new genus Arastichus was recovered within the subfamily Tetrastichinae with strong support (Fig. 2). Arastichus is within the Aprostocetus group sensu Rasplus et al. (2020) , and the sister to Neohyperteles DeSantis with strong support (Fig. 2).

Figure 2. 

Maximum likelihood reconstruction of Eulophidae phylogeny inferred from 50% complete matrix of 567 Ultraconserved Elements (UCE) loci. Support values shown as SH-aLRT/UFBoot2. All nodes except for Tetrastichinae collapsed, with the two major genus groups (Aprostocetus group and Tetrastichus group) highlighted, and Arastichus in red.

Arastichus Gates, Hanson, Jansen-González & Zhang, gen. nov.

https://zoobank.org/6DB405D8-4660-4698-A9B6-1950816E86DF
Figs 3, 4–5, 6–7, 8–9, 10–15, 16–20, 21–25

Type species

Arastichus gallicola (Ferrière).

Diagnosis

Vertex with single erect seta mesad to eye margin, ~0.5× eye height (Fig. 10); vertex depressed posteriad and laterad lateral ocelli (Figs 12, 22); toruli positioned above middle of face, 1–1.5× torular diameters from median ocellus (Figs 10, 21, 24); intrascrobal carina step like in lateral view with V-like carinae diverging to lateral margins of median ocellus (Figs 12, 22); antennal formula 11242 (Fig. 14) or 11342 in A. capiculata. A1 ~1.5× wider at apex rather than base (note: often appears subdivided, representing fusion of two segments) wedge-like in lateral view, longest ventrally; ventral plaque present in male scape (Figs 5, 7, 9); clypeus bilobed, lobes apically truncate; gena ventrally extended beyond oral fossa/base of mandible (Figs 10, 21, 24); mesosoma shiny dorsally (Fig. 23); scutellum lacking submedian grooves (Figs 16, 23); petiole membranous ventrally; a tuft or sometimes one seta(e) anterad mesocoxa (Fig. 9); propodeal spiracles large, ~0.3× length propodeum; distinct, suberect setation on mesal surface of procoxa and metacoxa (Figs 8, 9), Gt6 with spiracular rim elevated (Fig. 19).

Arastichus gallicola was first described by Ferrière (1924) as Trichaporus gallicola, which was then transferred to Exurus Philippi by Costa Lima (1959a). LaSalle (1994) synonymized Exurus with Aprostocetus, through its type species E. colliguayae Philippi. He was hesitant about the status of A. gallicola (Fig. 3) as he was not able to examine any type specimens, but commented that it is quite distinct and warranted its own genus. As Ferrière did not designate a holotype, we hereby designate the top left specimen (female) on the pin with three other specimens as the lectotype (Fig. 3). The degree of morphological variation seen in Aprostocetus makes it difficult to characterize consistently using few characters; however, according to LaSalle (1994), most species have the SMV with ≥ 3 seta, propodeal spiracle partially covered by overhanging lobe of callus, and one cercal setae distinctly longest and sinuate or curved. Although Arastichus shares these diagnostics, several additional apomorphies set it apart from Aprostocetus (as noted in the diagnosis above).

Figure 3. 

Dorsal and lateral habitus of Arastichus gallicola lectotype (female on the top left), along with three paralectotypes on the same pin.

Description

Coloration : Female. Length 3.8–5.2 mm. Head, antennae, body, coxae, and legs yellow or brown (Figs 3–9). Tegula pale golden. Pronotum either completely brown, or yellow except for the anterolateral panel. Ventral mouthparts and tarsomeres pale yellow. Female fore wing with soft opaque area at basal and cubital folds, disc hyaline (Fig. 4). Male fore wing with opaque base of cubital and basal folds; disc with soft opaque pattern (Fig. 5).

Figure 4–5. 

Lateral habitus of Arastichus gallicola 4 female 5 male.

