Syntermes wheeleri, Emerson, 1945
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https://doi.org/ 10.1206/377.2 |
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persistent identifier |
https://treatment.plazi.org/id/038387DE-FF1F-FF3B-FFBC-9FE58058F91A |
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treatment provided by |
Felipe |
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scientific name |
Syntermes wheeleri |
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Syntermes wheeleri View in CoL
Microcerotermes baluchistanicus
Microcerotermes biroi x Microcerotermes bugnioni x Microcerotermes cameroni
Microcerotermes danieli x Microcerotermes diversus *
Micerocerotermes edentaus
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x x x x x
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x
x x
x x
x x
Argentina, Bolivia, Brazil, Paraguay Brazil
Argentina, Brazil, Paraguay Pakistan
India, Pakistan
Nigeria, Uganda
Guyana, Brazil
Australia
Australia
Kenya
Australia
Australia
Australia
Mozambique
Iran, Turkmenistan
Pakistan
Sri Lanka
Australia
Australia
Sudan
India
South Arabia
Sri Lanka
Malaysia
Malaysia, Thailand
India
Trinidad, Amazonia, Guianas Pakistan
India
Solomon Is.
Sri Lanka
India
India
Israel, Arabia, Iraq, Iran
Ivory Coast
TERMITE EVOLUTION: DIVERSITY, DISTRIBUTIONS, PHYLOGENY, FOSSIL RECORD
At any one moment in evolutionary history, the diversity of organisms is a product of the speciation and extinctions that have preceded it. While ecological and genetic factors clearly affect the speciation and extinction of populations, and thus of species, understanding diversity also requires a historical context, for which phylogeny is the sine qua non. Understanding phylogenetic relationships are necessary for indentifying monophyletic taxa and for discerning evolutionary patterns. While it is typical for entomologists to examine phylogenetic relationships of living species only, we have made an effort to also include extinct termites here, since fossils are required for interpreting past diversity, the ages and divergence times of taxa, and extinctions.
The monophyly of the termites has probably never been seriously questioned, and indeed the Isoptera is defined by a large suite of specialized features or synapomorphies. These include the following: an imago-worker head that is prognathous (vs. opisthognathous as in roaches and hypognathous as in mantises); narrow, homonomous wings that dehisce along a basal suture; reduction of the crossveins into reticulations and loss of many longitudinal veins; reduction of the typical, large dictyopteran pronotum; highly reduced genitalia; and advanced sociality, or eusociality. Termites, in fact, are the only major group of social animals in which all species have morphologically distinct reproductives and soldiers (and usually workers), which are also comprised of both sexes, not just females.
The relationships of termites, however, to the two other major lineages of Dictyoptera, the Blattaria and Mantodea, have historically been controversial, with each of the four possible permutations having been proposed. These early studies, up to approximately the year 2000, have been amply reviewed (Kambhampati and Eggleton, 2000; Thorne et al., 2000; Eggleton, 2001; Grimaldi and Engel, 2005; Klass and Meier, 2006). In the past decade, evidence has accumulated that has established an undisputed sister-group relationship between termites and the relict wood roaches, Cryptocercus . This is the sole genus of the family Cryptocercidae , with seven known species: four in the southern Appalachians, one in the Cascade Mountains of northwestern North America, and two species in the Far East.
The concept of a Cryptocercus -termite relationship began with the classic work of Cleveland et al. (1934) on the similar symbiotic ciliate and flagellate protists shared between Cryptocercus and some basal termites (i.e., the protist genera Leptospironympha and Trichonympha ). Besides harboring similar protist faunas, Cryptocercus also feeds on and nests within decaying wood in small colonies of parents and offspring. Cryptocercus are long-lived, monogamous, have extended parental care, and engage in transfer of protists among nestmates (reviewed in Grimaldi and Engel, 2005). Specialized structure of the proventriculus likewise supports this relationship (McKittrick, 1964; Klass, 1998), as do mandibular dentition (Ahmad, 1950) and other morphological features (Dietz et al., 2003; Grimaldi and Engel, 2005; Klass and Meier, 2006). It was the advent of molecular studies that fully corroborated the Cryptocercus -termite hypothesis (Lo et al., 2000; Inward et al., 2007a, 2007b; Legendre et al., 2008).
The view that termites are simply highly modified social roaches is no longer in dispute, demoted from an order to a subordinate taxon within Blattaria ? The proposal has even been made that the name Isoptera be replaced with a family name (such as Termitidae , s.l.) and current families become subfamilies (Inward et al., 2007a). Lo et al. (2007), in response to this proposal, indicated that this would create unnecessary taxonomic chaos, and that Isoptera can be retained either as an unranked group or eventually be given some formal superfamilial grouping within Blattaria . This would preserve the internal classification of Isoptera and satisfy most needs for a phylogenetic classification. Thus, we are proposing an Infraorder Isoptera within the Order Blattaria , along with a few modifications of the taxonomic ranks within Blattaria (see classification summary and Engel et al. 2009).
Along with the recent activity in phylogenetics of termites has been the discovery and study of diverse fossil termites (figs. 60–65). The majority of termite fossils are preserved as compressions or impressions in sedimentary strata (e.g., fig. 60), and most of these are preserved as isolated wings. Wings are less susceptible to decay, which is why they are the most common type of insect remains in fossil deposits (Grimaldi and Engel, 2005). Wing venation in termites provides some phylogenetic information, such as the branching of Rs, M, and Cu veins, but there is a great deal of intraspecific variation, which unfortunately makes phylogenetic interpretation difficult based on venation alone. Moreover, many of the most systematically reliable characters for termites are of minute structures unlikely to be preserved in compressions, such as ocelli, sulci, tarsomeres and tibial spines, cerci, and mandibular dentition. Fortunately, insects preserved in amber (figs. 63–65), and ones preserved as 3-dimensional mineralized replicas (such as from the Miocene of Calico, California, and the very important Early Cretaceous Crato Formation of Brazil [Grimaldi et al., 2008: fig. 62]), generally preserve detailed 3-D structure. There are also fossilized remains of nests and galleries, generally referred to as ichnofossils. As a result, we have tended to place more emphasis in our interpretation of the termite fossil record on these well-preserved fossils. Tables 11 through 14 summarize the global diversity of living and extinct genera and species, and their distributions.
Several comprehensive phylogenetic studies on termites have been published within the past decade. These include the studies by Donovan et al. (2000), which used morphological and biological characters; and the molecular studies by Thompson et al. (2000: using 2 genes), Inward et al. (2007: 3 genes), and Legendre et al. (2008: 7 genes). Hypotheses on the relationships of families and some basal genera of termites are compared in figure 61. Relationships that agree in all or most of the hypotheses include the following: Mastotermitidae is the most basal living family; all other living termites comprise a monophyletic group; other groups that are definitively monophyletic are the Kalotermitidae , the two genera Stolotermes + Porotermes (now placed in the Stolotermitidae [Engel et al., 2009]), the harvester termites ( Anacanthotermes , Hodotermes , and Microhodotermes : Hodotermitidae s.s.), those termites with a fontanelle (Neoisoptera), and the Termitidae . There also seems to be agreement in these major studies about the paraphyly of the Rhinotermitidae , though they differ as to relationships among rhinotermitids, as discussed below. Most recent is the morphological analysis of Engel et al. (2009), which included fossils with living taxa, and thus allows much more accurate
interpretation of the termite fossil record.
Using a phylogenetic framework, the following is our attempt to synthesize various aspects of termite biology and their fossil record into an evolutionary narrative.
