Introduction

Emerson (1925) described Crepititermes as a Neotropical termitine subgenus of Mirotermes Holmgren and diagnosed the small species Mirotermes (Crepititermes) verruculosus, based on external morphological characters of the imago and soldier castes from six colonies collected at Kartabo, Guyana, but he provided no remarks on field notes or biology. Snyder (1949) recognized the generic status of Crepititermes, and Mathews (1977) improved the generic diagnoses of the alate and soldier castes, establishing Crepititermes verruculosus Emerson as the type species by monotypy, recording C. verruculosus inside the nests of Cornitermes bequaerti Emerson, Cornitermes snyderi Emerson, and Silvestritermes euamignathus (Silvestri) in the “Serra do Roncador,” Mato Grosso, Brasil. Thereafter, the known geographical range of C. verruculosus was expanded by several recent records (Davies 2002, Bourguignon et al 2011, Palin et al 2011, Cancello et al 2014).

Based on a reexamination of specimens of Crepititermes deposited in the Museu de Zoologia da Universidade de São Paulo, São Paulo, Brasil (MZUSP), we describe the gut morphology and coiling in situ of the workers for the first time. We provide additional notes on the imago and soldier and present digital images and illustrations for all castes. We also update the currently known geographical distribution of the species, based on records from different collections of Isoptera, adding some biological notes.

Material and Methods

Biological material

All the specimens examined are housed in the Museu de Zoologia da Universidade de São Paulo, São Paulo, Brasil (MZUSP). The list of material examined is sorted by country (uppercase), state or province (italics), and locality. Collection data are listed as date, name of the collector, and lot number (in parentheses); an asterisk after the lot number indicates samples with imagoes. We also examined imagoes, soldiers, and workers of the following Neotropical termitine type species, which are part of the Termes group (Krishna et al 2013) for comparison: Cavitermes tuberosus (Emerson), MZUSP-12224; Cornicapritermes mucronatus Emerson, MZUSP-8815; Dihoplotermes inusitatus Araujo, MZUSP-16448; Divinotermes tuberculatus Carrijo & Cancello, MZUSP-12683; Genuotermes spinifer Emerson, MZUSP-8383; Inquilitermes fur (Silvestri), MZUSP-2062; Neocapritermes opacus (Hagen), MZUSP-3126, 7891; Planicapritermes planiceps (Emerson), MZUSP-7413; Termes fatalis Linnaeus, MZUSP-3790. The alates of the type species of Orthognathotermes Holmgren and Dentispicotermes Emerson, both genera that are also assigned to the Termes group, have not yet been described; instead, we used Dentispicotermes brevicarinatus (Emerson), MZUSP-8815 and Orthognathotermes insignis, MZUSP-3272.

Descriptive terminology and morphometric characters

We use the terminology of Fontes (1987) to describe worker mandibles and that of Noirot (2001) for the different parts of the digestive tube of workers. We took measurements with a micrometric reticle in the eyepiece of a Leica M125 stereomicroscope of the following morphometric characters (Roonwal 1970): for imagoes, LH, length of head capsule (9); WH, width of head capsule without eyes (18); DE, diameter of eye (48); LO, length of ocellus (55); WO, width of ocellus (56); EOD, eye-ocellus distance (57); LP, length of pronotum (65); WP, width of pronotum (68); and LT, length of hind tibia (85); for soldiers, LH, length of head capsule (9); WH, width of head capsule (18); HH, height of head excluding postmentum (21); WP, width of pronotum (68); LT, length of hind tibia (85).

Drawings and digital images

We drew the coiled gut in situ of the workers of C. verruculosus with a camera lucida, took the photographs of the imago and soldier castes with a digital camera coupled to a stereomicroscope at different focal points, and merged the sequences of images with the software Leica Application Suite V3.Ink®. The foregut and the enteric valve of the worker caste were mounted on a slide with glycerin and photographed under an optical microscope. We mapped the distribution with the records of the specimens examined in the MZUSP and included records of specimens housed at the Museu Paraense Emílio Goeldi, Belém, Pará, Brasil (MPEG); Departamento de Zoologia, Universidade de Brasília, DF, Brasil (UnB); Laboratório de Termitologia, Universidade Federal da Paraíba, João Pessoa, Paraíba, Brasil (UFPB); and University of Florida Termite collection, Fort Lauderdale Research and Education Center, Davie, Florida, USA (UF).