Head : Surface rugulose or umbilicately punctate dorsally, laterally, and anteriorly, 1.3–1.6× as broad as high. Supraclypeal area concave, glabrous, asetose (Figs 10, 21, 24), extending to toruli; lower tentorial pits minute. Genal carina present, extending to lower third of eye posteriorly (Figs 10, 13). Torulus with dorsal margin positioned at lower ocular line; intertorular space punctate, obtusely pointed; scrobal depression margined laterally, margin fading dorsally, reticulate with fine irregular rugae and with median carina between depressions in ventral half (Fig. 10). Eyes setose, seta sparsely distributed and very short. Mandible tridentate with apical and middle teeth acute, basal tooth broad and rounded (Fig. 21). Clypeus emarginate in step-like manner (Fig. 21), medially produced. Posterior surface of head without postgenal lamina, postgenal grooves slightly ridged, slightly convergent ventrally, extending to upper margin of hypostomal bridge; dorsal margin of lateral foraminal plate obliterated; subforaminal plate absent; postgenal sulci distinct; postgenal bridge glabrous (Fig. 11). Antenna (Figs 14, 15) with scape broadest medially, coarsely imbricate. Pedicel triangular in lateral view, narrowed ventrally; anelli (two in all species except A. capipunctata, which has three) transverse, glabrous; F1 chalice-shaped, imbricate in basal half (Fig. 14); funicle with each segment fusiform, longer than broad, apically truncate with two rows of MPS and sparse, semi-erect setation; F5–6 fused, apex with radially asymmetric sensillar area (Fig. 14).

Mesosoma : Surface smooth, rugulose or umbilicate with interstices alveolate. Pronotum in dorsal view 2.2–3.3× as broad as long. Mesoscutal midlobe 1.0–1.1× as broad as long; notaulus complete, clearly indicated (Fig. 16). Scutellum 1.2–1.3× as long as broad at its widest; broadly convex dorsally. Scutellum distinctly overhanging dorsellum. Sublateral prepectal concavity shallow; epicnemium flattened, with superficial submedial, shallow depressions to receive procoxa, these separated by low carina connecting to epicnemial carina ventrally. Procoxa imbricate anterobasally and medially, flat, low diagonal carina separating this area from umbilicately punctate anteroventral and lateral portion of procoxa; mesocoxa rugulose to imbricate; mesocoxal foramina narrowly open posteriorly; metacoxa rugulose to imbricate. Metapleuron and lateral areas of propodeum shallowly umbilicate, propodeum vaguely rounded laterally (Fig. 20), bordered laterally by reticulate sculpture overlain with umbilicate punctation; spiracle situated about 1/3 its greatest diameter from dorsellum, median channel with series of distinct transverse carinae (Fig. 20). Fore wing hyaline, venation whitish, setae pale brown, evenly distributed; PMV 1.0–1.1× of V and S 0.7–0.8× of M. Basal cell delimited by cubital and basal folds; speculum present; disc uniformly setose; number of dorsal setae on submarginal vein: female: 2–3, male: 1–4. Parastigma not swollen; marginal vein constricted near its base after parastigma and three times as long as stigmal vein. Stigmal vein at an angle of 20°–30° in relation to marginal vein. Uncus small, not extending far from stigma. Postmarginal vein reduced, less than 1/4 of stigmal vein (Figs 4, 5). Hind wing disc evenly setose. with apex of vein (at hamuli) not swollen or knobbed but darkened, with three hamuli.

Metasoma : Petiole 0.3–0.4× as long as broad in dorsal view, laterally protuberant, connected by dorsal transverse carina. Gaster ovate in lateral view; all terga with finely imbricate sculpture, evenly setose, setae fine and erect; Gt1 depressed behind petiole, setose; Gs1 fused with petiole (Fig. 19); syntergum short, setose; third valvula setose apically, arranged radially and curved.

Genitalia: Female: First valvifer falcate 1/4–1/8 of ovipositor total length, articulates with T9 and the second valvifer very near each other, on its proximal end; second valvifer broad, sickle-shaped; second valvula 3/4 of ovipositor length, with row of 3–4 spaced setae at apical half; third valvula 1/3–1/5 of total ovipositor length (Fig. 26). Male: Phallobase cylindrical, 1.5–2.0× as long as wide, paramere pointed with one apical seta, 1/5× the length of phallobase. Volsella 1/2–1/3 of paramere length. Digitus dorsoventrally flattened, bean-shaped in either ventral or dorsal view, 2–3× as long as wide, bearing a single apical digital spine. Aedeagus cylindrical, dorsoventrally flattened, pointed or round at apex (Fig. 27).

Etymology

Name from the host plant family, Araceae. Gender masculine.

