Species in the family Cynipidae, one of the two largest families included in the Cynipoidea (Insecta: Hymenoptera), are biologically peculiar because all their representatives are associated with plant galls. They either induce the galls themselves or live inside galls caused by other insects, most frequently other cynipids but also Chalcidoidea and Lepidoptera (Nieves-Aldrey, 2001; Van Noort et al., 2007; Nieves-Aldrey & San Blas, 2015; Ronquist et al., 2015). According to Ronquist et al. (2015), the family is currently divided into 12 tribes: Aylacini, Aulacideini, Ceroptresini, Cynipini, Diastrophini, Diplolepidini, Eschatocerini, Paraulacini, Pediaspidini, Phanacidini, Qwaqwaini and Synergini. Of these, Cynipini is the most species-rich and diverse tribe, with approximately 1,000 species of so-called “oak gall wasps,” cynipids associated with oaks (Quercus species) and other plants of the Fagaceae family (Csóka et al., 2005; Stone et al., 2009).

The vast majority of Cynipini species described have been from the Holarctic region, but more recently, rich faunas of cynipids are being discovered from the Oriental and the Neotropical regions, historically poorly sampled with regard to cynipids (Liljeblad et al., 2008; Nieves-Aldrey et al., 2009; Stone et al., 2009; Melika et al., 2010; Medianero & Nieves-Aldrey, 2011; Tang et al., 2016). In the Neotropical region, an increasing sampling effort in countries such as Costa Rica, Panama and Colombia has yielded rich Cynipini fauna, for the most part undescribed. These studies have extended the geographical distribution of genera of gall wasp such as Amphibolips Reinhard, Disholcaspis Dalla Torre & Kieffer, Loxaulus Mayr, Odontocynips Kieffer, Bassettia Ashmead, Diastrophus Hartig, Andricus Hartig, Callirhytis Förster and Melikaiella Pujade-Villar (Pujade-Villar, 2008; Medianero & Nieves-Aldrey, 2011; Nieves-Aldrey et al., 2013; Medianero & Nieves-Aldrey, 2014; Pujade-Villar & Rodríguez, 2015). At the same time, new genera endemic to this region have been described, for example Agastoroxenia Nieves-Aldrey & Medianero, Coffeikokkos Pujade-Villar & Melika, Barucynips Medianero & Nieves-Aldrey and Zapatella Pujade-Villar & Melika (Nieves-Aldrey & Medianero, 2010; Pujade-Villar et al., 2012a, 2012b; Medianero & Nieves-Aldrey, 2013).

Neuroterus Hartig is one of the more species-rich Cynipini genera along with Andricus Hartig. Since Hartig (1840) described the genus for the first time, based only on European species, Neuroterus has become one of the more problematic Cynipini genera regarding their generic limits and the identification and classifications of their included species. The reasons for this are diverse. Neuroterus is a taxonomically complex genus, very rich in species and widely distributed around the world; the species are extremely uniform in morphology, and finding reliable diagnostic characters that allow for their identification is extremely difficult.

Some morphological and molecular phylogenetic studies have found evidence that the genus is not monophyletic with regard to certain lineages or species groups (Liljeblad et al., 2008; Stone et al., 2009; Melika et al., 2010), as traditionally conceived by Hartig and subsequently by Kinsey (1923). As a consequence, and based on host Quercus associations, some authors have noted that the classification should split some lineages or groups of species closely related to Neuroterus into the separate genera Pseudoneuroterus Kinsey and Cerroneuroterus Melika & Pujade-Villar. More recently, a new genus closely related to Neuroterus, Cycloneuroterus Melika & Tang, was described for a group of Oriental species associated with the ancestral Fagaceae ―Quercus subgenus Cyclobalanopsis, Lithocarpus and Castanopsis― in Taiwan and mainland China (Tang et al., 2011, 2016).

Currently, Neuroterus, as conceived by Melika et al. (2010), includes approximately eighty species from the Holarctic Region. From the United States and Canada, 56 species have been listed (Kinsey, 1923; Burks, 1979; Melika & Abrahamson, 1997, 2002). Kinsey (1938) recorded six new species from Mexico, and three more have been recently described (Pujade-Villar et al., 2015, 2016), for a total of nine Neuroterus species recorded from that country. The presence of Neuroterus species south of Mexico has been not recorded to date.