Taxonomic treatment

Genus Crepititermes Emerson

Mirotermes (Crepititermes) Emerson 1925: 433; Crepititermes, Snyder 1949:177; Crepititermes, Mathews 1977: 133; Crepititermes, Krishna et al 2013: 2086 (catalog).

Type species. Mirotermes (Crepititermes) verruculosus Emerson 1925 by monotypy.

Type locality. Guyana: Kartabo.

Distribution (Fig 1). Neotropical region (Bolivia, Brasil, Ecuador, French Guiana, Guyana, Paraguay, Peru, and Trinidad and Tobago).

Fig 1
figure 1

Current known distribution of Crepititermes verruculosus.

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Diagnosis. The imago is distinguished from other Neotropical Termitinae genera by the following combination of characters: head capsule surface concave in profile, fontanelle area not depressed; postclypeus rather flat in profile; right mandible with the third marginal tooth very reduced to absent (not visible); left mandible with the second marginal tooth absent (not visible); eyes medium-sized and smaller ocelli; pronotum slightly wider than long; posterior margin of the mesonotum and metanotum slightly emarginate, and posterior corners close to each other; pronotum partially overlapping the base of the fore wing pair. The soldier is distinguished by the subrectangular head capsule with a flat forehead, without projection in dorsal view, and symmetrical snapping mandibles. The worker has a unique enteric valve ornamentation; the distal paunch with a conspicuous pear-shaped diverticulum displaced laterally to the right, and the very short mesenteric tongue and short and tubular ileum; the same mandibular pattern as the imago but broader molar areas. For the soldiers and workers examined, we observed that their bodies rupture through a weak area between the metanotum and the first abdominal tergite, resulting in protrusion of at least part of the paunch and the pear-shaped diverticulum.

Remarks. Emerson (1925), Snyder (1949) and Mathews (1977) included Crepititermes as part of the non-monophyletic subfamily Termitinae. Following Krishna et al (2013), we compared Crepititermes with other Neotropical genera of the Termes group. Crepititermes has not appeared as a terminal taxon in any phylogenetic scheme.

Crepititermes verruculosus Emerson (Figs 1–19)

Crepititermes verruculosus Emerson 1925: 433, Fig 84a-d; Davies 2002:241 (checklist, feeding group); Costa et al 2009:449 (nesting); Ackerman et al 2007:271 (checklist, nesting); Constantino & Schmidt 2010:201 (checklist); Bourguignon et al 2011:264, 265 (checklist, feeding group); Palin et al 2011:3, supporting information (checklist, feeding group); Krishna et al 2013: 2087 (catalog); Kutalová et al 2013:340, 342, Fig 3C (imagoes frontal gland); Cancello et al 2014:6, supporting information (checklist, feeding group).

Description of worker and additional notes on imago and soldier castes

Imago (Figs 2–4). Vide Emerson (1925:434), Mathews (1977:134) and Roonwal & Verma (1980:462). Range of measurements (mm) of six females (two each from MZUSP 3521, 21231, and 21216) and three males (one from MZUSP 3521 and two from 21216): LH, 0.50–0.53; WH, 0.48–0.50; DE, 0.17–0.20; WO, 0.06–0.09; EOD, 0.03–0.05; LP, 0.44–0.47; WP, 0.53–0.59; LT, 0.59–0.66. No apparent dimorphism in characters or size between female and male. Among all the specimens studied, those from Rondônia, Brasil, are darker colored, with larger eyes and ocelli (Figs 2–4) than those from Guyana.

Figs 2–4
figure 2

Crepititermes verruculosus, female: 2 head capsule and pronotum in profile, 3 head capsule in dorsal view, and 4 thoracic nota in dorsal view.