Biology

Ferrière (1924) first described Arastichus gallicola (as Trichoporus gallicola) and defined the species as gall inducer on pistilate flowers of Philodendron selloum (now a synonym of Thaumatophyllum (Philodendron) bipinnatifidum (Mayo 1991) (Fig. 3). Gibernau et al. (2002) described the galls of A. gallicola on flowers of T. solimoesense and reported it as a seed predator. Recently, a more detailed study of the developmental biology of A. gallicola discards seed predation and supports the idea that this species is a gall inducer specialized on ovaries of T. bipinnatifidum (SJG, unpublished).

Female wasps of A. gallicola oviposit during the period of anthesis which lasts 24–48 hours, when the inflorescence spathe is open and leaves the hundreds of pistilate flowers accessible to pollinators and female Arastichus (Gibernau et al. 2002). Once anthesis ends the spathe closes and the space between the spathe and the inflorescence fills with a liquid, often trapping and killing the female wasps inside.

Time of development can vary from one to four months in Arastichus gallicola. Once the infrutescence attains maturity, the spathe develops an encircling dehiscent line at its base and falls, uncovering the orange fruits and galls. Exposure of galls to light and outer atmosphere might trigger adult wasp emergence from the galls, which is done by chewing through each gall wall. A single wasp develops per gall with up to six galls developing in a single fruit. It is possible to find infrutescences and/or fruits containing only seeds, combinations of seeds and galls, or only galls (Fig. 1).

Although we have detailed information about gall induction only in A. gallicola, it is possible that the other two species of Arastichus are also gall inducers rather than seed predators. Examination of collected material for A. gibernau and A. capipunctata indicates that the biology of these species should not be very different from that of A. gallicola.

The eurytomid Prodecatoma philodendri is associated with the galls of Arastichus gallicola and A. gibernau. Ferrière (1924) reported that Prodecatoma were phytophagous, and oviposits from the outside when the spathe is closed and Arastichus galls are in the process of formation (Gibernau et al. 2002; SJG pers. obs.). When examining the cavities from which Prodecatoma adults emerge, a series of tunnels communicate with adjacent Arastichus galls. These attacked galls contained dismembered body parts of Arastichus pupae, indicating that Prodecatoma larvae might consume several of them along with some gall tissue (Gibernau et al. 2002; SJG pers. obs.); this is in line with the fact that the adult Prodecatoma is about 4–5 times larger than the Arastichus adult. Thus, taken all together, P. philodendri is likely entomophytophagous, a common mode of feeding within Eurytomidae.

It is difficult to estimate the taxonomic breadth of the relationship between Arastichus and Araceae. Philodendron is traditionally subdivided in three subgenera: Meconostigma, Philodendron and Pteromischum, but members of Meconostigma have been recently recognized as a distinct genus Thaumatophyllum Schott (Sakuragui et al. 2018). Arastichus has been found in species belonging to Thaumatophyllum (T. bipinnatifidum, T. solimoesense), and in the subgenus Philodendron (P. radiatum). SJG has collected what seem to be female Arastichus body parts from inside closed spathes of P. cordatum and P. curvilobum in Brazil. Further studies and more extensive collecting are needed to determine the degree of species-specificity and to determine whether Arastichus is present in the subgenus Pteromischum as well.

Key to Species of Arastichus

1 Mesoscutum bilobed at posterior margin (Fig. 23). Face with numerous large punctures (Figs 21, 22). Female body (excluding legs and lower face) completely brown (Fig. 6) A. capipunctata sp. nov.
– Mesoscutum straight or slightly emarginate at posterior margin (Fig. 16). Face with at most a few faint, widely spaced punctures (Figs 10, 24). Female head and thorax extensively yellow (Figs 4, 8) 2
2 Posterior corner of metapleuron with circular fossa that is at least half as wide as propodeal spiracle (Fig. 25, arrow). Vertexal suture rounded where it curves down along the inner eye margin (Fig. 24) A. gibernau sp. nov.
– Posterior corner of metapleuron without a noticeable fossa, or with an elongate depression (Fig. 4). Vertexal suture angulate or rounded where it reaches the inner eye margin (Fig. 10) A. gallicola (Ferrière)

Arastichus capipunctata Gates, Hanson, Jansen-González & Zhang, sp. nov.

https://zoobank.org/3F50B966-83A2-456F-9D56-52C800D8C907
Figs 6, 7, 21–23

Diagnosis

Arastichus capipunctata can be distinguished from all other known species through the bilobed mesoscutum at the posterior margin (Fig. 23), and the numerous large punctures on the face (Figs 21, 22). The coloration of both males and females are uniformly brown (Figs 6, 7). Females have three anelli.