In the framework of a continued study of the oak gall wasps (Cynipidae) in the Neotropical region, this paper includes the description of three new species of Neuroterus from Panama and Costa Rica; this represents the first accurate report of this genus in Central America and the Neotropical Region.

STUDY MATERIAL

The adults studied were reared from galls collected from Quercus bumelioides Liebm. and Quercus lancifolia Schledl & Cham., in montane tropical forests in Panama. The Panama samples were collected from December 2007 to May 2009 and November 2016 in several sites in Chiriqui Province, Panama. Additionally, some localities were sampled by the second author in January 2014 in Costa Rica, where galls from Q. bumelioides yielded one of the new species described. The adult insects emerged from the galls in rearing cages under laboratory conditions. Voucher specimens of adults and their galls were deposited in the entomology collections of the Museo Nacional de Ciencias Naturales, Madrid (Spain) (MNCN) and Maestría en Entomología, Universidad de Panamá (MEUP). The identification of the Quercus species was based on several key references (Burger, 1977; Breedlove, 2001), as well as comparison with materials from the collections of the University of Panama and the Smithsonian Tropical Research Institute.

SPECIMEN PREPARATION

Adult cynipids were dissected in 70% ethanol, air dried, mounted on a stub and coated with gold for observation under a scanning electron microscope (SEM). Micrographs were taken by an EVO 40 Zeiss and FEI QUANTA 200 microscope (high vacuum technique) for several standardized views. The forewings were mounted on slides in Euparal and were later examined under a Wild MZ8 stereo microscope. Images of the adult habitus and gall dissections were taken with a NIKON Coolpix 4500 digital camera attached to a Wild MZ8 stereo microscope.

TERMINOLOGY AND MEASUREMENTS

Measurements were performed with a calibrated micrometer scale attached to an ocular of the light microscope. The terminology of morphological structures and abbreviations follows Ronquist & Nordlander (1989), Ronquist (1995), Nieves-Aldrey (2001) and Liljeblad et al. (2008). For the cuticular sculpture we follow Harris (1979). Measurements and abbreviations used include the following: the post-ocellar distance (POL) is the distance between the inner margins of the posterior ocelli; the ocellar-ocular distance (OOL) is the distance from the outer edge of a posterior ocellus to the inner margin of the compound eye.

DESCRIPTION OF SPECIES

Neuroterus elvisi Medianero & Nieves-Aldrey sp. n.

(Figs. 1, 2 & 7C-F)

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Diagnosis and Comments. The simple claws, distinctive malar sulcus and presence of a median propodeal carina, but lack of lateral carinae on the propodeum, are diagnostic characters which group the new species within the Nearctic and Neotropical species of Neuroterus and differ from Palaeartic species of Neuroterus sensu lato. Neuroterus elvisi can be distinguished from the other two new species described in this paper by a combination of diagnostic characters listed in Table 1 and as follows: predominantly yellowish coloration, notauli weak but traceable; mesoscutum with alutaceous sculpture visible, speculum of mesopleuron smooth; antennal flagellum of female with 11 segments, median carina of propodeum conspicuous, divided in two arms anteriorly and Rs of forewing not prolonged at apex. By the type of gall, the closet species geographically is Neuroterus junctor Kinsey, 1938 from Mexico, although the gall of the latter is hairy, whereas the gall of N. elvisi is glabrous. Morphologically, adults of the two species are similar, but the new species differs from N. junctor in its lighter coloration, which is black in N. junctor, and mesoscutum with alutaceous sculpture (smooth in N. junctor). By the sculpture of the mesosoma and metasoma, N. elvisi resembles Neuroterus ellongatum Pujade-Villar & Melika (asexual generation), recently described from Mexico (Pujade-Villar et al., 2015), but F1 is only slightly longer that F2, and the metasoma is 2.0 times as long as high in lateral view in Neuroterus ellongatum, whereas F1 is 1.7 times as long as F2, and the metasoma is only slightly longer than high in N. elvisi. Additionally, the galls of the two species are different, developing in twigs in N. ellongatum and in leaves in N. elvisi.