The earliest termites derive from the Early Cretaceous, 135–100 Mya, and in fact all species from the Cretaceous Period (145–65 Mya) are primitive (figs. 60, 62–64, 66). By “primitive” we mean they are either stem groups to all families of termites (i.e., Cratomastermes), to Mastotermes (several genera), to the Euisoptera , or to and among the basal living families including the Kalotermitidae . The most derived termite from the Cretaceous is the only one that possesses a fontanelle, Archeorhinotermes rossi (fig. 64C–D). Until recently (Engel et al., 2009), Isoptera was considered unique among major insect orders in having no extinct families, but this concept was merely an artifact of classifications that have not been based on phylogenetic study of the fossils. Almost all Cretaceous taxa, for example, were placed into a broad Hodotermitidae (Emerson, 1969; Nel and Paicheler, 1993; Thorne et al., 2000; Grimaldi and Engel, 2005). Engel et al. (2009) clarified the position of various Cretaceous genera that have either traditionally or provisionally been placed in the Hodotermitidae , such as Meiatermes (fig. 62D), Carinatermes (figs. 63A, B), and Mariconitermes (fig. 62A), and found that these are actually stem groups to the Euisoptera (see below). With the exception of Archeorhinotermes and Proelectrotermes holmgreni (both in 100 Myo Burmese amber; fig. 64E), all Cretaceous genera, where known, plesiomorphically have numerous antennomeres, a Y-shaped epicranial sulcus, five fully developed tarsomeres, numerous and well-developed superior branches of vein Rs, vein reticulations, a relatively large pronotum, and well-developed and serrated tibial spurs.
The most primitive Cretaceous termites—indeed, apparently the most basal of all known termites—is Cratomastotermes wolfschwennegeri Bechly from Brazil’s Crato Formation (fig. 62B). As the name suggests, it was originally placed in the Mastotermitidae (Bechly, 2007) , but this robust, heavy-bodied termite has features that are even more primitive than those of the mastotermitids, and so has been placed into a separate family, the Cratomastotermitidae (Engel et al., 2009) . These are, namely, a very large, broad head (the presence/absence of ocelli is unknown), an exceptionally large pronotum, and wing venation in which the reticulations are actually developed as complete crossveins (in all living and extinct Mastotermitidae these crossvein reticulations do not join the longitudinal veins).
Mastotermes darwiniensis Froggatt is the sole living species of the family Mastotermitidae , and undisputedly the most basal living species of termite (figs. 11, 61, 66). It is found in the tropical, nonforested regions of northern Australia and has been introduced into southern New Guinea (fig. 67). Primitive features it retains are the following: large body size; ocelli; relatively large pronotum; hind wing with a large, fanlike anal lobe; numerous branches of veins Rs, M, and Cu; hind wing with barely developed basal suture; five tarsomeres; keeled fore coxae; multisegmented cerci; ovipositor (though internal) with valvulae; eggs laid in a vestigial ootheca; and specialized mycetocytes that harbor symbiotic Blattabacterium bacteria that are also found in roaches. It has been known for some time that Mastotermes darwiniensis is highly relict, since fossil Mastotermes are nearly global, from the Miocene through the Eocene of Europe (Emerson, 1965; Engel and Wappler, 2006), and in Miocene amber from Chiapas,
Mexico (Krishna and Emerson, 1983), and the Dominican Republic (Krishna and Grimaldi, 1991), for a total of 13 extinct species of the genus. All three castes, in fact, are known for Mastotermes electrodominicus (Grimaldi and Engel, 2005) . This species was also the subject of study for ancient DNA (DeSalle et al., 1992), though the authenticity of ancient DNA from amber fossils is doubtful (reviewed in Grimaldi and Engel, 2005). Fossil M. electrodominicus workers even yielded finely preserved remains of symbiotic protists from the hind-gut tissue (Wier et al., 2002). Despite the relict nature of Mastotermes , M. darwiniensis is a notorious pest with a very broad diet. Its distribution seems to be limited mostly by climate, which may have been the primary factor in the widespread extinction of Mastotermes .
There are seven other genera in the Mastotermitidae , all extinct and distributed throughout the world. The oldest apparent mastotermitid is Valditermes brenane Jarzembowski from Early Cretaceous Wealden clay of England. Its phylogenetic position has been disputed, but based on the long, straight anal edge of the incompletely preserved hind wing, it appears to have had a large anal lobe. Perhaps the most remarkable fossil mastotermitid is Garmitermes succineus , recently discovered in Baltic amber (Engel et al., 2007; fig. 65A–C). It is known only from a unique dealate specimen that is beautifully preserved, and it possesses features that are even more plesiomorphic than those in Mastotermes : a very large pronotum that wraps laterally, large lateral cervical sclerites, apical flagellomeres that are tapered, and plantular pads on the tarsi. Oddly, despite centuries of collecting and study of Baltic amber, this is the only known mastotermitid from that fossil deposit. In the study by Engel et al. (2009), Mastotermitidae were surprisingly defined as monophyletic, even though they have traditionally been defined on the basis of plesiomorphic morphological features. Monophyly of the family is weakly supported, though, based only on two homoplastic features, the presence of ocelli and the shape of the pronotum.
All the remaining Isoptera exclusive of the Mastotermitidae and Cratomastotermitidae are a monophyletic group that have been named the Euisoptera (Engel et al., 2009: fig. 66) based on the loss of various blattodean features of mastotermitids: absence of symbiotic Blattabacterium and ootheca (eggs instead are laid singly), complete loss of an ovipositor and an anal lobe/fan in the hind wing, as well as reduction in the size of the pronotum. There thus seems to be a sizeable phenotypic gap between the Mastotermitidae and the remaining termites. Relationships are ambiguous and contentious among those basal living genera of Euisoptera that traditionally have been classified in the Hodotermitidae and Termopsidae , as summarized in the classifications in table 10 and cladograms in figure 61.
One grouping of agreement among the major phylogenetic studies is the monophyly of the three genera of the “harvester” termites, Anacanthotermes , Hodotermes , and Microhodotermes (figs. 33–35), or what are classified as the Hodotermitidae s.s. (Engel et al., 2009: fig. 66). The molecular study by Inward et al. (2007) confirmed this close relationship, as did Legendre et al. (2008), though only the last two of these genera were included in that study. Morphologically and behaviorally the harvester termites share a suite of derived features: lacinia with one tooth subapical instead of both teeth apical, loss of soldier ocelli, the inferior branches of vein Rs parallel and diagonal to the trunk of Rs, and life in grasslands and steppes where they provision their nests with fragments of dried grasses and seeds. There are 21 species of harvesters
(16 in Anacanthotermes alone), distributed throughout Africa and extending into the Middle East, Eurasia, and to northwest India (fig. 67). Besides seeds and dried grasses, harvesters also feed on palm debris, herbivore dung, and occasionally on small amounts of wood. Some species of Anacanthotermes have been known to consume the straw embedded within the mud bricks of rural dwellings. The nests are a loose system of subterranean chambers and passages in the soil, marked on the surface by shallow mounds. Some of the chambers within the nest serve as “granaries.” Although Engel et al. (2009) did not include the genus Ulmeriella in their analysis (which is known almost entirely from wings), Ulmeriella were possibly harvesters. This is the largest extinct genus of termites, with 11 described species, and is known from the Pliocene to the Oligocene of Asia, Europe, and North America (Emerson, 1968). The geo- graphic and stratigraphic distribution of Ulmeriella suggests that the current range of the harvester termites is contracted and that the family, though phylogenetically basal, is rather young and no doubt originated and expanded with the grasslands in the Oligocene and Miocene. It is likely that the harvester termites are derived from one of the many stem-group Cretaceous termites.
Another very stable group comprises the two genera Stolotermes and Porotermes , each of which has traditionally been placed as a subfamily ( Stolotermitinae and Porotermitinae , respectively) within the Hodotermitidae (Snyder, 1949a; Emerson, 1955, 1968a, 1968b; Krishna, 1970) or Termopsidae (Grassé, 1949) , but which have recently been classified into a separate family, the Stolotermitidae (Engel et al., 2009: fig. 66). This group is biogeographically unique among all termites, the only species with a distribution that is a classic austral disjunction (Grimaldi and Engel, 2005; fig. 67). There are only 10 living species, most of which dwell and feed in rotting logs and tree trunks, although Porotermes adamsoni from eastern Australia attacks a variety of living trees and can be a serious timber pest. Two other species of Porotermes are P. quadricollis , from the wet temperate forests of Cautin Province, Chile, and P. planiceps Sjöstedt from South Africa (fig. 36A–C). Stolotermes occurs in southeast Australia ( S. australicus Mjöberg , S. victoriensis Hill , S. queenslandicus Mjöberg ), in New Zealand and Tasmania ( S. brunneicornis [Hagen], S. inopinus Gay , and S. ruficeps Brauer ), and in South Africa ( S. africanus Emerson ; fig. 36D–E). Austral disjunctions are classically interpreted as relicts of gondwanan drift, in which case these taxa would derive from the Cretaceous, although this interpretation is contradicted by various instances of austral insect fossils from the Northern Hemisphere (reviewed in Grimaldi and Engel, 2005). Cretatermes carpenteri Emerson (1967) , from the Late Cretaceous of Labrador, has been interpreted on the basis of wing venation as similar to that of the Stolotermitidae , but Emerson classified it in a monotypic subfamily Cretatermitinae ; otherwise there are no fossils of this group. Cretatermes was the first Cretaceous termite discovered and described.