Figure 6–7. 

Lateral habitus of Arastichus capipunctata 6 holotype female 7 paratype male.

Material examined

Holotype Costa Rica • [1F]; Guanacaste 9km S Santa Cecilia, Estación Biológica Pitilla, 600 m 18.XII.2010. L. Chavarria leg.; USNMENT01788075; deposited in USNM. Paratypes: [44F, 26M]; same information as holotype; USNMENT01829180–250; USNM. [4F, 4M]; same information as holotype; ANIC. [4F, 4M]; same information as holotype; BMNH. [4F, 4M]; same information as holotype; CNCI. [4F, 4M]; same information as holotype; MNHN. Mexico • [3F, 4M]; Veracruz, San Andrés Tuxtlas, Est. Biol. Tropical Las Tuxtlas, 2.III.2017, 124 m 18°35'22.1"N, 95°5'24.9"W, G. Amancio, A. Aguirre, F. Ozul leg., ex galled fruit Philodendron radiatum; USNMENT01788065–69; USNM. [1F, 1M]; same information as before; CNIN. [46F, 52M]; same information as before; MZUCR.

Description

Holotype female. Body length 2.9 mm. Color: Brown except for the following yellow: scape, pedicel, lower face, prepectus, legs (except metacoxa brown), wing veins white to brown (Fig. 6).

Head. 1.45× as broad as high, with large punctures (Figs 21, 22); anterior tentorial pits with epistomal groove extending ventrally. Supraclypeal area glabrous; clypeus bilobed. Lower margin of eyes slightly sunken; malar suture distinct; malar space 0.37× eye height, asetose beneath eye in elongate microreticulate area; frons protuberant. Preorbital carina absent; intrascrobal area divergent dorsally to laterad anterior ocellus, delimiting shallow equilateral triangular depression in front of anterior ocellus. Ratio of LOL:OOL:POL as 1:2.1:2.5. Vertexal seta 0.45× eye height; vertexal suture rounded at inner eye margin (Fig. 21); occipital margin without transverse, sinuate carina. Head posteriorly lacking postgenal lamina, postgena with ventral depression near ventral margin.

Antenna. (Fig. 6) ratio of scape (minus radicle): pedicel: A1: A2: A3: F1: F2: F3: F4: F5: club as 74:14:1:1:2:18:18:18:18:16:16; A1 constricted medially; A2 transverse; one row of MPS on all funicular segments, erect setae at 45° angle to angle to funicular segment, shorter than the funicular segment to which it is attached (Fig. 6).

Mesosoma. 1.27× as long as broad. Pronotum with two sets of setae posterolaterally. Midlobe of mesoscutum 0.88× as long as broad; smooth, with one pair of adnotaular setae; posterior margin of mesoscutum bilobed (Fig. 24, arrow). Notauli complete, shallow. Scutellum 0.90× as long as broad, effaced imbricate, with two pairs of setae; scutellum lacking submedian scutellar grooves, posterior margin rounded. Propodeum raised medially, laterally imbricate, with paraspiracular carina complete. Prepectus triangular, broadly rounded posteriorly, imbricate. Mesepimeron smooth anteriorly. Epicnemium imbricate. Metapleuron without circular fossa that is at least half as wide as propodeal spiracle. Fore wing with ratio of M:PMV:S as 9:1:4 (Fig. 6); SMV with three setae on dorsal surface.

Metasoma. Finely imbricate; setose along the posterior edges of each gastral tergite; gastral sternites fused or weakly divided; third valvula extends beyond gaster.

Male. Overall morphology and coloration as in female (Fig. 7). Body length 2.9 mm. Antennal ratio of scape (minus radicle):pedicel: A1:F1:F2:F3:F4:F5:F6:club as 25:8:1:2:17:17:17:17:16:9; scape with distinct ventral plaque in apical ½ (Fig. 7), funicular segments clavate basally, with whorl of setae extending ~1.5x length of the funicular segment to which it is attached. MPS sparse and located at midlength; clava with basal whorl and apical setae, MPS located at apex (Fig. 7). Genitalia: phallobase less than twice as long as broad, digitus with tooth-like projection on anterior margin, aedeagus broad, with apex rounded (Fig. 27).