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Comparisons. Crepititermes tuberosus (see Emerson 1925: Figs 88a, b, p 443) resembles C. verruculosus in having an arched postclypeus; the head capsule slightly concave in profile; a different thoracic nota shape; tibial spurs; but differs in having the same mandibular dentition and molar area pattern (left M3 very reduced but not obsolete), the fontanelle tiny and barely depressed, and number of antennal articles as C. verruculosus. Dihoplotermes inusitatus (see Krishna 1968: Fig 38, 311) has different mandibular dentition and molar area, as well as pronotum shape, but shares with C. verruculosus a slightly arched postclypeus, size of the eyes and ocelli, and the tiny rounded fontanelle. Divinotermes tuberculatus (see Carrijo & Cancello 2011: Figs 1C, D, p 540) differs from C. verruculosus in the arched postclypeus; head capsule slightly concave in profile; different thoracic nota shape; tibial spurs; but has the same mandibular dentition and molar area pattern (left M3 very reduced but not obsolete); fontanelle tiny but not depressed; and number of antennal articles. Dentispicotermes brevicarinatus (see Emerson 1950: Fig 3, p 7) has different mandibles with the posterior margin of the apical teeth not concave, the left M3 and right M2 well visible, and the molar tooth visible as well between the molar plate and left M3; head capsule surface not concave in profile; fontanelle conspicuous in dorsal view, depressed in profile; postclypeus arched; number of antennal articles; thoracic nota shape; and tibial spurs. Genuotermes spinifer (see Rocha 2013: Figs 3–5, p 110) has different mandibles with the posterior margin of the apical teeth not concave, left M3 reduced but visible, gap between molar plate and M3 filled by molar tooth, right M2 conspicuous; fontanelle conspicuous and depressed in dorsal view, postclypeus arched; number of antennal articles; thoracic nota shape; and tibial spurs. Inquilitermes fur (see Mathews 1977: Fig 81, p 136) has the left mandible with M3 reduced but visible, fontanelle conspicuous in dorsal view, slightly depressed in profile; head capsule surface not concave in profile; postclypeus arched; number of antennal articles; mesonotum and metanotum more emarginate, posterior corners not close together, and tibial spurs; but I. fur also has mandibles with the apical tooth very prominent and the posterior margin concave and the right M2 absent and a similar pronotum shape as C. verruculosus. Neocapritermes opacus (see Krishna 1968: Fig 42, p 315) has different mandibles, with the apical teeth not more prominent than the marginal dentition, the left M3 and right M2 well visible, posterior margin of the right M2 not concave; head capsule surface not concave in profile; fontanelle conspicuous in dorsal view, slightly depressed in profile; postclypeus arched; number of antennal articles; thoracic nota shape; and tibial spurs. Orthognathotermes insignis (see Rocha & Cancello 2009: Fig 20, p 19) has different mandibles, with the left M3 and right M2 reduced but well visible, left M1 + 2 connected with M3 by a sinuous margin; fontanelle conspicuous in dorsal view, depressed in profile; head capsule surface not concave in profile; postclypeus arched; number of antennal articles; thoracic nota shape; and tibial spurs. Planicapritermes planiceps (see Mathews 1977: Fig 82, p 136) has different mandibles, with the apical teeth not more prominent than the marginal dentition, left M3 and right M2 well visible, posterior margin of right M2 not concave, thoracic nota shape, and tibial spurs; however, P. planiceps has the same number of antennal articles; head capsule surface concave in profile; postclypeus not arched, as in C. verruculosus. Termes fatalis has different mandibles, with the apical teeth not as prominent and the posterior margin concave, right M2 and left M3 reduced but visible; fontanelle conspicuous, not depressed; larger eyes and ocelli; and postclypeus arched; although T. fatalis has the same number of antennal articles; head capsule concave in profile; thoracic nota shape; and tibial spurs as in C. verruculosus. Cornicapritermes mucronatus has no alate described.