Monophyly of the family Archotermopsidae (Engel et al., 2009) remains to be defined, although some of the molecular studies indicate a close relationship of two of the three genera placed in this family, Archotermopsis and Zootermopsis (Inward et al., 2007; Legendre et al., 2008). The relationships of the monotypic genus Hodotermopsis from southeast Asia (containing H. japonicus [= H. sjostedti ]) are as yet unclear (Engel et al., 2009; Legendre et al., 2008). Morphologically, an apomorphic feature of this group is the reduced second tarsomere, which is not visible when viewed dorsally. Archotermopsis and Zootermopsis have a disjunct distribution, with two living species of the former genus, A. wroughtoni (in the Himalayan foothills of northern Afghanistan, Pakistan, and India) (fig. 31), A. kuznetsovi Beljaeva (from Vietnam), and three species of Zootermopsis found in western North America (fig. 32A–C). Close relationship of the fossil species Archotermopsis tornquisti , in Eocene Baltic amber, to the living species of the genus is supported by their unique lenticular eyes. The fossil genera Parotermes and Gyatermes , while known largely from wings, are likely archotermopsids. With the exception of Zootermopsis laticeps from Arizona and northern Mexico, which excavates nests in deciduous softwoods, the other three species of Zootermopsis and Archotermopsis construct
simple, gallerylike nests within rotting conifer logs. A great deal of research has been done on Zootermopsis (e.g., Thorne, 1990, 1991; Thorne et al., 1993). Traditionally classified with these three living genera is the extinct genus from Baltic amber, Termopsis (Snyder, 1949a; Grassé, 1949; Emerson, 1955, 1968a, 1968b; Krishna, 1970; Roonwal and Chhotani 1989), but this genus appears phylogenetically basal to Archotermopsidae and even Hodotermitidae s.s., so Termopsidae s.s. has been proposed for Termopsis alone (Engel et al., 2009). There are two species of Termopsis , T. bremii and T. ukapirmasi (fig. 65C).
Monophyly of the “dry-wood” termites, family Kalotermitidae , is well established, based on morphological, behavioral, and genetic features (Krishna, 1961; Thompson et al., 2000; Inward et al., 2007; Legendre et al., 2008; Engel et al., 2009). Morphologically the kalotermitids are defined by the microstructure of the wing membrane (with either a pimplate or nodulose surface), a swollen humeral margin of the forewing scale, and three metatibial spurs. The common name derives from the habit of these termites excavating galleries in sound wood, either dead or living, sometimes even infesting dense tropical hardwoods like mahogany (e.g., some Neotermes ). They are further distinctive in the loss of the worker caste. With 489 species (457 of them living) and 20 living genera, this is the second largest family of termites after the Termitidae . The monograph by Krishna (1961) on the genera remains the definitive reference for Kalotermitidae . Several interesting aspects of their biology relate to their wood-boring habits. One of these is that kalotermitids are dominant features of insular termite faunas, such as occur on islands in the Caribbean and the Pacific. Particularly for oceanic islands, colonization by kalotermitids is apparently facilitated by rafting in rather buoyant sound wood. Secondly, the soldiers of some genera are phragmotic, having plug-shaped heads used for blocking the openings to the galleries. In the most specialized phragmotic soldiers the frons is swollen, making the front of the head flat to concave, and the anterior half of the head with heavily sclerotized, wrinkled cuticle bearing short mandibles.
Traditionally, the Kalotermitidae were considered to be the sister group to the Mastotermitidae (Ahmad, 1950; Krishna, 1961), but, with the exception of Legendre et al. (2008), modern studies place the family as the sister group to Rhinotermitidae + Serritermitidae + Termitidae (Donovan et al., 2000; Thompson et al., 2000; Inward et al., 2007; Engel et al., 2009: fig. 61). Kalotermitidae are well represented as fossils in amber, the oldest of which are in 100 Myo Burmese amber, Proelectrotermes swinhoei and P. holmgreni (fig. 64E). Baltic amber contains three species of Kalotermitidae : Electrotermes affinis , E. girardi , and Proelectrotermes berendtii . The phylogenetic study of Engel et al. (2009) indicates that these extinct genera are stem groups to a crown group that consists of the living kalotermitids. Three species of Kalotermitidae are preserved in Miocene amber from the Dominican Republic, which belong to the speciose living genera Cryptotermes , Glyptotermes , and Incisitermes . The phylogenetic and stratigraphic positions of kalotermitid fossils thus indicate a Late Cretaceous divergence of living Kalotermitidae lineages from their extinct stem groups. There is even a well-preserved kalotermitid nest within in mineralized (“petrified”) wood from the Late Cretaceous Javelina Formation of Texas (Rohr et al., 1986).
There are three monotypic genera that appear to be stem groups to the Kalotermitidae and Neoisoptera, which are Dharmatermes avernalis and Tanytermes anawrahtai in 100 Myo Bur-
mese amber (fig. 64), and Baissatermes lapideus , a 135 Myo compression fossil from Siberia (Engel et al., 2009; fig. 60). Baissatermes is the oldest fossil termite, whose phylogenetic position indicates that the basal divergences of Isoptera probably extended into the Late Jurassic. The Neoisoptera is a definitive monophyletic group distinguished by a unique synapomorphy, the presence of a fontanelle (Engel et al., 2009), which is a grouping that is also consistently defined on a genetic basis (Thompson et al., 2000; Inward et al., 2007; Legendre et al., 2008). Archeorhinotermes rossi Krishna and Grimaldi (fig. 64C, D), also in Burmese amber, was originally reported as the first Cretaceous Rhinotermitidae , placed in its own subfamily, the Archeorhinotermitinae (Krishna and Grimaldi, 2003); recent analysis indicates this species is a stem group to the Neoisoptera (Engel et al., 2009), and so should be placed in a separate family, the Archeorhinotermitidae . Archeorhinotermes has a distinctive left mandible, with four long, sharp marginal teeth (fig. 64D). Thus far, Archeorhinotermes is the only Cretaceous neoisopteran.
A genus that was not incorporated into the major studies (Donovan et al., 2000; Thompson et al., 2000; Inward et al., 2007; Legendre et al., 2008) is Stylotermes , formerly of the Rhinotermitidae (Stylotermitinae) (fig. 49). It is now placed in the Stylotermitidae along with the closely related fossil genus Parastylotermes (Engel et al., 2007b, 2009) by virtue of lacking some of the derived features of Rhinotermitidae s.s. (such as a clypeus keeled in profile, and strongly reticulate wings lacking setae on the membrane), as well as having the unique feature of three tarsomeres. There are 45 species of Stylotermes , all from southeast Asia where they have small colonies living in tunnels of sound or dying wood. Parastylotermes contains four species, three of which are compression or mineralized specimens from the Miocene of California and Washington, and the fourth is P. robustus (Rosen) in Eocene Baltic amber. Because of the incomplete nature of the Miocene specimens it is difficult to determine whether these are indeed stylotermitids. In the study by Engel et al. (2009), Stylotermitidae is the living sister group to the remaining Neoisoptera (fig. 66).