Figure 8–9. 

Lateral habitus of Arastichus gibernau 8 holotype female 9 paratype male.

Variation

Both sexes: setation and sculpture variable; sometimes with faint traces of submedian scutellar grooves. Females: length of body 2.9–3.2mm, SMV with 2–3 setae. Males: length of body 2.4–2.9mm.

Etymology

Named for the distinctive punctate head.

Biology

Reared from Philodendron radiatum.

Distribution

Costa Rica and Mexico.

Arastichus gallicola (Ferrière), comb. nov.

Figs 3, 4–5, 10–15, 16–20

Trichaporus gallicola, Ferrière, 1924.

Exurus gallicola (Ferrière), Costa Lima (1959)

Aprostocetus gallicola (Ferrière), LaSalle (1994)

Material Examined

Lectotype Paraguay • [1F, top right of the pin]; 1914, R. Chodat leg., ovaries of Philodendron selloum = Thaumatophyllum bipinnatifidum (Schott ex Endl.) Sakur., Calazans & Mayo; MNHN. Paralectotypes [9F, 4M]; same information as holotype; MNHN. Other material: Brazil • [37F, 48M]; São Paulo, Ribeirão Preto, University of São Paulo campus, 1.II.2011, Sergio Jansen-González leg., ex galled fruits of Philodendron bipinnatifidum; USNM01829346–432; USNM. [11F, 4M] same information; 13.II.2011; MZUSP. [11F, 6M]; São Paulo, Araras Zoo, 14.II.1988, F.D. Bennett leg., Philodendron inflorescence; ANIC. [1F]; Nova Tenutonia, 27°11'S, 52°23'W, 300–500m, 12.I.1962, F. Plaumann leg.; CNCI. [1M]; same info as before; V. 1971.; CNCI. [3F]; Rondonia, 62 km SW. Ariquemes near faz. Rancho Grande 26.XII.1992, U. Schmitz leg., blacklight trap; CNCI. [5F] same info as before, J.E. Eger leg., 3–15.XII.1997; CNCI. [3F]; Rondonia, 62 km SW. Ariquemes near faz. Rancho Grande 26.XII.1992, U. Schmitz leg., blacklight trap; CNCI. [5F] same info as before, J.E. Eger leg., 3–15.XII.1997; CNCI. French Guiana • [144F, 54M]; Kourou National Road #1, km 96, 26.IV.2012. M. Gibernau leg. ex. Galled fruits of Philodendron solimoesense; USNMENT01829000–01829163; USNM. [4F, 4M] same information as before; ANIC; [4F, 4M] same information as before; BMNH; [4F, 4M] same information as before; CNCI; [4F, 2M] same information as before; CNIN; [4F, 4M] same information as before; MNHN; [9F, 4M] same information as before; MZUCR; [3F] same information as before; MZUSP.

Diagnosis

Arastichus gallicola is morphologically similar to A. gibernau, but the posterior corner of metapleuron of A. gallicola lacks a noticeable fossa, or with an elongate depression (Fig. 4). Additionally, the vertexal suture is angulate or rounded where it reaches the inner eye margin in A. gallicola (Fig. 10), whereas in A. gibernau this suture is always rounded.

Figure 10–15. 

Arastichus gallicola 10 frontal view of head 11 posterior view of head 12 dorsal view of head 13 anterolateral view of head 14 female antenna 15 male antenna.

Description

Female holotype. Body length 3.3mm. Color: Yellow: head, mouthparts, scape, pedicel, mesosoma, femoral depression, acropleuron, legs, ovipositor sheaths; dark brown: funicular segments, apices of mandibles, pronotum immediately surrounding spiracle, scutellum, dorsellum, propodeum, mesopleuron, metapleuron, metasoma. Wing veins white to light brown (Figs 3, 4).