Description. Body length, 1.8 mm (range 1.5- 2.3 mm; N = 6) for females; 1.8 mm (range 1.5–2.2; N = 4) for males (Figs. 7C-E). Head yellowish-orange, except frons and distal part of mandibular teeth which are dark brown to blackish; mesosoma predominantly shining brown to blackish except medial area of mesoscutum, pronotum laterally and mesopleura, which are orange to light brown. Metasoma blackish. Scape, pedicel and first flagellomere of antennae yellowish, remaining flagellomeres light brown; legs entirely yellowish. The males have a predominantly yellowish coloration, except the frons, lateral and anterior areas of the mesoscutum, propodeum and metasoma (entirely), which are orange to light brown. Forewings are hyaline in both sexes.

Sexual Female. Head (Figs. 1A-C), uniformly alutaceous, barely pubescent; in dorsal view 2.3x as broad as long. POL 1.2 times as long as OOL; posterior ocellus separated from inner orbit of eye by 3.5 times its longest diameter (Fig. 1C). Head more or less pentagonal in anterior view, with ocellar plate raised (Fig. 1A), 1.17x as broad as high. Genae not expanded behind eyes. Vertex, frons and face uniformly alutaceous; vertex and frons with a few sparse short setae, face with more numerous and relatively longer setae, occiput barely pubescent with sparse and shorter setae. Clypeus trapezoidal, 2.0x as broad as high; with very weak sculpture and some long setae medially; ventral margin straight and strongly projecting over mandibles. Anterior tentorial pits conspicuous; epistomal sulcus and clypeo-pleurostomal lines indistinct. Malar space 0.22x as long as height of compound eye; malar sulcus distinct, ending near clypeal margin. Distance between antennal rim and compound eye 1.3 times width of antennal socket including rim. Head, posterior view (Fig. 1B) with weak alutaceous sculpture and with some long sparse setae at external edges. Gula long; distance between occipital and oral foramina 1.5x as long as the occipital foramen. Hypostomal sulci inconspicuous, converging at the oral foramen.

Mouthparts (Figs. 1B, 1D). Mandibles strong and exposed, right mandible with three teeth, left with two teeth. Cardo of maxilla visible, maxillary stipes approximately 1.6 times longer than wide. Maxillary palp five-segmented. Labial palp with two visible segments.

Antennae (Fig. 1E) of moderate length, as long as 0.7 body length, with 13 segments; flagellum not broadening toward apex, with short, erect setae and elongate placodeal sensilla visible on all flagellar segments. Relative length/width of antennal segments: 20/9:16/10:30/9:18/10:17/10:20/10:16/9:17/10:15/10:13/10:15/10:15/10:10/9. Pedicel, 1.6x as long as broad, 0.8 times as long as scape; F1 1.7x as long as F2 (Fig. 1E); F11 2x as long as broad and 1.3 times as long as F10 (Fig. 1E).

Mesosoma short; 1.2x as long as broad in dorsal view (Fig. 2A), slightly longer than high in lateral view and with dorsal margin strongly convex (Fig. 2B). Pronotum very short medially in frontal view, with weak alutaceous sculpture in lateral view and barely pubescent.

Mesonotum. Mesoscutum (Fig. 2A), delicately coriaceus, shiny, glabrous except for a group of sparse short setae anteromedially. Notauli shallowly marked but visible, more clearly in posterior one third of mesoscutum; anteroadmedian signa and parapsidial signa absent, indicated only by delicate sculpture (Fig. 2A). Median mesoscutal impression absent. Transscutal fissure absent. Scutellum rounded (Fig. 2A), approximately 0.5 times as long as mesoscutum, delicately coriaceous, barely pubescent, dorsal surface with a distinct sharp margin posterolaterally, posterior margin not emarginate. Scutellar foveae in form of transverse deep groove, smooth and shining. Scutellum, barely overlapping the dorsellum posteriorly in lateral view (Fig. 2B). Mesopleuron (Fig. 2B) weakly alutaceous, except for the smooth postero dorsal area (speculum); barely pubescent with sparse shorter setae in mesopleural triangle.

Metanotum (Fig. 2C). Metapectal-propodeal complex. Metapleural sulcus reaching posterior margin of mesopectus at about two thirds distance from ventral margin (Fig. 2B). Metascutellum with weak rugose sculpture; metanotal trough smooth and glabrous. Propodeum almost smooth; lateral propodeal carinae absent; medial carina present, divided in two branches anteriorly and posteriorly in some longitudinal carinae (Fig. 2C). Median propodeal area smooth and pubescent on the sides

Legs. Metafemur 3.6x as long as broad; metatibia 1.3x as long as combined length of metatarsomeres (Fig. 2F). Metatarsal claws simple, without a basal lobe or tooth (Fig. 2G).