Figs 5–7
figure 3

Crepititermes verruculosus, soldier: 5 dorsal, 6 profile, and 7 ventral view, showing molar plate and prominence in detail.

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Soldier (Figs 5–7). Vide Emerson (1925:434) and Mathews (1977:134). Head capsule covered with erect hairs and very short hairs, only short hairs on front. Postclypeus with scattered erect bristles and short hairs. Labrum with long decumbent bristles plus few short hairs. Pronotum with anterior lobe slightly emarginate, scattered erect bristles on margins, and very short hairs over surface. Tergites densely covered with erect hairs, IX and X tergites with scattered long erect bristles on posterior margin. Sternites densely covered with decumbent hairs and some long erect bristles on posterior margin. Anterior face of procoxa with discrete hump and few short hairs over surface. Tibial spurs 3:4:2. Range of measurements (mm) for one soldier from each of MZUSP lots 12222, 22708, 3522, two soldiers from MZUSP 6589, 9481; three soldiers from MZUSP 12601: LH, 0.91–0.94; WH, 0.58–0.63; HH, 0.47–0.53; WP, 0.34–0.38; LT, 0.41–0.47.

Comparisons. No other Neotropical termitine genera have the combined characters of symmetrical snapping mandibles and no frontal projection.

Worker (Figs 8–19). Head capsule rounded, with fontanelle region inconspicuous in dorsal view. Postclypeus arched and fontanelle region slightly depressed in profile. Antenna with 13 articles. Anterior lobe of pronotum more developed than posterior lobe; anterior margin of pronotum slightly emarginate. Anterior face of procoxa with discrete hump. Tibial spurs 3:4:2. Head capsule covered with abundant erect hairs. Postclypeus with short hairs over surface and erect bristles on anterior margin. Labrum with decumbent bristles larger than those of postclypeus. Thoracic nota and abdomen with similar pilosity to soldier. Body pale yellow overall. Mandibles (Fig 8). Apical teeth acute and more prominent than first marginal teeth; posterior margin of apical teeth concave, forming acute angle with anterior margin of first marginal teeth. Left mandible: M1 + 2 tooth conspicuous, its posterior margin slightly sinuous; third marginal tooth absent (not visible); apex of molar tooth beneath molar prominence; molar prominence concave without ridges. Right mandible: first marginal tooth conspicuous; second marginal tooth absent (not visible); molar plate concave, without ridges; and a broad basal notch. Digestive tube (Figs 9–19). Coiled gut in situ visible through abdominal wall as in Figs 9–12. Crop slightly more developed than gizzard (Fig 11); crop cuticle armed with pectinate scales. Gizzard with completely sclerotized cuticular armature (hexaradial symmetry); pulvillar belt more developed than columnar belt, pulvillus I more developed than pulvillus II, both with their entire surface smooth, with no apparent ornamentations (Fig 15); columns I and II, also with the entire surface smooth (Fig 15). Mesenteron passing through right side of abdomen to join the ileum (P1), reaching just before medial line in ventral view (Fig 11). Very short mixed segment external to mesenteric arc, with lateral margins converging distally (Fig 13). Malpighian tubules arranged in two closely set pairs but attached individually at mesenteron-proctodeum junction on inner face of mesenteric arc; tubules slightly dilated at attachment point (Fig 14). P1 tubular, about half as long as abdomen; P1 cuticle with triradial symmetry (Fig 18), three recognizable cushions, each one armed with cluster of several rows of three to five aciculiform spines (Fig 18), distally, cushions unarmed but with crenate appearance. Enteric valve (P2) in ventral view at right side of abdomen (Fig 11); P2 cuticle with triradial symmetry (Fig 17), armed with one asymmetrical ring of major cushions alternating with slightly shorter ones; both cushions with small subtriangular spines on proximal region, followed by crenulated area and ending in cluster of larger subtriangular spines in curved line, bending in the direction of the food-flux distal surface (Figs 16, 17). Paunch (P3) with proximal region very enlarged, displaced to left side of body; distal part of P3 voluminous, protruding through mesenteric arc with a noticeable pear-shaped diverticulum, right-laterally displaced; diverticulum not visible in unopened abdomen; isthmus relatively short and conspicuous. Dorsal torsion well developed. “U-turn” tubular, not dilated. Distal colon tubular, joining the rectum in dorsal view.

