Novelties from a cave lace bug (Heteroptera, Tingidae): first nymphal description with a discussion on the morphological patterns of Vianaidinae immatures

A nymph of Thaumamannia Drake & Davis, 1960, a rare vianaidine genus known only from adults, is described by the first time. The specimens were collected in the soil and walls of caves located in the state of Pará, Brazil. This is the first record of Vianaidinae for Brazil. The T. vanderdrifti fifth instar is compared with the same stadium of Anommatocoris coleopteratus (Kormilev, 1955), the only other vianaidine nymph described so far, and patterns between them and within the family are also discussed.

Thaumamannia vanderdrifti Doesburg, 1977 was described from specimens found in soil samples (DoeSburG, 1977).To our knowledge, this was the only sample of T. vanderdrifti obtained thus far.It differs from its congener by the pronotum, deeply punctuate and posteriorly rounded; costal area narrower anteriorly, longer carina-like vein elevation on the hemelytra; and by the lateral branch of metasternal scent gland, extending far beyond the hemelytra (Drake & DaviS, 1960;DoeSburG, 1977).Besides the description of both genres for this species, no information regarding the immatures was provided.The species was well-illustrated despite some incongruences between the illustrations and description (DoeSburG, 1977).In addition, there is no information about the nymphs of T. manni as well.
Tingidae immatures, specially nymphs, were recently target of evolutionary studies and phylogenetic analyses (Guilbert, 2004;Guilbert et al., 2008).It is believed that the remarkable morphology of the exaggerated outgrowths of some lace bugs nymphs has evolved from simple to complex in a similar pattern observed in the adult morphology (Guilbert, 2004).Regardless the importance of immature descriptions, contributions about this life stage in Tingidae are not very common, especially when all the stadia are considered (GuiDoti & barcelloS, 2013).The only vianaidine with immatures described so far is Anommatocoris coleopteratus (Kormilev, 1955).However, only the fifth nymph was described for this species, although measurements are available for third and fourth stadia.An illustration of A. coleopteratus fifth stadium is also available (Drake & DaviS, 1960).
We described here the fifth instar of Thaumamannia discussing its morphology within the family.Hypotheses regarding adaptative traits are proposed.In addition, the first record of the subfamily for Brazil is presented.This constitutes the first nymphal description for Vianadinae illustrated with SEM images.Collection and preservation.Specimens were collected during 2010 and 2011 and are deposited in the Zoology Collection, Seção de Invertebrados Subterrâneos (ISLA) at the Universidade Federal de Lavras (UFLA), Campus Universitário de Lavras, Minas Gerais, Brazil.Specimens were visualized throughout the floors and walls of the caves (Figs 2,3), captured with a fine brush and placed into vials with 70% ethanol.Special attention was also paid to decaying vegetation (e.g., leaves and tree bark) and animal carcasses, although this material was only common near the cave entrances.Fourty-seven individuals were observed (although just a few were collected: three fifth stadium nymphs and three adult males) in 22 caves -GEM-117, GEM-1195, GEM-1645, GEM-1646, GEM-1694, GEM-1701, GEM-1707, GEM-1709, GEM-1717, GEM-1719, GEM-1721, GEM-1727, GEM-1734, GEM-1735, GEM-1744, GEM-1753, GEM-1755, GEM-1757, GEM-1760, GEM-1770, GEM-1789, GEM-1799).Specimens treatment.Photographs were taken with a digital camera attached to a microscope.Specimens were dried with critical point and gold coated for SEM analysis.Measurements were obtained from three specimens with a measuring reticle attached to the eyepiece, here presented in millimeters as mean (minimum -maximum).The body width was measured at the middle line of pronotum.The terminology followed Guilbert (2005).
Head sligthly longer than wide.Eyes prominent, bearing about three omatidia.Clypeus well developed, much longer than juga.Lateral margins of juga convex, slightly angled near apices; these rounded.Antenniferous tubercles well developed.Antennal segments pubescent, increasing  in length towards fourth; scape about half of the pedicel, not surpassing apex of head; pedicel, basiflagellomere and distiflagellomere slightly different in size.Rostrum almost reaching posterior margin of third urosternite.
Pronotum about three times wider than long; anterior and lateral margins convex; posterior margin sub-rectilinear.Lateral margins bearing scale-like integumentary projections (Fig. 7).Small rounded granular projections distributed throughout pro-and mesonotum.Pronotal scars darker and depressed.Wing pads reaching the limit between third and fourth urotergite.Metanotum small, almost half the width of first urotergite; similar in aspect to the abdominal tergites.Legs pubescent; longer hairs scattered among shorter ones along outer margin; coxae conical, projected ventrally.Tibial combs (Fig. 8) present in all legs.First tarsomere very short, about one fourth the length of the second.Claws well-developed.Spiracles present on pro-and mesopleura.A scar present in metapleura, in the same region of the adult metathoracic gland.Pro-and mesopleura bearing the same small rounded granular projections than the pro-and mesonotos, these absent in metapleura.
Nine shiny, strongly esclerotized urotergites visible; intersegmental membrane bearing transversal lines composed by small rounded granular projections (Fig. 9).Lateral margins with integumentary projections as those of the thorax.Scent glands openings present laterally in the posterior region of fourth urotergite, followed by a large evaporatory area free of projections (Fig. 10).Connexivum well delimited dorsally.Ventrally, nine segments are distinguished.Spiracles visible on sternites II-VIII.