Relationships of the small living family Serritermitidae within Neoisoptera are somewhat ambiguous, with some hypotheses placing them as the living sister group to Rhinotermitidae + Termitidae (Donovan et al., 2000; Thompson et al., 2000), as closely related to some Rhinotermitidae (Inward et al., 2007) , as a subfamily of Rhinotermitidae (Austin, 2004) , or as the sister group to the Termitidae (Engel et al., 2009) . Serritermitidae contains two genera and three species, Serritermes (monotypic: serrifer [Hagen and Bates]) and Glossotermes (occulatus Emerson and sulcatus Cancello and De Souza ), all of which are from South America and generally nest in mounds of Cornitermes ( Termitidae : Syntermitinae ). Glossotermes was formerly classified in the Rhinotermitidae . Soldiers of both genera are particularly distinctive, possessing long, straight mandibles having numerous fine serrations on the inner edge (fig. 56).
The family Rhinotermitidae , a diverse assemblage of 335 living species in 12 genera and 6 subfamilies, is paraphyletic with respect to Termitidae . They nest in the ground or decaying logs and stumps, and infest moist, decaying wood in contact with the soil. There is significant disparity among the major studies as to which rhinotermitids are the sister group to Termitidae (fig. 68). According to Inward et al. (2007), there is a grade of at least four major rhinotermitid lineages, with Termitidae closely related to the most derived of these (fig. 68). The earlier study by Lo et al. (2004), which used portions of three mitochondrial genes, largely agrees with
the results by Inward et al. (2007). Legendre et al. (2008) postulated that Termitidae is the sister group to all Rhinotermitidae except Reticulitermes , and Engel et al. (2009) hypothesized a monophyletic Rhinotermitidae (sans Stylotermes ) as sister group to Termitidae + Serritermitidae . Clearly, thorough study of rhinotermitid relationships is needed. Despite the ambiguities, a few groups of genera are consistently hypothesized, indicated as A and B in figure 68. Group A contains the genera Dolichorhinotermes , Rhinotermes , and Schedorhinotermes , and corresponds to the subfamily Rhinotermitinae ; group B contains Coptotermes , Heterotermes , and Reticulitermes , and would correspond to the subfamilies Coptotermitinae and
The group A genera, including the monotypic Macrorhinotermes from Borneo, are partly distinguished by having dimorphic soldiers. The minor soldiers of these species have a long labrum and bladelike mandibles lacking teeth; in those species with a very long labrum this structure is used for dispersing a defensive secretion. Schedorhinotermes contains 40 species throughout the IndoPacific; Rhinotermes and Dolichorhinotermes contain five and seven species, respectively, all of them Neotropical.
Group B contains the largest genera of the family and some of the most notorious termite pests. Coptotermes (71 species; circumtropical) has distinctive soldiers that bear a very large fontanelle, which exudes a “milky secretion, which sets to a rubbery mass on contact with air” when the soldiers are disturbed (Roonwal, 1970c: 336). The genus contains one of the world’s most destructive termites, C. formosanus Shiraki (the “formosan termite”), a subtropical temperate species, which has been introduced nearly worldwide. Colonies of C. formosanus can reach over one million individuals. Heterotermes contains 31 species distributed in all tropical regions except central Africa, some of which are also significant pests. Reticulitermes , which contains 140 species, is very well known because it contains the most northerly termites. In the Palearctic, Reticulitermes extends to approximately 45°N latitude (through southern France, northern Italy, the Balkan states, east to the northern and eastern shores of the Black Sea). In the Nearctic, Reticulitermes extends to approximately 50°N in the west (because of the temperate rain forests along the coast of British Columbia), and in the east to about 43°N. The few species of Reticulitermes that range this far north clearly benefit by competitive release from other termites.
Two enigmatic genera of Rhinotermitidae are Psammotermes and Termitogeton (figs. 50A, F). Psammotermes contains six species from arid regions of Africa (Sahara, Namib), the Middle East, and western India. It is the only truly desert-dwelling genus of termites, with some species living in sand dunes while feeding on the windblown chaff of plant debris and ungulate dung. Like the harvesters, Psammotermes provision their subterranean nests with bits of dried grass, seeds, and similar material. At least some species are reported to have trimorphic soldiers (Roonwal, 1970c; Roonwal and Chhotani, 1989). Termitogeton contains only three species from southeast Asia, which are distinctive for the flat, cordate heads of the soldier and wing venation where vein M is virtually or entirely lost.
There are 18 fossil species of Rhinotermitidae , all belonging to living genera. Most of these are in Miocene amber from Mexico and the Dominican Republic ( Coptotermes , Dolichorhinotermes ) (Emerson, 1971; Schlemmermeyer and Cancello, 2000; Engel and Krishna, 2007c; Krishna and Grimaldi, 2009), and in Eocene Baltic amber (Engel et al., 2007b; Engel, 2008). Coptotermes priscus Emerson , in Dominican amber, is even known for all three castes. Reticulitermes antiquus (Germar) is the most common termite in Baltic amber; Reticulitermes minimus Snyder , also in Baltic amber, is one of the smallest known termites.
Termitidae is the largest family of termites with 2072 living species and 238 living genera, a diversity that has seriously impeded efforts at unraveling phylogeny. Traditional views of relationships have relied upon systems employing one or a few characters, such as the mandible structure of imago-workers and soldiers (Ahmad, 1950) as well as head (e.g., fontanelle)
structure (Krishna, 1970). Studies by Noirot and coworkers on the structure of the digestive system (usually just called the “gut”) have revealed significant variation, and thus have provided many morphological characters that correlate with habits and phylogenetic groupings (Noirot, 2001; Bitsch and Noirot, 2002; Sands, 1972; Donovan et al., 2000; Inward et al., 2007; figs. 69, 70). Although the study by Donovan et al. (2000) used 196 morphological and biological characters, many of these appear to have been overly “split” with multiple character states of questionable homology, which may explain the low support values for many of their clades. In general, other than the highly specialized heads of soldiers, the morphology of Termitidae is rather limited for deciphering relationships among such a diverse group, so molecular data promise to be particularly informative for this family. There have been several molecular studies analyzing Termitidae , but most of them have had very limited gene sampling (i.e., just COII: Miura et al., 1998; Austin et al., 2004; Ohkuma et al., 2004) or limited taxon sampling. The study by Legendre et al. (2008), for example, used sequences from seven genes, but only for 14 genera and species of Termitidae . The study by Inward et al. (2007) used only three genes, but for 240 species in over 100 genera of Termitidae —a taxon sampling that is unlikely to be duplicated. Thus, we are using this last study as the main reference for our discussion of termitid relationships.
Based on these and other studies, there are several unambiguous phylogenetic patterns and monophyletic groups in the Termitidae .
The Macrotermitinae is a monophyletic sister group to the rest of the Termitidae . This is a morphologically conservative group of 378 species in 12 genera that is behaviorally very specialized. These are the well-known fungus-growing termites that cultivate the mycelia of a Tricholomataceae (Basidiomycetes) fungus, Termitomyces , in the intricate galleries of their subterranean nests. Nest architecture is distinctive to most genera. This famous symbiosis has been studied for more than a century (Doflein, 1906; Petch, 1906; Bose, 1923; Heim, 1940; Grassé, 1994, 1945; Roonwal, 1962a; Batra and Batra, 1966; Sands, 1969; Rouland-Lefèvre, 2000). Workers forage outside the nest and apply feces to the nest walls on which the fungus grows. Mycelia and globular conidia of the fungus, on which the termites feed, metabolize the lignocellulose in the feces. Though many macrotermitines are dependent on this fungus, some apparently are not, and phylogenetically the various species of Termitomyces appear to be associated with particular genera of termites (Sands, 1969; Rouland-Lafèvre, 2002). Thus, the relationship appears completely analogous to the situation in the fungus-growing ants, the Attini. The ants also culture Tricholomataceae fungi on the walls of their nests, on which they feed, but for many of them the most intimate, coevolved symbiosis involves Lepiotaceae fungi (Chapela et al., 1994). In termites, such an intimate mutualism may have evolved from the habits of many Rhinotermitidae , which prefer to invade wood permeated by fungi, particularly by wet and soft rot fungi. While there is no known rhinotermitid-fungus symbiosis, the termites generally benefit nutritionally from wood conditioned by fungal mycelia, though this depends on the termite, the fungus species, and the type of wood. Some fungi, in fact, are toxic to termites. The large mounds of macrotermitines are familiar landmarks on the savannas of Africa, where most species occur. Some macrotermitines have spread to southern Asia as far as Sulawesi (but not to New Guinea or Australia). Oddly, despite the prevalence of macrotermi-
tines in Africa, Termitomyces is considered to be absent from Madagascar, and may reflect the early separation of these landmasses. The only Malagasy macrotermitines are Ancistrotermes kauderni , Microtermes sakalava Cachan , and M. divellens Sjöstadt.