Head. 1.3× as broad as high, effaced imbricate; anterior tentorial pits with epistomal groove extending ventrally (Fig. 10). Supraclypeal area glabrous; clypeus bilobed. Lower margin of eyes slightly sunken; malar suture distinct; malar space 0.58× eye height, asetose beneath eye in elongate microreticulate area; frons protuberant (Fig. 10). Preorbital carina absent; intrascrobal area divergent dorsally to laterad anterior ocellus, delimiting shallow equilateral triangular depression in front of anterior ocellus. Ratio of LOL:OOL:POL as 1:3.1:3.4. Vertexal suture angulate, or rounded at inner eye margin (Fig. 10); occipital margin with transverse, sinuate carina. Head posteriorly lacking postgenal lamina, postgena without ventral depression near ventral margin.

Antenna. (Fig. 14) ratio of scape (minus radicle): pedicel: A1:A2:F1:F2:F3:F4:F5:F6:club as 12.5:3.8:1.3:1:4.5:4.5:4.5:3.8:3.8:5; A1 constricted medially; A2 transverse; two rows of setae on all funicular segments (Fig. 14); erect setae at 45° angle to funicular segment, shorter than the funicular segment to which it is attached to (Fig. 4).

Mesosoma. 1.8× as long as broad. Pronotum with two sets of setae posterolaterally. Midlobe of mesoscutum 1.0× as long as broad; with two pairs of adnotaular setae; posterior margin of mesoscutum not bilobed (Fig. 16). Scutellum 1.2× as long as broad; effaced imbricate, with one to two pairs of setae; notauli complete, shallow; scutellum lacking submedian scutellar grooves, posterior margin rounded. Propodeum raised medially, laterally imbricate, with paraspiracular carina complete. Prepectus triangular, broadly rounded posteriorly, imbricate. Mesepimeron striate, becoming smooth anteriorly grading into femoral depression. Epicnemium imbricate. Metapleuron without circular fossa that is at least half as wide as propodeal spiracle. Fore wing with ratio of M:PMV:S as 3:1:1.1 (Fig. 4).

Figure 16–20. 

Arastichus gallicola 16 dorsal view of mesosoma 17 ventral view of mesosoma 18 ventral view of female metasoma 19 lateral view of female metasoma 20 propodeum.

Metasoma. Finely imbricate; setose along the posterior edges of each gastral tergite; gastral sternites fused or weakly divided; third valvula does not extend beyond gaster.

Male. Overall morphology as in female (Fig. 5). Body length 2.5 mm. Color: Dark brown except the following golden: base of scape, ventral mouthparts, acropleuron, coxae apically, legs, metatibia in apical 1/4. Antennal ratio of scape (minus radicle):pedicel: A1:F1:F2:F3:F4:F5:F6:club as 6.9:1.4:1:4.3:4.7:4.7:4.3:4.1:3.6:2.9; scape with distinct, white ventral plaque in apical ½ (Fig. 5), funicular segments wide at base and narrowing off towards apex, with whorl of setae extending ~1.5x length of the funicular segment to which it is attached, MPS sparse and located at midlength; clava with basal whorl and apical setae, MPS located at apex (Fig. 5). Genitalia: phallobase twice as long as broad, digitus slender without projection on anterior margin, aedeagus slender, with apex pointed; digiti with or without a submedian longitudinal suture from the base of the digital tooth but not reaching the base of the digiti (Fig. 27).

Variation

Both sexes: setation and sculpture variable; sometimes with faint traces of submedian scutellar grooves; vertexal suture can be rounded or angulate. Females: 2.6–3.8mm, scutellum with brown coloration often incomplete laterally, complete medially and anteriorly/posteriorly on scutellar margins; ocellar triangle sometimes brown; pronotal setation ranges from 1–3 per side, adnotaular setation ranges from 1–3 per side with the occasional odd seta in the notaulus; ocellar triangle often with two small divergent setae. Males: 2.5–3.0mm, may have brownish infuscation of the pro- and mesofemur, meso- and metacoxa may be entirely brown. Specimens from Araras Zoo in Brazil consistently had two setae on the lateral lobes of mesoscutum, whereas other specimens had three. However given the lack of other consistent characteristics, we conservatively group them under A. gallicola. Variation in female and male genitalia was found. Females reared from T. bipinnatifidum showed two distinct ovipositor morphologies with variation due mostly to larger or smaller first and second valvifers. Females reared from T. solimoesense showed an intermediate size ovipositor. Males reared from T. solimoesense show a longitudinal submedian suture in the digiti that begins at the base of the digital tooth and does not reach the base of the digiti.