Forewing (Fig. 7F). 1.3 times as long as body, hyaline, setose, veins dark brown to black. Radial cell 4x as long as broad, open along anterior margin, areolet triangular, closed and distinct; R1 oriented obliquely to anterior margin of wing. Rs slightly expanded at apex. R1 reaching margin of wing, Rs ending close to wing margin. M nearly straight, not reaching wing margin. Rs+M incomplete reaching basalis at its mid-height. First abscissa of radius (2r) slightly angulate in the middle. Basal cell setose; costal cell conspicuously setose. Apical margin of wing with a fringe of long setae.

Metasoma (Fig. 2D). Short, as long as mesosoma, 1.2x as long as high, in lateral view. Tergites smooth and shining dorso-laterally, T4-T7 alutaceous ventrally (Fig. 2E). T3 with a group of sparse short setae anteromedially. Projecting part of hypopygial spine, beyond attachment of lateral flap, relatively short (Fig. 2E); approximately 1.1 times as long as basal height of the spine; lateral margins of hypopygial spine with long setae projecting over apical end of the spine.

Male. Besides the lighter body, antennae and leg coloration (Fig. 7D), differs from the female as follows: antennae (Fig. 1F) with 14 segments; F1 2.3x as long as F2; F1 modified, curved and flattened and slightly expanded distally. Mesoscutum without alutaceous sculpture, smooth and shining. Genitalia. Phallus (Fig. 2H). Apical part of aedeagus moderately expanded subapically; length of paramere short, not reaching beyond digitus; basidorsal margin of parameral plates only weakly incised medially. Apical margin of basal ring incised.

Gall (Figs. 8F-H). Small, irregular swellings of the leaves, with smooth and bare surface. Polythalamous, developing in petiole and midrib and engulfing leaf lamina. The galls are light green when fresh but dark green when mature and brown when old. Diameter 10 to 18 mm. Galls are relatively common on Quercus bumelioides at the Volcán Barú site. The gall most closely resembles that of Neuroterus junctor from Mexico.

Distribution. N. elvisi was found at 1,800 m above sea level at Volcán Barú, Chiriquí Province, Panama.

Etymology. Named after Elvis Segundo for his help in field work and oak gall wasps samplings in the mountains of Panama.

Biology. Sexual generation. Galls formed in the leaves of Q. bumelioides mature in May and insects emerge soon thereafter in the same month. Although the asexual generation is unknown, we have circumstantial evidence that they are similar to those of the sexual generation but develop in early November (Fig. 8H) during the rainy season when new Q. bumelioides leaves begin to appear. The similarity between galls and insects of the two alternating generations in the Nearctic species of Neuroterus has been mentioned by Kinsey (1923).

Neuroterus pulchrigalla Medianero & Nieves-Aldrey sp. n. (Figs. 3, 4 & 7A-B)

http://urn:lsid:zoobank.org:act:B41783B3-6490-42B8-8471-2F6E71B2A861

Diagnosis and Comments. Neuroterus pulchrigalla is similar to Neuroterus elvisi in many morphological diagnostic characters. Besides the light brown coloration in N. pulchrigalla, the two species can be readily separated as follows (see Table 1): Antennal pedicel only 1.3x as long as broad (1.6x in N. elvisi); placodeal sensilla present only on flagellar segments 3 to 11, while present in all the flagellomeres in N. elvisi; genae not expanded behind eyes; clypeus evidently not trapezoidal; mesoscutum almost smooth and notauli invisible; mesopleuron entirely alutaceous, mesoscutellum smooth, median propodeal carina not marked and Rs of forewing not apically enlarged. The gall of the new species has a distinctive appearance (Figs. 8A-E). Among the Nearctic species of Neuroterus, including the species described from Mexico, only the gall of Neuroterus argentatus Weld, 1944, described from Arizona on Quercus gambelii, has some resemblance, but the galls of N. argentatus are different in shape and covered by radiating silvery hairs. Furthermore, the morphology of the adults is also different, mainly with respect to body coloration and the relative length of flagellomeres F1/F2.

General Description. Body length, 1.41 mm (range 1.2-1.75 mm; N=12) for females. Female body predominantly dark brown. Scape, pedicel and F1 yellow, remaining flagellomeres dark yellowish. Legs predominantly brown, with coxae distally, trocanters, distal femorae, tibiae (except metatibia) and all tarsi yellowish. Forewings hyaline with veins brown.

