Key to the soldiers of South American Heterotermes with a new species from Brazil (Isoptera: ) REGINALDO CONSTANTINO

A soldier-basedkey to the South American species of Heterotermes is presented. Six species are recognized: H. assu sp. n., H. convexinotatus,H. crinitus, H. longiceps, H. sulcatus and H. tenuis. H. assu sp. n., is described from the BrazilianAtlantic forest, including the imago, soldier and worker castes. H. assu is also recorded from urban areas as a pest. The imago of H. longiceps is described and illustrated for the first time. The soldiers of all species are illus- trated and their known distribution mapped, with several new records. R. Constantino,Departamento de Zoologia, Universidadede Brasilia,70910-900 Brasília, DF, Brazil (e-mail: [email protected]).

Introduction The genus Heterotermes Froggatt, 1900 has about inotatus. Most of these species were initially 50 described species from all major tropical and included in the genus Leucotermes Silvestri, 1901, subtropical regions of the World. Heteroter-mes which was later synonymized with Heterotermes and Reticulitermes Holmgren, 1913 are currently by Light (1933). Light (1933) described also H. the only genera placed in . maculatus from Mexico. Emerson ( 1971 ) stated Reticulitermes is restricted to the northern temper- that H. convexinotatus should be treated as a sub- ate zone, while Heterotermes is essentially tropi- species of H. aureus, but most authors still treat cal. Both Heterotermes and Reticuliter-mes are the former as a full species. Mathews (1977), economically important, including some of the described another species, H. sulcatus, from cen- major pest in many regions. There are 9 tral Brazil, and also redescribed H. longiceps. described species of Heteroter-mes in the New Species of Heterotermes are among the most World, 5 of them occurring in South America widespread termites in South America, being (Constantino 1998). abundant both in natural and urban environments. The New World species of Heterotermes were Several South American species, especially H. first revised by Snyder (1924), who recognized 6 tenuis, have been reported to be important both as species: H. aureus (Snyder, 1920), from southern agricultural and structural pests. Despite their eco- United States and northern Mexico, H. convexino- nomic importance, and contrasting with the vast tatus (Snyder, 1924), from southern Mexico and amount of literature on Reticulitermes, the biolo- Central America, H. cardini (Snyder, 1924), from gy and geographic distribution of Heterotermes the Bahamas, H. crinitus (Emerson, 1925), from species remains poorly known. Guyana, H. longiceps (Snyder, 1924), from cen- In this paper, a soldier-based key to the South tral Brazil, and H. tenuis (Hagen, 1858), which is American species of Heterotermes is presented, widespread in South America. Snyder's (1924) and a new species is described from the Brazilian revision did not include H. insularis (Wasmann, Atlantic forest. The imago of H. longiceps is 1903), from Cocos Island, Costa Rica, and he sug- described for the first time, and new distribution gested that it could be a synonym of H. convex- records are added for other species. 464