The only reports of macrotermitine fossils are of nests. One is a three-dimensional, silicified fungus comb from the Late Miocene (7 Myo) of Chad, putatively of Odontotermes (Duringer et al., 2006) , though this genus is apparently poly- and paraphyletic (Inward et al., 2007). The other report concerns pillars of putatively Early Jurassic termites from South Africa, similar to those of modern Macrotermes or Amitermes (Bordy et al., 2004) . A Jurassic termitid, let alone a macrotermitine, completely contradicts fossil and phylogenetic evidence, which other-
wise indicates an entirely Tertiary origin of the Termitidae , as we discuss elsewhere in this chapter. Genise et al. (2005) provided detailed reasons as to why these pillars were even doubtfully of termites, but even if they were we must concur that “an assessment of the possibility of these [fossil nests] being modern structures made with ancient sediments should have been made” (Genise et al., 2005: 306).
The remainder of the Termitidae sans Macrotermitinae are probably monophyletic, based on the genetic evidence and a few morphological characters (such as loss of styli in soldiers and workers, and a bilobed worker pronotum). The basalmost taxon in the nonmacrotermitine Termitidae is a small group of three genera and eight species: the genera Sphaerotermes (African only) and Foraminitermes (African and Asian), and the Asian genus Labritermes (from the Malay Archipelago west of Bali). These are now placed into two subfamilies, the Sphaerotermitinae (monogeneric) and the Foraminitermitinae (which also includes Labritermes and Pseudomicrotermes ) (Engel and Krishna, 2004a). All are denizens of tropical forests, where they feed on soils. Soil feeding is a highly specialized lifestyle in termites, which evolved exclusively and multiple times among Termitidae in the lowland tropical forests of southern Asia, central Africa, and the neotropics (see the review by Brauman et al., 2000). Soil feeders consume the actual, mineralized particles of soil beneath the humus, another stratum exploited by different groups of Termitidae . Soil feeders have generally converged on a syndrome of features: very light sclerotization of the body, proportionally few soldiers per colony, and small colonies of only a few hundred to a few dozen individuals living in amorphous, subterranean nests. They comprise some two-thirds of termitid genera and nearly half of all termite species, but they are also taxonomically the poorest known guild of termites because the colonies are so obscure.
The next basal group after the Foraminitermitinae is the Apicotermitinae . In the broad sense this subfamily genetically has grouped into it Eburnitermes , Jugositermes , Allognathotermes , and Coxotermes (Inward et al., 2007) , which appear to be a grade to a definitively monophyletic group where the soldier caste has been lost (the Apicotermitinae s.l.). Apicotermitine workers of at least some genera defend the colony in a most peculiar way: as suicide bombers that douse their attackers with digesta from their exploded abdomen. The Apicotermitinae are largely forest-dwelling soil feeders in Africa, although the closely related genera Euhamitermes and Speculitermes are Asian, and the large genus Anoplotermes is Neotropical (of which there are dozens of undescribed species, and one view holds that this genus should be split into more than a dozen genera [Eggleton, 2000]). There are nine fossil species of Anoplotermes in Miocene Dominican amber (Krishna and Grimaldi, 2009).
After the Apicotermitinae , the next subfamily of Termitidae are the Cubitermitinae . These are soil feeders with highly specialized guts, some of which build earthen mounds and account for a large proportion of the animal biomass in African forest soils (Eggleton, 2000). Cubitermitinae appears to be the sister group to all of the remaining Termitidae . The subfamily is entirely African, and thus there is a clear biogeographic pattern indicating that the basal lineages of the Termitidae are African (with a few genera that spread to Asia). Almost certainly, the origin and early diversification of the Termitidae was within sub-Saharan Africa, then more derived lineages (such as various Termitinae and Nasutitermitinae ) spread throughout south-
ern Asia, Australia, and the New World.
The subfamily Termitinae presents a significant taxonomic and phylogenetic problem, since it appears to be both para- and polyphyletic (Inward et al., 2007), although monophyletic groups of termitine genera are readily defined. One such group is an Australian lineage comprised of genera that inhabit grasslands and subtropical forests such as Cristatermes, Epholotermes, Macrognathotermes , Paracapritermes , and Xylochomitermes . Another such group is a Neotropical lineage comprised of Cavitermes , Dihoplotermes , and Spinitermes , though the last of these genera is probably para- and polyphyletic. A large group of at least 10 genera occurs in various regions, including the cosmopolitan genus Amitermes (comprised of 114 described species), a group related to the so-called mandibulate genera, the entirely Neotropical Syntermitinae (Engel and Krishna, 2004a) .
Two competing hypotheses account for the origins of nasute soldiers: the diphyletic hypothesis (Emerson, 1949l; Ahmad, 1950; Sands, 1957a; Sen-Sarma, 1968; Krishna, 1970), where the nasute soldier and subsequent reduction of mandibles evolved independently in syntermitines and nasutitermitines; and the monophyletic hypothesis, where the syntermitines are interpreted as a basal grade to the nasutitermitines, which bear vestigial mandibles (Holmgren, 1912; Hare, 1937; Miller, 1986). The recent evidence from DNA sequences (Inward et al., 2007) supports a diphyletic origin and is further reflected by the structure of the frontal pore itself: it is broad, flat, and ringed with fine hairs in the syntermitines, but minute and simple in the nasutitermitines. Indeed, the frontal gland secretions of the two groups also differ. Nasutitermitines squirt secretion (which contains diterpenes [Prestwich, 1983; Prestwich and Collins, 1981b]) in a fine stream that reaches more than several times the body length. Syntermitines apply to attackers large droplets of secretion that contain no diterpenes. In several syntermitine genera such as Rhynchotermes and Armitermes , the soldier mandibles are large hooks shaped like ice tongs, which are used to grasp an attacker while smearing it with the secretion.
Closely related to the Nasutitermitinae s.s. are two distinctive, monophyletic groups. One is a small group of two genera, Orientotermes and Protohamitermes (which inhabit forests of peninsular Asia and Borneo). These and the Australian genus Invasitermes are the only other termitids besides apicotermitines that have lost the soldier caste, and where workers defend the colony as “suicide bombers” like apicotermitines. In contrast to this is another group, of more than six genera and 100 species from Asia, whose soldiers have elaborately specialized mandibles: Discupiditermes, Homallotermes , Mirocapritermes , Pericapritermes , Procapritermes , and Sinocapritermes . These soldiers have asymmetrical “snapping” mandibles, wherein the left mandible has a large kink near the middle, such that scissoring of the right mandible over the left creates a sudden snap (fig. 57). The soldier is propelled into the air if the snapping mandibles are touched to the ground, or it propels an attacker into the air if the mandibles are beneath an attacker. Interestingly, there appears to have been four origins of these bizarre mandibles in Termitidae according to Inward et al. (2007): once each in the African genus Capritermes , in the Neotropical genera Neocapritermes and Planicapritermes , and in the Oriental Dicuspiditermes and related genera.