DISCUSSION
The caves where the specimens were collected are associated to the superficial ferruginous breccia (canga formation).Although considered "macro" caves, most of those cavities are small, with sizes varying from 8 meters (GEM 117) to 204 meters (GEM 1727) (mean±SD corresponding to 70.38±55.28m).However, all of those caves are connected to a large network of small channels (canaliculi), typically found in the canga formation, which considerably increases the habitats for the subterranean fauna in iron ore caves (Souza-Silva et al., 2011).Accordingly, it is possible that specimens migrate between caves by sub-superficial voids.The position of specimens inside each cave was quite variable.In some caves, individuals were found near the entrance while in others in deeper areas.It suggests a lack of preference for specific conditions of temperature, light and moisture inside the caves.This could be also supported by the fact that these caves possess distinct morphologies and dimensions, so those factors seem not to be relevant to determine species preferences.Individuals were found under fallen rocks on the floor or associated to roots aggregations that grow in different parts of the caves.Most of the specimens (32 from 47) were observed in the dry season, what could indicate that the association to caves is eventually related to a search for moist habitats.Unfortunately, no interactions were observed between T. vanderdrifti and any other species.
Considering Tingidae nymphal morphology, the fifth instar here described shares several traits with the other vianaidine nymph known thus far.However, the brief description available for the A. coleopteratus nymph (Kormilev, 1955), and the only illustration provided (Drake & DaviS, 1960), hamper the comparison between these species.The absence of detailed and illustrated descriptions plays a major role as an impediment for further comparisons and establishment of homology hypotheses on Tingidae immatures (GuiDoti & barcelloS, 2013).Nevertheless, the position of the scent glands opening, the scape not surpassing the apex of clypeus and the absence of cephalic, abdominal and thoracic (both lateral and dorsal) tubercles are the most remarkable features presented by both T. vanderdrifti and A. coleopteratus nymphs.Although there are some genera within Tingidae which have nymphs without any tubercle (e. g., Atheas insignis Heidmann, 1909 -Guilbert, 2005) and some with short scape (Dictyonota strichnocera Fieber, 1844 -Guilbert, 2004), the position of the scent gland opening seems to be an unique character for vianaidines within Tingidae.
The exaggerated outgrowths of Tingidae nymphs, such as the lateral and dorsal tubercles aforementioned, are associated with chemical communication and chemical and physical protection (livinGStone, 1976;alDrich et al., 1991;MaSon et al., 1991).The habitat of T. vanderdrifti, as well as of all coleopteroid species of Vianaidinae, justifies the barely developed compound eyes of both nymphs and adults.The lack of the visual perception of their surroundings could be a positive pressure for a complex scenario of chemical communication.Thereby, the absence of those tubercles is interesting.The body colour, similar to the cave soil, may be an effective camouflage strategy that meets the species needs regarding predation protection.In addition, the uncommon large evaporatory area for Tingidae nymphs could be associated with potentialized effectivity of the abdominal scent glands products (Schuh & Slater, 1995).Therefore, the lack of the protective properties of the exaggerated outgrowths absent in this nymph could be supplied by the body camouflage and a higher scent gland activity.These hypotheses are based exclusively in the morphology here described, and thus, deserve further supporting.
More data on Tingidae immatures, particularly on vianaidines, are very important to the understanding of morphological patterns here highlighted, as well as for phylogenetic analyses on the evolutionary trends and relationships among the family taxa.Well-illustrated contributions may provide enough data for further and more comprehensive studies.The knowledge on all nymphal stadia could bring important informations on the ontogenetic steps of species development, and these can reveal new homologies between vianaidines and within lace bugs.
area.The caves in which the specimens were observed are located in two interconnected ferruginous DOI: http://dx.doi.org/10.1590/1678-47662014104199103outcrops situated in Parauapebas municipality (state of Pará, northern Brazil; Fig. 1).Such outcrops are inserted in a protected area (Floresta Nacional de Carajás), although they are threatened by mineral exploitation (for the extraction of iron ore).