Methods - Pronotum with hairs only on margins (Fig. 1- 5) ...... 4 Drawings were prepared with a camera lucida 2. Tergites with a line of bristles on posterior attached to a dissection microscope. Measure- margin and numerous microscopic hairs on ments were taken with a micrometric reticle on the surface, width of head 0.79-0.84 mm; Colom- bia and Venezuela(Fig. 9, 14, 20) ...... eyepiece of a dissection microscope. Measure- ...... H. convexinotatus ments presented in Tab. 1 correspond to the fol- - Tergites with a line of bristles on posterior lowing numbers in Roonwal's (1970) system: margin and numerous long hairs on surface, = about 1/3 of the length of marginalbristles...... 3 length of head [to side base of mandibles] no. 5; 3. Head covered with hairs and = densely bristles; width of head no. 17; width of head without mandibles light brown; postmentum with a eyes = no. 18; height of head [excluding postmen- narrow mid segment with parallel sides; sol- dier tum] = no. 21; length of left mandible = no. 37; monomorphic; Guianas, Venezuela and BrazilianAmazonia; antennae with 14-15 arti- of hind tibia = no. 85; width of length pronotum = cles, usually 14 (Fig. 8, 13, 21 ) ...... H. crinitus no. 68; length of pronotum = no. 65; diameter of - Head with less dense hairs; mandibles dark eye = no. 48; length of ocellus= no. 55; length of brown; postmentum with concave sides; sol- no. 74. The distribution were dier dimorphic; antennae with 15-17 articles, forewing= maps pre- 15 H. tenuis with the Generic Tools & usually (Fig. 6, 7, 12, 22, 23) ...... pared Mapping (Wessel 4. Frons with two elevations in profile and a V- Smith 1998) based on the material examined and shaped groove between them; width of head on records 1924; Emerson 0.70-0.81 mm (Fig. 5, 15, 19)...... H. sulcatus published (Snyder - 1925; 1959; Mathews Torales et al. Frons without elevations in profile ...... 5 Snyder 1977; 5. Width of head 1.32-1.62 soldier H. tenui.r was not because it is mm; 1997). mapped monomorphic,antennae with 18 articles (Fig. widespread and very common, recorded from 1, 10, 16)...... H. assu - Panama to northern Argentina, east of the Andes. Width of head 0.85-1.03 m; soldier conspicu- Terms used for hairs are Bristles ously dimorphic, antennae with 15-17 articles comparative. 2-4, 11, 17, H. are thick hairs with well-marked bases. Hairs are (Fig. 18)...... longiceps slender. Microscopic hairs are those visible only at Heterotermes assu sp. n. magnifications of 40X or higher. The material examined is deposited in the fol- Typematerial. - Holotype (soldier): BRAZIL. State of collections: Espirito Santo. Presidente Kennedy, Praia das Neves, lowing entomological Departamento 27.iv.98,R. Constantino (DZUB). Paratypes: BRAZIL. de Zoologia, Universidade de Brasilia, Brazil State of Espírito Santo. Presidente Kennedy, Praia das (DZUB), Museu Paraense Emilio Goeldi, Bel6m, Neves, 27.iv.98,R. Constantino (soldiers and workers); Brazil, Museu de da Universidade de same locality, 30.iv.98, R. Constantino (soldiers and Zoologia State Minas Gerais. M.P. Sdo Brazil de workers). of Viqosa, 25.iv.99, Paulo, (MZSP), Departamento Souza (soldiers and workers). State of Sáo Paulo. Sao Sistemdtica e Ecologia, Universidade Federal da Paulo, 27.vi.95, A.T. Lelis (soldiers and workers); Paraiba, Joao Pessoa, Brazil (UFPB), Depart- 30.iii.94, A.T. Lelis (soldiers and workers); 25.iii.95, amiento de Universidad Central de A.T. Lelis (soldier); 14.i.98;L.F. Romagnano (soldiers, Entomologia, workers and R. Amaral and de alates); 10.xi.97, (soldiers Venezuela, Maracay, Venezuela, Departamento workers); 06.ii.00, D. K. Suganuma (soldier); 15.ii.00, Biologia , Universidade Federal de Viqosa, G. A. C. Lopez (soldier). All paratypes currently in Brazil. DZUB; some will be deposited in MZSP. Imago (Fig. 24, 25). The head capsule is brown; Key to the soldiers of South American the occiput is paler. The mandibles are the same Heterotermes color as the head, becoming darker near cutting and teeth. The antennae and are brown- Note: Soldier dimorphism is present in two edge palps ish-yellow, than head. The labrum and the but it is in H. longiceps. paler species, conspicuous only are The For this reason, major and minor soldiers are not postclypeus brownish-yellow. pronotum is a little than the head. The metan- treated in this and is brown, paler separately key, dimorphism otum and mesonotum are The used as a character. However, this brownish-yellow. supplementary are as The should work even if one of soldier tergites the same color the pronotum. key only type stemites are than the The are is available. paler tergites. legs brownish-yellow. The wings are brownish. The 1. Pronotum with at least some hairs on surface head capsule has numerous bristles and hairs of (Fig. 6-9) ...... 2 variable size. The postclypeus has 4-6 bristles. 465

Figures 1-5. Head and pronotum of soldiers in dorsal view: (1) Heterotermes assu; (2) H. longiceps, major soldier from Brasflia; (3) H. longiceps,major soldier from Espfrito Santo; (4) H. longiceps,minor soldier; (5) H. sulcatus.