Figs 8–14
figure 4

Crepititermes verruculosus, worker: 8 mandibles; coiling gut in 9 dorsal 10 right, 11 ventral, and 12 left view; 13 mixed segment in detail; and 14 Malpighian tubules in detail. C crop, D diverticulum, P1 ileum, P2 enteric valve, P3 paunch, P4 colon, and P5 rectum.

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Figs 15–17
figure 5

Crepititermes verruculosus, worker: 15 gizzard in plain view; 16 major cushion of the enteric valve in detail, and 17 cushions in plain view. Arrow shows the food flow (P1–P3).

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Figs 18–19
figure 6

Crepititermes verruculosus, worker: 18 sketch and 19 photograph of the ornamented cuticle of the ileum. Arrow shows the food flow (P1–P3).

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Comparisons. No other Neotropical termitine genera has the enteric valve ornamentation, the distal paunch with a conspicuous pear-shaped diverticulum displaced laterally to the right, and coiled gut described for Crepititermes, neither the African Termitinae genera (Sands 1998) nor the Australian species of the Termes-Capritermes complex (Miller 1991). Nevertheless, the coiled gut in situ resembles that of the nasute genus Subulitermes Holmgren.

Material examined. Paratype. GUYANA. Kartabo, 21.vi.1919, A.E. Emerson, one soldier (3522). Other material. GUYANA. Kartabo, 9.iv.1924, A.E. Emerson (3521*). BRASIL. Amazonas: Manaus, BR 174 Km 45, 15.viii.1990, A.G. Bandeira (9481). Bahia: Ilhéus, Mata Esperança, 23.v.2001, Y. Reis (12222); Porto Seguro, ESPAB, 22.i.2003, Y. Reis (12221). Goiás: Mineiros, Mata farm, 25.vii.2011, T.F. Carrijo (22434); Niquelândia, 16.xi.2013, T.F. Carrijo (22707). Mato Grosso: Chapada dos Guimarães, Chapada dos Guimarães National Park, 11.ii.1976, R.L. Araujo (6589, 6749), 1-5.viii.2009, T.F. Carrijo (12601, 12609, 12625); Cláudia, 13.x.2010, Q.C.L. Santos (15928), 25.viii.2011 (15957); Confresa, Parque do Xingu, 2.xi-11.xii.1973, G.R. Kloss (5304); Cuiabá, 7 km NO, 16.ii.1976, R.L. Araujo (6540). Minas Gerais: Chapada Gaúcha, Grande Sertão Veredas National Park, 12.x.2012, M.M. Rocha (16149, 16191), T.F. Carrijo (22785); Jaboticatubas, Serra do Cipó National Park, 7.x.1012, M.M. Rocha (16266), T.F. Carrijo (22783, 22784); Sete Lagoas, 13.ii.1986, D.J. Domingos (8973). Pará: Abel Figueiredo, Juca Marhe farm, 27.xi.2013, T.F. Carrijo (22708). Rondônia: Porto Velho, District of Abunã, Jirau Hydroelectric Reservoir, 17.ix.2010, M.M. Rocha and V.T.C. Mercado (21193, 21194*), 15.v.2010, T.F. Carrijo and M.M. Rocha (21186), 09.iii.2010, T.F. Carrijo and R.G. Santos (12881), 30.vi.2010, T.F. Carrijo and S.P. Rosa (21189*), 27.vi.2011, S.P. Rosa and G.R. Mazão (21220), 11-12.ix.2011, T.F. Carrijo and L.R. Fernandes (21224, 21223), 08.iv.2011, V.T.C. Mercado and R.S. Probst (21214), 05.iv.2012, M.M. Rocha and R.G. Santos (21231*, 21232*), 27.vi.2012, R.G. Santos and K. Kawamishi (21238), 13.ix.2012, T.F. Carrijo and R.G. Santos (21239, 21240, 1241, 21242) District of Fortaleza do Abunã, Jirau Hydroelectric Reservoir, 11.iii.2010, T.F. Carrijo and