Biology

Reared from Thaumatophyllum bipinnatifidum and T. solimoesense.

Distribution

Brazil and Paraguay.

Arastichus gibernau Gates, Hanson, Jansen-González & Zhang, sp. nov.

https://zoobank.org/65576A2E-AFA1-4A26-9C76-675B614EAC82
Figs 8, 9, 24, 25

Material Examined

Holotype Panama • [1F]; Barro Colorado Island, Canal Zone, 40-22220, J. Zetek leg., ex. Philodendron oxycardium flowers, 8.30'40 1.IX.1940 ; USNMENT01829267; USNM. Paratypes [24F, 25M]; same information as holotype; USNMENT01829268–325; USNM. [3F, 3M]; same information as holotype; ANIC. [4F, 4M]; same information as holotype; BMNH. [4F, 4M]; same information as holotype; CNCI. [4F, 4M]; same information as holotype; MNHN. [4F, 4M]; same information as holotype; MZUCR.

Figure 21–25. 

Arastichus capipunctata 21 frontal view of head 22 dorsal view of head 23 dorsal view of mesosoma, arrow pointing to the bilobed posterior margin of mesoscutum 24–25 Arastichus gibernau 24 frontal view of head 25 lateral view of mesosoma, arrow pointing to the circular fossa on the posterior corner of metapleuron.

Diagnosis

Arastichus gibernau is morphologically similar to A. gallicola, but the posterior corner of metapleuron of A. gibernau has a noticeable fossa, or with an elongate depression ((Figs 8, 9). Additionally, the vertexal suture is always rounded where it reaches the inner eye margin in A. gibernau (Fig. 24), whereas in A. gallicola this suture is angulate or rounded (Fig. 10).

Description

Female holotype. Body length 4.4 mm. Color. Golden: head, mouthparts, antenna (brownish tint), mesosoma, femoral depression, acropleuron, legs, ovipositor sheaths. Light brown: wing veins, antennae. Dark brown: scutellum, dorsellum, propodeum, metapleuron; wing veins whitish to brownish (Fig. 8).

Head. 1.36× as broad as high, effaced imbricate; anterior tentorial pits with epistomal groove extending ventrally (Fig. 24); supraclypeal area with sparse setae extending from below scrobe to clypeus; clypeus bilobed. Lower margin of eyes slightly sunken; malar suture distinct; malar space 0.46× eye height, asetose beneath eye in elongate microreticulate area; frons protubertant. Preorbital carina absent; intrascrobal area divergent dorsally to laterad of anterior ocellus, delimiting shallow, equilateral triangular depression anterad to anterior ocellus. Ratio of LOL:OOL:POL as 1:2.4:2.6. Vertexal suture rounded at inner eye margin (Fig. 24); occipital margin with transverse, sinuate carina. Head posteriorly lacking postgenal lamina, postgena without ventral depression near ventral margin. Gena expanded ventrally, giving it a “puffy cheeks’’ appearance.

Antenna. Ratio of scape (minus radicle): pedicel: A1: A2: F1: F2: F3: F4: F5: club as 18:5:1.5:1:8.3:7.3:7:6.3:6.3:2.5 (Fig. 8); A1 constricted medially, A2 transverse, one row of MPS on all funicular segment, two rows of erect setae at 45° angle to funicular segment, shorter than the funicular segment to which it is attached (Fig. 8).

Mesosoma. 1.34× as long as broad. Pronotum with three sets of setae posterolaterally. Midlobe of mesoscutum 0.73× as long as broad; with two pairs of adnotaular setae; posterior margin of mesoscutum not bilobed. Notauli complete, shallow. Scutellum 1.01x as long as broad; effaced imbricate, with two pairs of setae. Metapleuron with circular fossa that is at least half as wide as propodeal spiracle (Figs 8, 25 arrow). Propodeum raised medially, laterally imbricate, with paraspiracular carina complete. Prepectus triangular, broadly rounded posteriorly, imbricate. Mesepimeron striate, becoming smooth anteriorly grading into femoral depression. Epicnemium imbricate. Fore wing with ratio of M:PMV:S as 2.5:3.3:1.

Metasoma. Finely imbricate (Fig. 8); setose along the posterior edges of each gastral tergite; third valvula extends beyond metasoma.