The labrum has 14-16 hairs of variable size. The bristles on posterior margin and numerous hairs pronotum has numerous bristles and hairs of vari- on surface. The tibial spurs are 3:2:2. The head able size. The tergites and stemites have a row of capsule is oval, relatively wide. The antennae 466

Figures 6-15. Head and pronotum of soldiers in dorsalview (6-9); postmentumof soldiers (10-15): (6) Heterotermes tenuis, major soldier; (7) H. tenuis, minor soldier; (8) H. crinitus; (9) H. convexinotatus;(10) H. assu; (11) H. lon- giceps, major soldier; (12) H. tenuis, major soldier; (13) H. crinitus; (14) H. convexinotatus;(15) H. sulcatus.

have 20 articles: 1 st is the longest, 2nd is as long The ocelli are present, but small, close to eyes. as 3rd plus 4th, 4th is the shortest, 5th to 20th The fontanelle is small and rounded. The post- become slightly longer. The eyes are broadly oval. clypeus is short and moderately inflated. The ante- 467

Table 1. Measurementsof soldiers and imagoes of Heterotermes assu and of imagoes of H. longiceps.

rior margin of pronotum is slightly emarginate; ous ; the eye region is a little paler than the head. the posterior margin is nearly straight. The poste- The labrum is tongue-shaped and relatively short. rior margin of mesonotum and metanotum form a The pronotum is nearly as wide as head; its ante- wide angle. The measurements are in Tab. 1. rior margin is conspicuously emarginate; its pos- Soldier (Fig. 1, 10, 16). Monomorphic. The terior margin is nearly straight. The measurements head capsule is yellow, a little darker anteriorly. are in Tab. 1. The mandibles are chestnut-brown, with yellow- Worker (Fig. 28, 29). The head capsule is white brown base. The antennae and palps are about the to yellowish-white. The remainder of body is same color as the head. The labrum is yellow, with whitish. The head capsule has many bristles and a hyaline tip. The pronotum, mesonotum, meta- numerous hairs. The tergites and stemites have a notum, tergites and stemites are yellow, paler than row of bristles on posterior margin and many hairs head. The legs are pale yellow. The head capsule on surface, which are longer and more numerous has a few scattered bristles: 4-7 on frons, 10-14 on than those of soldier. The antennae have 18-19 vertex, 9-10 on each lateral side, 0-2 on underside. segments. The width of head is 1.26-1.36 mm; the The postclypeus has 2 bristles. The postmentum length of hind tibia is 0.86-1.06 mm (n=5). The has 4 bristles near anterior margin. The labrum has mandibles are as in Fig. 28-29. 4 bristles and 2-4 hairs. The pronotum has numer- Etyniology. -From the Tupi, açu, large. ous bristles on margins, and none on surface. The mesonotum and metanotum have bristles on later- Comparisons. - All castes are conspicuously larg- al and The have an posterior margins. tergites er than all other New World species of irregular row of bristles on posterior margin and Heterotermes. The head of the soldier has fewer scattered hairs of variable size on which surface, hairs than all species except H. longiceps, which are more numerous on posterior segments; their has about the same number. The soldier labrum is also surface has numerous microscopic hairs. The shorter than in other species. The antennae of sol- of but with more pilosity stemites is similar, diers of other New World species have 14-17 arti- hairs on 12- numerous surface. The foretibia has cles, and of imagoes 16-17 articles. The head of 14 thick bristles on inner short, margin, organized the imago of all other New World species is con- in and about 6 of the same bristles on two rows, spicuously more elongate. Ocelli were present in outer in a row. The tibial are margin, single spurs the examined imagoes; some Heterotermes The head is the ratio 3:2:2. capsule subretangular; species seem to lack ocelli (H. longiceps) while in of of head to width of head is 1.52-1.75. length others they may be present or absent. If present, have 1 st is the The antennae 18 articles: longest, they are always very small. 2nd is longer than 3rd, 4th is the shortest, 3rd and 5th are subequal; 6th is longer than 5th, 6th to 18th Remarks. - H. assu seems to be native of the becoming a little longer. The eyes are inconspicu- Brazilian Atlantic Forest. The type locality is a 468