Asexual Female. Head, uniformly alutaceous, barely pubescent; in dorsal view approximately 2.4x as broad as long (Fig. 3A). POL 1.67x longer than OOL; posterior ocellus separated from inner orbit of eye by 2.3 times its longest diameter (Fig. 3A). Genae not expanded behind eyes. Head oval elongate in anterior view (Fig. 3B), about as high as broad. Vertex, frons and face uniformly alutaceous; vertex and frons without setae, face with relatively long white setae. Clypeus trapezoidal, 1.6x wider than high, shining, moderately pubescent, ventral margin straight and projecting over mandibles; median area of clypeus with weak alutaceous sculpture; the lateral and the ventral projected areas smooth. Anterior tentorial pits conspicuous; epistomal sulcus and clypeo-pleurostomal lines indistinct. Malar space 0.2x the height of compound eye, with a distinctive, complete and well-impressed malar sulcus. Distance between antennal rim and compound eye 1.3x the width of antennal socket including rim. Ocellar plate slightly raised. Head, posterior view (Fig. 3C) with weak alutaceous sculpture and some setae on outer areas. Gula long; distance between occipital and oral foramina 1.5x as high as the occipital foramen. Hypostomal sulci visible, converging at the oral fosa. Without an occipital carina.

Mouthparts. Mandibles strong and exposed, right mandible with three teeth, left with two teeth. Cardo of maxilla not visible, maxillary stipes 1.4x as long as broad. Maxillary palp five-segmented. Labial palp with two visible segments.

Antennae (Fig. 4A) of moderate length, as long as 1/2 body length, with 13 segments; flagellum slightly broadening toward apex, with short, erect setae and elongate placodeal sensilla visible only on flagellar segments 3-11. Relative length/width of antennal segments as: 21/12:20/15:30/8:20/8:16/10:19/10:17/10:​17/10:16/11:17/11:17/11:15/11:17/12. Pedicel, globose, 1.3x as long as broad, 0.6x as long as F1; F1 1.5x as long as F2 (Fig. 4A); F11 1.4x as long as broad and slightly longer than F10.

Mesosoma short, 1.2x as long as broad in dorsal view (Fig. 3D), 1.1x as long as high in lateral view and with dorsal margin strongly convex (Fig. 3E). Pronotum in frontal view very short medially, 0.08x as long as lateral distance of pronotum (Fig. 3F), pronotal plate indistinct, with alutaceous sculpture in lateral view, and barely pubescent (Fig. 3E).

Mesonotum. Mesoscutum (Fig. 3D), virtually smooth, although with obsolete alutaceous sculpture visible in some areas, glabrous except for a group of sparse short setae anterolaterally. Notauli and median mesoscutal impression absent; anteroadmedian signa and parapsidial signa absent. Transscutal fissure absent. Scutellum rounded, approximately 0.5x as long as mesoscutum, almost smooth and barely pubescent, dorsal surface with a distinct sharp margin posterolaterally, posterior margin not emarginate. Scutellar foveae in form of transverse deep, smooth and shining, inverted V-shaped groove. Scutellum not overlapping the metascutelum posteriorly in lateral view (Fig. 3E). Mesopleuron (Fig. 3E) weakly alutaceous and glabrous on its entire surface; ventral margin of mesopleural triangle somewhat interrupted in the middle.

Metanotum (Fig. 4B). Metapectal-propodeal complex. Metapleural sulcus reaching posterior margin of mesopectus at about two thirds distance from ventral margin (Fig. 3E). Metascutellum with weak rugose sculpture; metanotal trough smooth and glabrous. Propodeum almost smooth; lateral propodeal carinae absent; a medial, weakly marked carina is visible (Fig. 4B). Median propodeal area smooth and pubescent on the sides.

Legs. Metafemur 3x as long as broad; metatibia 1.3x as long as combined length of metatarsomeres (Fig. 4E). Metatarsal claws simple, without a basal lobe or tooth (Fig. 4F).

Forewing (Fig. 7B). 1.3x as long as body, hyaline, setose, veins dark brown to black. Radial cell 4x as long as broad, open along anterior margin, areolet triangular, closed and distinct; R1 oriented obliquely to anterior margin of wing. Rs not expanded at apex; R1 and Rs reaching margin of wing, Rs+M incomplete reaching basalis at its mid-height. First abscissa of radius (2r) slightly angulate in the middle. Basal cell and costal cell setose. Apical margin of wing with a fringe of long setae.