The subfamily Nasutitermitinae s.s. is the largest monophyletic subfamily of termites, with 76 genera and approximately 600 species ( Termitinae has more species, but it is not
monophyletic). This group is defined by soldiers with vestigial mandibles and a nasus having a minute pore at the apex (figs. 22f, 57). There are some generic groups in this subfamily, most of which correspond to geographic regions. Group A, the Subulitermes group, is Neotropical; group B ( Fulleritermes group) is African; groups C, D, and E are Asian; and group F is a group of mostly grass-feeding genera that are endemic to Australia. Amongst the Asian generic groups, group C (the Hospitalitermes group) is particularly interesting, since these are darkbodied termites that forage exposed and in processions during the day (and thus resemble ants), feeding on lichens and sooty molds. The last group (G) includes the large genus Nasutitermes , which is a circumtropical genus of over 250 species, many of which construct large arboreal carton nests. Among Nasutitermes are smaller endemic genera (e.g., Coarctitermes, Malagasitermes , Trinervitermes , Tumulitermes ). While the suggestion has been made that Nasutitermes needs to be split to accomodate the endemic genera, it is probably more appropriate phylogenetically and taxonomically to synonymize at least some of these small genera into Nasutitermes . The oldest nasutitermitines are 17 species in Miocene Dominican amber, which include the soldiers of several genera and species (Krishna and Grimaldi, 2009).
SUMMARY
Termites diverged from a common ancestor with cryptocercid wood roaches some time in the latter half of the Jurassic about 150–160 Mya, though as of June, 2012 the oldest termite is the 135 Myo Baissatermes from the Early Cretaceous of Siberia. The ancestral termite was certainly wood feeding, harbored diverse symbiotic protists in its hindgut, and was social (though not necessarily having morphologically defined castes, as all termites have today). Diverse termites from later in the Cretaceous are all stem-group taxa, indicating that the divergences of the modern basal families—Masotermitidae, Termopsidae s.s., Hodotermitidae s.s., Archotermopsidae , Stolotermitidae , and Kalotermitidae —took place in the Early Cretaceous, with diversification within each of these families being probably mostly Tertiary. Extensive extinction of the living basal families rendered most of them with modern ranges that are disjunct and/or highly endemic, particularly Mastotermes (which was formerly global), as well as Archotermopsidae and Stolotermitidae . All Cretaceous and Early Tertiary termites doubtless retained ancestral features of harboring symbiotic protists and of feeding on wood, as do the basal families today along with the Rhinotermitidae (except for the havesters, Hodotermitidae s.s., which feed on grasses). With the development of the fontanelle, colonies evolved a highly effective new mechanism for defense. This, plus the development of fungus and bacterial symbioses in the Termitidae , along with profound changes in the digestive system and diverse diets (including grass, soil, and humus feeding), must have allowed the exploitation of new habitats, and eventually the construction of massive nests harboring hundreds of thousands to millions of siblings. Termites were relatively rare components of insect faunas until the diversification of family Termitidae (which contains two-thirds of all termite species) in approximately the Late Oligocene. All basal lineages of the Termitidae are African, indicating that this continent harbored the origin and early diversification of the family, sometime in the Tertiary, perhaps 45–55 Mya. The Termitidae subsequently spread throughout the world’s trop-
ics into one of the most recent radiations of an ecologically keystone animal group.
SUMMARY CLASSIFICATION OF ISOPTERA (Modified from Engel, Grimaldi, and Krishna 2009)
Genera Arranged in Alphabetical Order within Families
Order BLATTARIA Burmeister Infraorder ISOPTERA Brullé
Family † Cratomastotermitidae Engel, Grimaldi, and Krishna † Cratomastotermes Bechly
Family Mastotermitidae Desneux
† Garmitermes Engel, Grimaldi, and Krishna
† Khanitermes Engel, Grimaldi, and Krishna
Parvorder EUISOPTERA Engel, Grimaldi, and Krishna
Family incertae sedis
= † Cretatermitinae Emerson
† Asiatermes Ren
† Huaxiatermes Ren
= †Lutetiatermitinae Schlüter
= †Carinatermitinae Krishna and Grimaldi
† Carinatermes Krishna and Grimaldi
Genera incertae sedis
† Aiuruocatermes Martins-Neto and Pesenti
† Aragonitermes Engel and Delclòs
† Ardatermes Kaddumi
† Baissatermes Engel, Grimaldi, and Krishna
† Cantabritermes Engel and Delclòs
† Cretarhinotermes Bechly
† Dharmatermes Engel, Grimaldi, and Krishna
† Francotermes Weidner and Riou
† Jitermes Ren
† Mariconitermes Fontes and Vulcano
† Meiatermes Lacasa-Ruiz and Martínez-Delclòs † Melqartitermes Engel, Grimaldi, and Krishna
† Morazatermes Engel and Delclòs
† Mylacrotermes Engel, Grimaldi, and Krishna
† Paleotermopsis Nel and Paicheler
† Santonitermes Engel, Nel, and Perrichot
† Syagriotermes Engel, Nel, and Perrichot
† Tanytermes Engel, Grimaldi, and Krishna
† Yanjingtermes Ren
† Yongdingia Ren
Family † Termopsidae Holmgren , s.s.
Family Archotermopsidae Engel, Grimaldi, and Krishna
Family Hodotermitidae Desneux
Family Stolotermitidae Holmgren
† Chilgatermes Engel, Pan, and Jacobs
Family Kalotermitidae Froggatt
† Kachinitermes Engel, Grimaldi, and Krishna
† Kachinitermopsis Engel and Delclòs
Nanorder NEOISOPTERA Engel, Grimaldi, and Krishna
Family † Archeorhinotermitidae Krishna and Grimaldi † Archeorhinotermes Krishna and Grimaldi
Family Stylotermitidae Holmgren and Holmgren
† Parastylotermes Snyder and Emerson
† Prostylotermes Engel and Grimaldi
Stylotermes Holmgren and Holmgren
Family Rhinotermitidae Froggatt
Prorhinotermitinae Quennedey and Deligne
Dolichorhinotermes Snyder and Emerson
Family Serritermitidae Holmgren
Family Termitidae Latreille
Sphaerotermitinae Engel and Krishna
Eucasitermes Silvestri
Apicotermitinae Grassé and Noirot
Adynotermes Sands
Indotermes Roonwal and Sen-Sarma
Labidotermes Deligne and Pasteels
Longustitermes Bourguignon and Roisin
Syntermitinae Engel and Krishna
Macuxitermes Cancello and Bandeira
Noirotitermes Cancello and Myles
Paracurvitermes Constantino and Carvalho
Ampoulitermes Mathur and Thapa
Antillitermes Roisin, Scheffrahn, and Křeček
Caribitermes Roisin, Scheffrahn, and Křeček
Cotaritermes Matthews
Curcubitermes Li and Ping
Diwaitermes Roisin and Pasteels
Emersonitermes Mathur and Sen-Sarma
Nasopilotermes Gao, Lam, and Owen
Ngauratermes Constantino and Acioli
Niuginitermes Roisin and Pasteels
Paraconvexitermes Cancello and Noirot
Rounditermes Ensaf, Ponchel, and Nel
Xiatermes Gao and He
Cubitermitinae Weidner
Dicuspditermes Krishna
Divinotermes Carrijo and Cancello
Kemneritermes Ahmad and Akhtar
† Nanotermes Engel and Grimaldi
Onkotermes Constantino, Liotta, and Giacosa
Oriencapritermes Ahmad and Akhtar
Pseudohamitermes Holmgren
Syncapritermes Ahmad and Akhtar
Nomina dubia
†Caatingatermitinae Martins-Neto, Ribeiro-Júnior, and Prezoto † Araripetermes Martins-Neto, Ribeiro-Júnior, and Prezoto † Caatingatermes Martins-Neto, Ribeiro-Júnior, and Prezoto † Nordestinatermes Martins-Neto, Ribeiro-Júnior, and Prezoto
†Eutermitinae Holmgren
THE TAXONOMIC COMPENDIUM
In this Compendium letters after dates in citations are for identification only and do not indicate sequence of publication; thus, citations with identical dates may not appear in alphabetical order. In the few instances in which names and dates of different authors coincide, initials are given to distinguish the “outlier” from the more commonly cited investigator. Geographical coordinates (in square brackets) and Latin terms such as nom. nov. are cited exactly as they appear in the original publications and as a result are not consistent in style. All other square brackets indicate the present authors’ remarks. Contemporary names for localities are used throughout (Sulawesi, Myanmar, Sri Lanka), except where the equivalent is not clear ( Congo, Borneo) or the reference is broad (America, Africa). Historical names used by earlier authors are in parentheses. First references for valid taxa names are in bold fonts, with synonyms listed subsequently in nonbold fonts. † indicates a fossil taxon. The closing date for entries is June 2011.