Figures 16-23.Soldier heads in profile: (16) Heterotermes assusp. n.; (17) H.longiceps, major soldier; (18) H. long- iceps, minor soldier; (19) H. sulcatus. 20) H. convexinotatus;(21) H. crinitus; (22) H. tenuis, major soldier; (23) H. tenuis, minor soldier. 469

Figures 24-29. Head and pronotum of imagoes (24-27); mandibles of worker (28-29): (24-25) Heterotermesassu; (26-27) H. longiceps; (28-29) H. assu.

patch of restinga forest on top of sandy soil, at sea Heterotermes longiceps (Snyder) and about m from the coastline. All level only 500 Leucotermeslongiceps Snyder, 1924:20 [major soldier] other samples come from urban areas at higher Heterotermes longiceps; Mathews 1977:83 [major and elevations, where it has been reported as a struc- minor soldiers] tural pest. Imago (Fig. 26, 27). The head capsule is brown, with a paler, oval area posterior to fontanelle. The 470

Figure 30. Distributionrecords of Heterotermes in South America: H. assu sp. n. (circle), H. convexinotatus(trian- gle), H. crinitus (square),and H. sulcatus (inverted triangle). The type-localitiesare indicated by a double symbol,

antennae and palps are brownish-yellow. The face. The tergites and stemites have a row of bris- postclypeus and labrum are light brown. The tles on posterior margin and dense short hairs on pronotum is brown, with a T-shaped paler area in surface. The tibial spurs are 3:2:2. The head cap- the middle. The mesonotum and metanotum are sule is elongate, and the fontanelle is small. The brownish-yellow. The tergites are paler than the antennae has 17 articles: 1 st is the longest, 3rd is pronotum but darker than the mesonotum. The the shortest, 4th and 5th are subequal; 6th to 17th stemites and legs are brownish-yellow. The wings become slightly longer. The eyes are oval, elon- are brownish. The head capsule has numerous gate, relatively small. The ocelli are absent in all hairs and bristles of variable size. The postclypeus examined specimens. The postclypeus is relative- has 6-8 bristles and a few short hairs. The labrum ly long (length is about 0.18 mm compared to 0.12 has 14-16 hairs and bristles. The pronotum has mm in H. tenuis) and strongly inflated. The poste- numerous hairs and bristles on margins and sur- rior margin of mesonotum and metanotum are 471

Figure 31. Distributionrecords of Heterotermeslongiceps in South America.The type-localityis indicatedby a dou- ble circle.

strongly concave, sometimes deeply V-shaped. Brazil tend to have more elongate heads, while The measurements are in Tab. 1. those from the coastal region have shorter and wider heads. However, this variation seems to Comparisons. - Very similar to the imago of H. form a continuum, and it is not observed in ima- tenuis, from which it can be distinguished on the goes or minor soldiers. This species is second in size of the postclypeus, longer and more inflated South America in abundance and geographic in H. longiceps. The imago of H. longiceps is also range, being surpassed only by H. tenuis. It has darker. also been reported as an agricultural and structur- al pest. In a recent survey in a savanna Remark. - The major soldier of H. longiceps (cerrado) area in Brasilia (Constantino, unpub- shows a wide range of variation, especially in lished data), H. longiceps was the second most head length (Fig. 2 & 3). Specimens from central frequent species. 472