Metasoma (Fig. 4C). As long as head + mesosoma combined; as long as high in lateral view. Tergites, smooth and shining dorso-laterally (Fig. 4C). T3 with a group of sparse short setae anteromedially. Projecting part of hypopygial spine short, about as long as broad (Fig. 4D); lateral margins of hypopygial spine with long setae, the subapical ones projecting over apical end of the spine.

Gall (Figs. 8A-E). Galls have a cylindrical shape, measuring 5 x 2 mm. the gall surface is covered with long dense yellowish hairs. Internally, two parts are visible; an ovoid larval cell at the attachment of the gall on the leaf and an apical empty part (Fig. 8D). The galls grow isolated or more frequently grow in close clusters formed by 2-10 galls on the midrib of Quercus bumelioides leaves (Figs. 8A-C). The galls are yellow when fresh, orange when mature and brown when old. Galls are relatively abundant on Quercus bumelioides at the Volcán Barú site in Panama.

Distribution. Neuroterus pulchrigalla was found between 1,431-1,800 m above sea level at Volcán Barú and El Salto, Chiriquí Province, Panama. We have found galls of this species in the same type locality type as the other new species described in this paper from Panama.

Etymology. Named after the pretty, brilliantly colored leaf galls induced by this species.

Biology. Only the asexual generation of Neuroterus pulchrigalla is known, inducing galls on Q. bumelioides leaves. The galls are found between January and March, during the dry season, when new Q. bumelioides leaves begin to mature. The adult insects emerge from mature galls in February or May.

Neuroterus glandiphilus Nieves-Aldrey & Medianero sp. n.

(Figs. 5, 6, 7G-H & 9)

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Diagnosis and remarks. Neuroterus glandiphilus differs from N. elvisi and N. pulchrigalla in the diagnostic characters and character states shown in Table 1. N. glandiphilus is readily distinguished by the 13/14 segmented antenna; with F1 only 1.2x as long as F2; mesoscutum with visible coriaceous sculpture, including some longitudinal ridges on the postero medial area; the dark brown to black coloration, mesopleuron entirely coriaceous, and the median propodeal carina branched anteriorly and posteriorly are additional distinguishing features.

We know of only one species of Neuroterus in the American continent galling acorns, Neuroterus cupulae Kinsey, 1922, later considered an asexual generation synonym of Neuroterus quercicola var. pacificus Kinsey (Kinsey, 1923; Weld, 1952), a species distributed in California. However, the gall of N. cupulae differs from the gall of N. glandiphilus in its smaller size and position in the acorn cup.

Description. Body length 2.2 mm (range 2-2.5; N = 5) for females; 2.2 mm (N = 1) for males. Head, mesosoma and metasoma of female black, Mandibles light brown. Antenna with scape, pedicel and first flage-llomere light brown; remaining flagellomeres dark brown. Forewing hyaline, with brown veins. Legs brown except coxae, proximal femur, distal tibiae and last tarsomere dark brown to blackish. Males have a similar coloration.

Sexual Female (Fig. 7G). Head 2.4x as broad as long in dorsal view, slightly broader than mesosoma in dorsal view. Temples expanded behind compound eye. POL 1.6x OOL; posterior ocellus separated from inner orbit of eye by 2.6x its longest diameter. Head 1.15x as broad as high in anterior view (Fig. 5A); genae slightly expanded behind eye. Face with sparse long setae, absent in frontal area. Face and frons with weak coriaceous sculpture. Clypeus distinct, with tighter coriaceous sculpture, its ventral margin sinuate and projecting over mandibles (Fig. 5A). Anterior tentorial pits conspicuous; epistomal and clypeo-pleurostomal lines not marked. Malar space 0.26x height of compound eye. Malar sulcus conspicuously well marked. Toruli situated slightly above mid-height of compound eye; distance between antennal rim and compound eye 1.2x width of antennal socket including rim. Head in posterior view with weak coriaceous sculpture and sparse setae around external edges (Fig. 5B). Gula short; distance between occipital foramen and oral foramen as long as the height of the occipital foramen. Posterior tentorial pits clearly visible, buttonhole-like; hypostomal sulci visible, converging and slightly separated at the oral foramen.