Male. Overall morphology as in females (Fig. 9). Body length 3.3 mm. Color: Dark brown except the following white: all tibia, procoxa apically, pro- and meso femur, metatibia in apical 1/4. Antennal ratio of scape (minus radicle):pedicel: A1:F1:F2:F3:F4:F5:F6:club as 10.3:2.5:1:6.8:6.8:6.8:6.5:5.3:4.8:.3.5; scape with distinct ventral plaque in apical ½ (Fig. 9), funicular segments clavate basally, with whorl of setae extending ~1.5x length of the funicular segment to which it is attached, MPS sparse and located at midlength; clava with basal whorl and apical setae, MPS located at apex (Fig. 9). Genitalia: phallobase twice as long as broad, digitus slender with a blunt projection on anterior margin, aedeagus slender, with apex pointed (Fig. 27).

Figure 26. 

Female genitalia of Arastichus spp. based on photographs of slide-mounted specimens. Morphological variations are evident among species and within species.

Figure 27. 

Male genitalia of Arastichus spp. based on photographs of slide-mounted specimens. Dsp digital spine; Aed aedeagus; Dqt digitus; Dsp digital spine; Phl phallobase; Prm paramere; Vsl volsella.

Variation

Considerable variation is noted. Females: 3.5–5.2mm, pronotal setation ranges from 1–3 per side, adnotaular setation ranges from 1–2 per side. Males: 2.8–3.5mm, may have brownish infuscation of the pro- and mesofemur.

Etymology

Named in honor of Dr. Marc Gibernau for providing a very large sample of specimens of this species for our research.

Biology

Reared from Philodendron hederaceum var. oxycardium.

Distribution

Panama.

Discussion

Gall induction have evolved multiple times within Tetrastichinae, and to date is known from 10 different host plant families (LaSalle 1994; Fisher et al. 2014; Gates et al. 2020; Singh et al 2022) around the world. However, given the diversity and the lack of taxonomic attention in recent years, the true number of tetrastichine gall inducers is likely much higher. Hopefully with the advances of phylogenomic techniques such as UCEs and broader taxonomic sampling of species-rich regions such as the Neotropics, we can gain a better understanding of the true diversity of gall induction within Eulophidae and Chalcidoidea as a whole.

Acknowledgements

We thank Barry Hammel of the Missouri Botanical Gardens and Christian Trejos of the University of Costa Rica for helping with plant identifications in Costa Rica, and Taina Litwak of USDA SEL for the illustration. We thank Christer Hansson and one anonymous reviewer for providing valuable feedback that have improved the manuscript. SJG was supported by FAPESP (#09/10273-9). The computations in this paper were conducted on the Smithsonian High Performance Cluster (SI/HPC), Smithsonian Institution. https://doi.org/10.25572/SIHPC. YMZ is supported by Oak Ridge Institute for Science and Education (ORISE) fellowship. Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer.

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  • Sakuragui CM, Calazans LSB, de Oliveira LL, de Morais EB, Benko-Iseppon AM, Vasconcelos S, Schrago CEG, Joseph Mayo SJ (2018) Recognition of the genus Thaumatophyllum Schott – formerly Philodendron subg. Meconostigma (Araceae) – based on molecular and morphological evidence. PhytoKeys 98: 51–71.https://doi.org/10.3897/phytokeys.98.25044
  • Shimbori EM, Penteado-Dias AM, Nunes JF (2011) Monitoriella Hedqvist (Hymenoptera: Braconidae: Doryctinae) from Brazil, with descriptions of three new species. Zootaxa 2921: 28–38. https://doi.org/10.11646/zootaxa.2921.1.3
  • Singh S, Kumar A, Kaneria M (2022) Description of five new eulophid species (Hymenoptera: Eulophidae) associated with leaf vein galls of Madhuca longifolia (J. Koenig) (Sapotaceae) in India. Zootaxa 5129: 1–36. https://doi.org/10.11646/zootaxa.5129.1.1

Supplementary material

Supplementary material 1 

Table S1

Y. Miles Zhang, Michael W. Gates, Paul E. Hanson, Sergio Jansen-González

Data type: Specimen information.

Explanation note: Locality information and accession numbers for UCE/Sanger loci.

This dataset is made available under the Open Database License (http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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