Material examined. - BRAZIL. State of Bahia. Reticulitermes, that the species currently recog- A.T. Lelis and Salvador, 17.vi.99, (soldiers workers). nized morphologically correspond to several Distrito Federal. Brasilia, 04.xi.1991, K.Kitayama(sol- diers and workers); 09.ix.1992, K. Kitayama (soldiers species complex. and workers); 16.xii.1991, K. Kitayama (soldiers and The existence of additional undescribed species workers); I.x.1999, O. Kitade; 23.x.1999, R. is likely, although Heterotermes does not seem to Constantino State Santo. Presidente (alates). of Espirito be highly diverse in the New World. Kennedy, Praia das Neves, 27.iv.98, R. Constantino (two samples with soldiers and workers). ,Stateof Mato Grosso. APM Manso, R. Constantino.State ll.v.1999, Acknowledgments of Minas Gerais. Sete Lagoas, 30.viii.84, D.J. Domingos (soldiers and workers); Joao Pinheiro, The author received financial support from the Brazilian 12.xi.98,N.R.A. Castro (soldier).State qf Paraiba. Joao National Council for Development of Science (CNPq, Pessoa, 2l.xii.1993, A.G. Bandeira (soldiers and work- grant no. 301423/87-3).A. Harada (Goeldi Museum), ers, UFPB). Areia, 29.xii.1998, M.P. Silva & A. A.T. Lelis (Instituto de Pesquisas Tecnologicasde S5o Vasconcellos(two samples with soldiers, workers and Paulo), A.G. Bandeira (Universidade Federal da alates, UFPB). State of Pernambuco. Caruaru, Paraiba) and C.J. Rosales (Universidade Central de 15.i.1998, A. Vasconcellos (soldiers and workers, Venezuela)are thanked for sending specimensfor study. UFPB) State of Sao Paulo. Penapolis, l3.viii.96, R.D. C.J. Rosales is also thanked for corrections to the iden- Amaral (soldiers and workers). All samples are in tification key. DZUB, except the ones indicated to be in UFPB.

Discussion Constantino,R. (1998) Catalog of the living termites of the New World (Insecta: Isoptera). Arquivos de Despite their abundance and economic impor- Zoologia 35: 135-230. tance, the South American species of Hetero- Emerson, A. E. (1925) The termites from Kartabo, ter-mes remain known. The dis- Bartica District, Guyana. Zoologica 6: 291-459. poorly geographic A. E. fossil Rhino- tribution of some is still uncertain. Emerson, (1971) Tertiary species of species highly termitidae (Isoptera),phylogeny of genera and recip- H. sulcatus, for instance, was previously known rocal phylogeny of associated flagellate (Protozoa) only from its type locality, and is know reported as and the Staphylinidae Coleoptera. Bulletin of the abundant in two distant localities. It is also sur- American Museumof Natural History 146: 243-304. S. F. Termitesof western Mexico. Univer- that H. assu a and Light, (1933) prising sp. n., large conspicuous sity of California Publications in Entomology6: 79- species, has never been reported by any entomol- 164. ogist, although it is native of the most densely Mathews, A. G. A. (1977) Studies on termites fromthe area of South America. Mato Grosso State, Brazil. Academia Brasileira de populated Ciências. 267 Rio de Janeiro. The record of Heter-otermes crinitus in pp. Roonwal, M. L. (1970) Measurementof termites (Isop- Venezuela (Snyder 1959), near Lake Valencia, tera) for taxonomic purposes. Journal of the Zoolo- was never reconfirmed despite a good collecting gical Societyof India 21: 9-66. effort in that around Snyder, T. E. (1924) Descriptions of new species and region, especially Maracay. hitherto unknown castes of termites from America H. convexinotatus has been found there. H. Only and Hawaii. Proceedings of the U.S. National Mu- crinitus is possibly rare in that region, or lives in a seum 64 (6): 1-45. very specific habitat not sampled. It is also possi- Snyder,T. E. (1959) New termites from Venezuela,with ble that there was some error in that record. keys and a list of the described Venezuelanspecies. American Midland Naturalist 61: 313-321. in Many taxonomic issues need to be examined Torales, G. J., Laffont, E. R., Arbino, M. O. & Godoy, more detail. Before Snyder's (1924) revision, all M. C . (1997) Primera lista faunistica de los isópteros South American Heter-otermes were treated as de la Argentina. Revista de la Sociedade Entomo- 56: 47-53. Heteroter-mes tenuis, which was considered a logica Argentina Wessel, P. & Smith, (1998) New, improved version of widespread and variable species. It is possible, as Generic Mapping Tools released. EOS Transactions it has been demonstrated for some groups of of the American GeophysicalUnion 79: 579.