NOMENCLATURAL CHANGES MADE IN THIS WORK
Eucryptotermes hagenii (Müller, 1873) . Reinstated name.
Incisitermes snyderi (Light, 1933) . Lectotype selected.
Calotermes maroccoensis Sjöstedt, 1904 ; synonymized with Kalotermes flavicollis (Fabricius, 1793) . New synonymy.
Neotermes major Snyder, 1922 ; synonymized with Neotermes connexus Snyder, 1922 . New synonymy.
Neotermes concavifrons Cachan, 1949 ; synonymized with Neotermes europae (Wasmann, 1910) . New synonymy.
Glyptotermes alaotranus Cachan, 1951 ; synonymized with Postelectrotermes longiceps (Cachan, 1949) . New synonymy.
Proneotermes delphinensis Cachan, 1951 ; synonymized with Postelectrotermes longus (Holmgren, 1910) . New synonymy.
Coptotermes mauricianus (Rambur, 1842) ; Species revivisco and new combination.
Termes arda Fabricius, 1781 . Lectotype selected.
Reticulitermes huangi Krishna , this work, nomen novum for Tsaitermes hunanensis Li and Ping, 1983 , now Reticulitermes hunanensis , a name preoccupied by Reticulitermes (Planifrontotermes) hunanensis Tsai and Peng, 1980 .
Rhinotermes (Schedorhinotermes) celebensis (Holmgren, 1911) . Lectotype selected.
Schedorhinotermes robustior Silvestri, 1909 . Status novus.
Schedorhinotermes tenuis (Oshima, 1923) . New combination.
Parahypotermes Zhu et al., 1990 ; synonymized with Hypotermes Holmgren, 1913 . New synonymy.
Hypotermes manyunensis (Zhu and Huang, 1990) . New combination.
Hypotermes ruiliensis (Zhu and Wang, 1990) . New combination.
Hypotermes yingjiangensis (Huang and Zhu, 1990) . New combination.
Macrotermes zhui Krishna , this work, nomen novum for Macrotermes latinotus Zhu and Luo, 1985 , which is preoccupied by Macrotermes gilvus latinotus Kemner, 1934 .
Eutermes fenerivensis Sjöstedt, 1914 ; synonymized with Microtermes kauderni Holmgren, 1909 . New synonymy.
Microtermes magnoculus Krishna , this work; nomen novum for Microtermes somaliensis Sjöstedt, 1927 , as the name is preoccupied by M. somaliensis (Sjöstedt, 1912) .
Odontotermes sundaicus form esuriens Kemner, 1934; synonymized with Odontotermes billitoni Holmgren, 1913 . New synonymy.
Mirotermes (Cubitermes) natalensis form obscurus Holmgren, 1913 ; synonymized with Alyscotermes kilimandjaricus (Sjöstedt, 1907) . New synonymy.
Anoplotermes burmeisteri (Czerwinski, 1901) . New combination.
Euhamitermes shillongensis (Roonwal and Chhotani, 1960) . New combination.
Hoplognathotermes angolensis Weidner, 1974 . Status novus.
Armitermes holmgreni Snyder, 1926 synonymized with Armitermes heyeri Wasmann, 1915 . New synonymy.
Bulbitermes fulvus (Tsai and Chen, 1963) . New combination. Bulbitermes pusillus (Holmgren, 1914) . New combination. Eutermes mitis Sjöstedt, 1902 ; synonymized with Kaudernitermes laticeps (Wasmann, 1897) .
New synonymy Kaudernitermes nigritus (Wasmann, 1897) . New combination. Kaudernitermes salebrithorax (Sjöstedt, 1904) . New combination. Milesnasitermes Dudley, 1890 , Eutermes costalis Holmgren. Selected as type species. Milesnasitermes Dudley, 1890 ; synonymized with Nasutitermes Dudley, 1890 . New
synonymy. Nasutitermes crinitus Krishna and Grimaldi , this work; nomen novum for Nasutitermes pilosus
Krishna and Grimaldi, as the name is preoccupied by Nasutitermes pilosus Snyder, 1926 .
Nasutitermes hexianensis Krishna , this work; nomen novum for Havilanditermes communis Li and Xiao, 1989 , which is a junior homonym of Nasutitermes communis Tsai and Chen, 1963 .
Nasutitermes longirostris sabahicola Engel and Krishna , this work; nomen novum for Nasutitermes longirostris minor Thapa , which is a junior secondary homonym of Nasutitermes minor (Holmgren, 1906) .
Nasutitermes matangensiformis christmasensis Krishna , this work; nomen novum for Eutermes (Eutermes) matangensiformis obscurus Holmgren, 1913 , as the name is preoccupied by Eutermes (Eutermes) insularis obscurus Holmgren, 1910 .
Nasutitermes obscurus (Holmgren, 1906) . New combination.
Nasutitermes mauritianus (Wasmann, 1910a) : [Status novus as correct name for taxon].
Tenuirostritermes strenuus (Hagen, 1860) . New combination.
Eutermes (Eutermes) sandakensis Oshima, 1914c [ Eutermes (Eutermes) sandakanensis by Oshima, 1914a (unjustified emendation)].
Cubitermes bilobatus form curta Sjöstedt, 1926; synonymized with Cubitermes bilobatus (Haviland, 1898) . New synonymy.
Cubitermes fungifaber var. elongata Sjöstedt, 1924 ; synonymized with Cubitermes fungifaber (Sjöstedt, 1896) . New synonymy.
Cubitermes sankurensis form elongata Sjöstedt, 1926; synonymized with Cubitermes sankurensis Wasmann, 1911 . New synonymy.
Ophiotermes receptus (Sjöstedt, 1913) . New combination.
Procubitermes curvatus Silvestri, 1914 . Status novus.
Procubitermes sinuosus Silvestri, 1914 . Status novus.
Amitermes gestroanus (Sjöstedt, 1912) . New combination.
Microcerotermes pauliani Krishna , this work; nomen novum for Gibbotermes longiceps Cachan, 1951 (now Microcerotermes longiceps ), a junior secondary homonym of Microcerotermes longiceps Cachan, 1949 .
Microcerotermes transiens Rosen, 1912 . Status revivisco.
Pericapritermes metatus Silvestri, 1914 . Raised to species rank.
Pericapritermes emersoni Krishna, 1968 ; synonymized with Pericapritermes nigerianus Silvestri, 1914 . New synonymy.
Procapritermes dakshinae (Chhotani and Ferry, 1995) . New combination.
Procapritermes keralai (Chhotani and Ferry, 1995) . New combination.
Procapritermes zhangfengensis (Yang, Zhu and Huang, 1995) . New combination.
Pseudhamitermes longignathus (Ahmad, 1965) . New combination.
Termes capensis (Silvestri, 1914) . New combination.