Mouthparts (Fig. 5B). Mandibles partially exposed in anterior view of head; right mandible with three teeth; left with two teeth. Cardo of maxilla hardly visible, maxillary stipes about as long as broad. Maxillary palp five-segmented. Labial palp with two visible segments.

Antenna 0.6x as long as body; with 13-14 segments (13 and 14 sometimes incompletely divided) (Fig. 5C); flagellum slightly broadening towards apex; with erect setae and placodeal sensilla visible on flagellar segments F2–F12, arranged in one row of 1-3 sensillae on each flagellomere. Relative length/width of antennal segments: 20/9:15/10:26/6:22/7:17/8: 17/8:16/8:15/9:15/9:16/9:14/9:15/9:14/9:11/7. Pedicel 1.5x as long as broad; F1 1.2x as long as F2. Last flagellomere 1.5x as long as broad, 0.8x as long as F11.

Mesosoma short; in dorsal view (Fig. 5E) 1.4x as long as broad, slightly longer than high in lateral view and with dorsal margin convex. Pronotum medially very short, without pronotal plate, laterally with alutaceous sculpture, with some setae dorsally and some longitudinal rugae at posterior margin (Fig. 6A). Mesoscutum (Fig. 5E) with weak coriaceous-alutaceous sculpture; medially, towards transcutal fissure, some longitudinal rugae visible jointly with a few long setae. Notauli traceable but indistinct, not marked, without clear limits. Median mesoscutal impression almost invisible. Anteroadmedian signa scarcely visible; parascutal impressions not visible. Transscutal fissure absent, marked as a deep depression without clear limits between posterior margin of mesoscutum and posterior margins of scutellar foveae. Scutellar foveae united into a smooth and shining broad depression only limited by a posterior margin. (Fig. 5E). Mesoscutellum oval, flat, with outer raised margins, almost smooth and scarcely pubescent. Mesopleuron (Fig. 6A) with visible coriaceous sculpture and almost glabrous. An interrupted line marking ventral margin of mesopleural triangle visible.

Metapectal-propodeal complex. Metapleural sulcus meeting posterior margin of mesopectus at middle point, relative to the posterior subalar pit. Metascutellum with rugose sculpture; metanotal trough smooth and glabrous. Propodeum almost smooth; lateral propodeal carinae absent; medial carine present, which is branched anteriorly and subdivided posteriorly in several short longitudinal carinae (Fig. 5F). Median propodeal area smooth and pubescent on the sides. Nucha dorsally with longitudinal ridges.

Legs. Metatarsal claw (Fig. 6D) simple, without secondary basal lobe or tooth.

Forewing (Fig. 7H). 1.3x as long as body; conspicuously setose. Radial cell 4.3x as long as broad, open along anterior margin; R1 and Rs reaching anterior margin of wing; R1 oriented obliquely to anterior margin of wing. Rs slightly expanded at apex; Rs+M distinct, reaching basalis slightly below middle part of its height. Medial and cubital veins visible; areolet large, triangular. Basal cell with some setae; costal cell heavily setose. Apical margin of wing with a fringe of long setae.

Metasoma (Fig. 6B). Slightly shorter than head + mesosoma. T2 0.4x as long as metasoma. Metasomal tergites glabrous, smooth and shining. Projecting part of hypopygial spine short (Fig. 6C); approximately 2x as long as high; hypopygial spine with some long erect setae in ventral view, the apical ones overlapping apex of spine.

Male. Similar to female in coloration and the majority of morphological characters. Differs from female as follows: Antennae with 14 clearly separate segments; F12 as long as F11. Mesoscutum without alutaceous sculpture, smooth and shining.

Distribution. The collecting site of the type material of this new species is located in the tropical montane cloud forests of the Cordillera of Talamanca in Costa Rica at an altitude above 2,500 m (Fig. 9B). The host tree, Quercus bumelioides Liebm. (=Q. copeyensis CH Mull.), is dominant in the cloud forest of this region of Costa Rica (Kappelle, 1996). The host tree is also distributed in other areas of Central America and southern Mexico, a large area that represents the potential distribution of their associated gall wasps. The new species is the first oak gall wasp (Cynipini) of the genus Neuroterus described from Costa Rica.