R.G. Santos (12882, 12883), 28.vi.2010, T.F. Carrijo and S.P. Rosa (21190), 6.iv.2011, V.T.C. Mercado and R.S. Probst (21215, 21216*), 09.ix.2011, T.F. Carrijo and L.R. Fernandes (21225, 21226), District of Jaci Paraná, Santo Antônio Hydroelectric Reservoir, 13-20.ix.2010, T.F. Carrijo and R.G. Santos (21252, 21253, 21254, 21255), 03-13.vi.2011, M.M. Rocha and J. Cabral (21260, 21261), 24.xi.2011, M.M. Rocha and J. Cabral (21262, 21263, 21264), 02-06.vi.2012, M.M. Rocha and J. Cabral (21268, 21269), District of Mutum Paraná, Santo Antônio Hydroelectric Reservoir, 01-05.iii.2010, T.F. Carrijo and R.G. Santos (12885, 12886, 12884*, 12887, 12888, 12889, 12890), 11.ix.2010, M.M. Rocha and V.T.C. Mercado (21196), 11.v.2010, T.F. Carrijo and M.M. Rocha (21187, 21188), 12-16.ix.2010, M.M. Rocha and V.T.C. Mercado (21195, 21197, 21201, 21202, 21198, 21199, 21200), 23-25.vi.2010, T.F. Carrijo and S.P. Rosa (21192, 21191), 05-12.i.2011, M.M. Rocha and L.P. Prado (21203, 21207, 21204, 21205, 21206, 21208, 21210, 21209*, 21211*, 21212, 21213), 14-18.ix.2011, T.F. Carrijo and L.R. Fernandes (21230, 21229, 21227, 21228), S.P. Rosa and G.R. Mazão (21221, 21222), 28-30.iii.2011, V.T.C. Mercado and R.S. Probst (21217, 21218, 21219), 08-10.ix.2012, T.F. Carrijo and R.G. Santos (21247, 21248, 21243, 21244, 21245, 21246), 29-30.iii.2012, M.M. Rocha and R.G. Santos (21233, 21234, 21235, 21236, 21237, 05-08.v.2013, F. Andriolli and P. Manholer (21251, 21249, 21250), District of Porto Velho, Santo Antônio Hydroelectric Reservoir, 19-22.ix.2010, T.F. Carrijo and R.G. Santos (21256, 21257), 06.iv.2011, R.G. Santos and C.Y. Mandai (21259), 19.i.2011, (21258), 28.xi.2011, M.M. Rocha and J. Cabral (21265, 21266), 09.iii.2012, T.F. Carrijo and J. Cabral (21267).

Other material, not examined. Records from termite collections in Brasil (MPEG, UFPB, UnB) and the United States of America (UF).

Biological notes

Crepititermes verruculosus was found inside nests (occupied or abandoned) of apicotermitines (Grigiotermes Mathews, and unidentified species), nasutitermitines (Nasutitermes Dudley) and syntermitines (Cornitermes Wasmann, Embiratermes Fontes, Labiotermes Holmgren, Silvestritermes Rocha & Cancello, Syntermes Holmgren) as well as inside fallen logs. Nevertheless, some field notes from voucher specimens in the MZUSP suggest that the species can build a small “nest” among rootlets, but this is not clear if these places are structured nests or only diffuse galleries among the roots. Ropero (2013) demonstrated the behavior of C. verruculosus in the presence and absence of Cornitermes cumulans (Kollar).

For the soldiers and workers examined, we observed that their bodies rupture through a weak area between the metanotum and the first abdominal tergite, resulting in protrusion of at least part of the paunch and the pear-shaped diverticulum. The question of whether chemical substances are released during the suicidal behavior by autothysis remains hypothetical, as well as of whether the pear-shaped diverticulum is involved in defense or simply as a site for microorganism settlement.