Gall (Figs. 9C-F). The galls develop inside acorns. They form a cluster of aggregated and joined chambers within the cotyledons and wall of the acorn. Individual galls consist of an oval larval cell surrounded by tissue that is pointed at the apex. Individual galls are grouped radially, appearing as orange segments. Affected acorns do not develop normally and remain stunted inside the acorn cup. Mature galls have woody, hard walls. The galled acorns measure 7 to 14 mm.

Etymology. Named after the acorn gall induced by this species.

Biology. Sexual generation. The adults emerged from the galls in the laboratory a few days after being collected, in early January. The asexual generation is unknown. One damaged female, presumably asexual according its morphology, was collected from different small galls in the acorn cup, which may be the alternating form of N. glandiphilus, but this hypothesis must be confirmed with additional collected galls and reared adult insects.

Melika et al. (2010) proposed the current accepted generic circumscription and limits of Neuroterus. However, the phylogenetic relationships and generic limits between Neuroterus and closely related genera, especially the new related genera, the Oriental Cycloneuroterus and the Nearctic species of Neuroterus remain uncertain and thus require more thorough phylogenetic studies.

The Nearctic species of Neuroterus have not been revised since Kinsey (1923). Tang et al. (2011) presented a combination of morphological characters that do not fit the concept of the genus Neuroterus defined by Melika et al. (2010), concluding that the taxonomic status of many Nearctic species is unclear and needing thorough revision. Pujade-Villar et al. (2015) argued that Nearctic Neuroterus is a polyphyletic group as currently defined and suggested that new genera will be established. However, there are no phylogenetic studies to support this hypothesis. Beyond speculation, there is an urgent need for a complete revision of Neuroterus and related genera, including the Nearctic and Neotropical species.

The new species described here present some important morphological diagnostic characters that do not fit with those defining Neuroterus given by Melika et al. (2010). The anomalous characters are mainly the simple tarsal claws, antenna with 11/12 flagellomeres and the sculpture of propodeum. However, we describe the species within the old concept of Neuroterus sensu Kinsey 1923, until the uncertainties about the placement of the American species of Neuroterus are resolved in a comprehensive revision of all the included species.

In this paper, the genus Neuroterus is recorded in Central America and so from the Neotropical Region for the first time. Along with the three new species described here, we found evidence of at least six distinctive galls with cynipid gall inducers, which likely represent additional new undescribed species (Fig. 10). We do not describe these species here, however, because of the incompleteness of the studied material. Regardless, the available evidence clearly shows that a rich fauna of Neuroterus species exists in the tropical montane oak forests of Central America, estimated at approximately 10-20 species (Medianero & Nieves-Aldrey, unp.). With more than 10 Quercus species as potential hosts, further studies and field work are necessary to reveal their undescribed associated cynipid fauna, not only of Neuroterus but also of other oak gall wasp (Cynipini) genera. South of Panama, there is still a possibility of finding the genus in Colombia, but no species of Neuroterus have been found in Colombia despite some field work in recent years. In comparison, only nine Neuroterus species have been described from Mexico (Kinsey, 1938; Pujade-Villar et al., 2015, 2016), a comparatively low number, surely reflecting poor sampling considering the 161 species of Quercus recorded from México, including 109 endemic species (Valencia-A, 2004), with presence of many species of white oaks that are their potential hosts.

HOST PLANT ASSOCIATIONS

The three new species described here induce galls on Quercus bumelioides and less frequently on Q. lancifolia, two species of white oaks belonging to the Quercus section of Quercus (Govaerts & Frodin, 1998). These results do not contradict the host association of most Nearctic species of Neuroterus, which are strictly confined to “white oaks” according to Kinsey (1923), with the exception of a more recently described species, N. chrysolepis Lyon, 1984, which is associated with the Protobalanus group of Quercus (Melika & Abrahamson, 1997). We did not find galls of Neuroterus species on Quercus salicifolia (section Lobatae, red oaks) sampled in Panama.

With regard to life cycles of the new species, two correspond to sexual generations, while the third is described from the asexual generation. However, we found circumstantial evidence in N. elvisi and N. glandiphilus indicating that they likely have alternating generations on the same host Quercus species and thus have heterogonic life cycles. Kinsey (1923) observed that the Nearctic species of Neuroterus included in the subgenus Dolichostrophus had largely identical alternating generations. According Tang et al. (2011), of the 59 species of Nearctic Neuroterus, 30 species are known only from their sexual generation, and the connection between the asexual and sexual generation has been established experimentally in only three species.