MUSEUMS AND REPOSITORIES
The following abbreviations have been used for the institutions in which the type specimens are held:
ACCU Instituto de Ecología y Sistemática, Academia de Ciencias de Cuba, Capdevila, KM 3,
Boyeros, Ciudad de La Habana, Cuba AM Australian Museum, Sydney, NSW, Australia AMNH American Museum of Natural History, New York ANIC Australian National Insect Collection, CSIRO, Canberra, ACT, Australia BCOT Beihai Control Office of Termites, Guangxi, China BMNH Natural History Museum (formerly British Museum (Natural History)), London, UK BPBM Bernice P. Bishop Museum, Honolulu, Hawaii BSIPL Birbal Sahni Institute of Paleobotany, Lucknow, India CAS California Academy of Sciences, San Francisco, California CGM Cairo Geological Museum, Cairo, Egypt CHM Charlestown Museum, Charleston, South Carolina CICC Chengdu Institute of Termite Control, Chengdu, China CITC Chongqing Institute of Termite Control, Chongqing, China CMFE Civico Museo “Federico Eusebio,” Alba, Italy CMNH Chicago Museum of Natural History, Chicago, Illinois CNAR Centre National d’Appui a la Recherche, N’Jdamena, Chad COM Colombo Museum, Colombo, Sri Lanka CPT The Fundación Conjunto Paleontológico de Teruel-Dinópolis, Teruel, Spain CUMZ Cambridge University Museum of Zoology, Cambridge, UK DEIB Deutsches Entomologisches Institut, Eberswalde, Germany DGAP Divisão de Geologia e Mineralogia, Avenida Pasteur, 404, Praia Vermelha,
Rio de Janeiro, Brazil DRSJ Desert Regional Station (Zoological Survey of India), Jodhpur, Rajasthan, India DZUB Departamento de Zoologia, Universidade de Brasilia, Brasilia, Brazil DZUC Departaments de Zoologia da Universidade de Coimbra, Coimbra, Portugal DZUP Departamento de Zoologia, Univerisdade Federal do Paraná, Curitiba, Brazil DZVU Universidad de Uruguay, Montevideo, Uruguay EMAG Ernst-Moritz Arndt Collection, Museum der Stadt Greifswald, Greifswald, Germany ENAR Departamento de Entomologia, Universidade Federal Rural do Rio de Janeiro, Brazil ERMNH Eternal River Museum of Natural History, Amman, Jordan (personal collection of
H.F. Kaddumi) FACENAC Facultad de Ciencias Exactas y Naturales Agrimensura, Universidad Nacional del
Nordeste, Argentina FDFI Forest Deparment, Colo-i-Suva, Fiji Islands FESG Forest Experiment Station, Gulfport, Mississippi FIB Fujian Institute of Biology, Fuzhou, Fujian Province, China FMNH Field Museum of Natural History, Chicago, Illinois FRCS Forest Research Centre, Sandakan, Sabah, Malaysia FRI Forest Research Institute, Dehradun, Uttarakhand, India
FRIP Forest Research Institute, Peshawar, Pakistan
FSCA Florida State Collection of Arthropods, Gainsville, Florida
FTLD University of Florida, Fort Lauderdale Research and Education Center, Davie, Florida
GBW Geologischen Bundesanstalt, Wien, Austria
GIEC Guangdong (Kwangtung) Institute of Entomology, Guangzhou, China
GIF Guizhou Institute of Forestry, Guiyang, Guizhou Province, China
GIUG Geologisch-Paläotologisches Institut, Universität Göttingen, Germany
GMR Geological Museum, Rostock, Germany
GMZ Geological Museum, Zurich, Switzerland
GPIUH Geologisch-Palälontologischen Institut der Universitäd Halle, Germany
GUNR Department of Geosciences of the University of Rennes, Rennes, France
GUQ Department of Geology, University of Queensland, Queensland, Australia
HMIM Hayk Mirzayans Insect Museum, Insect Taxonomy Research Department, Plant Pests and Diseases Research Institute, Tehran, Iran
HNHM Hungarian Natural History Museum, Budapest, Hungary
HTCC Huanan Tropical Crops College Tan-Hsien (Dan-Xian) Hainan Island, China
IAH Instituto Alexander von Humbolt, Arthropod collection, Villa de Leyva, Boyac, Colombia
IARI Entomology Division of the Indian Agriculture Research Institute, New Delhi, India
IEA Instituto di Entomologia Agraria, Portici, Italy
IEIL Institut d’Estudios Illerdenses, Lleida, Spain
IFAN Instituto Fondamental d’Afrique Noir, Dakar, Senegal
IFH Institute of Forestry, Changsha, Hunan Province, China
IIAA Instituto de Investigação Agronómica de Angola, Nova Lisboa, Angola
INHM Iraq Natural History Museum, Baghdad, Iraq
INPA Instituto Nacional de Pesquisas de Amazonia, Manaus, Brazil
IPM Iwate Prefectural Museum, Morioka-shi, Iwate, Japan
IPNC Institut des Parcs. Nationaux du Conge Belge, Tervuren, Belgium = Musée Royal de l’Afrique Centrale
ISH Institut für Seefischerei , Hamburg, Germany
ISM L’Institute Scientifique de Madagascar, Tervuren, Belgium = Musée Royal de l’Afrique Centrale
IZTAS Institute of Zoology, Turkmenian Academy of Sciences, Ashkhabad, Turkmenistan
KIZK Kunming Institute of Zoology, Academia Sinica, Kunming, China
KMNH Kitakyushu Museum of Natural History and Human History, Kitakyushu,
Fukuoka, Japan
KU University of Kansas, Museum of Natural History, Lawrence, Kansas
KUEL Entomology Laboratory of Kyushu University, Kyushu, Japan
LACM Los Angeles County Museum, Los Angeles, California
LRFC L.R. Fontes Collection, São Paulo, Brazil (personal collection)
LZFD Laboratoire Zoologique, Faculté des Sciences, Dijon, France
MACN Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” e Instituto Nacional de Investigaciones de las Ciencias Naturales, Buenos Aires, Argentina
MAVC Collection of M.A. Vulcano, São Paulo, Brazil
MCFC Museu de la Ciència, la Fundació La Caixa, Barcelona, Spain
MCNA Museo de Ciencias Naturales de Álava (Álava Province), Vitoria-Gasteiz, Álava, Spain
MCZ Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts
MD Museu do Dundo, Dundo, Angola
MEUV Museu de Entomologia da Universidade Federal de Viçosa Minas Geraias, Brazil
MHNAP Muséum d’Histoire Naturelle d’Aix-en-Provence, France
MHNB Muséum d’Histoire Naturelle (Naturhistorisches Museum), Basel, Switzerland
MJG Landesmuseum Joanneum, Graz (Abteilung für Zoologie ), Austria
MLP Museo de La Plata, La Plata, Buenos Aires, Argentina
MLU Martin Luther Universität, Halle-Wittenberg, Germany
MNHA Museo Nacional de Historia Natural del Paraguay (Asunción)
MNHP Muséum National d’Histoire Naturelle, Paris, France
MNM Mainzer Naturhistorische Museum, Germany
MPEG Museu Paraense “Emiliano Goeldi,” Belém
MPUC Museum of Paleontology, University of California, Berkeley
MW Museum Wasmann, Valkenburg, the Netherlands
MZB Museum Zoologicum Bogoriense, Bogor, Indonesia
MZBB Museum Zoologicum Bogoriense, Bogor, Java, Indonesia
MZBC Museum Zoologicum Bogoriense, Cibinong, Indonesia
MZD Museum zu Déva, Transylvania, Romania
MZUF Museo Zoologico, Università, Firenze, Italy
MZUSP Museu de Zoologia, Universidade de São Paulo, Brazil
NAP Institute of Zoology, Academia Sinica (formerly National Academy of Peiping), Beijing, China
NCIP National Collection of Insects, Pretoria, South Africa
NHMB Naturhistorisches Museum, Basel, Switzerland
NHMG Naturhistoriska Museet, Göteborg, Sweden
NHMM Natuurhistorisch Museum Museum of Maastricht, Maastricht, the Netherlands
NHMW Naturhistorisches Museum, Wien, Austria
NHRM Naturhistoriska Riksmuseet, Stockholm, Sweden
NITN Nanjing Institute of Termite Control, Nanjing, China
NMBZ National Museum, Bulawayo, Zimbabwe
NMK National Museum, Nairobi, Kenya
NMM Naturhistorisches Museum Mainz, Landessammlung für Naturkunde Rheinland-Pfalz, Mainz , Germany
NMNS National Museum of Natural Science, Taichung, Taiwan
NMV Museum of Victoria, Melbourne, Victoria, Australia
NSMT National Science Museum (Natural History), Tokyo, Japan
NTU National Taiwan Univeristy, Entomology Department, Taipei, Taiwan
NWUC Northwest University, Xi’an, Shaanxi Province, China
NZAC New Zealand Arthropod Coll. Landcare Research (formerly N.Z. Arthropod Coll. DSIR), Mt. Albert, Auckland, New Zealand
ONHM Oman Natural History Museum, Muscat, Oman
OSUC Oregon State University,, Corvallis, Oregon
OUM Hope Department Entomology, Oxford University, Oxford, UK
PEFO Petrified Forest National Park Museum, Holbrook, Arizona
PIM Paleontological Institute Moscow, Moscow, Russia PNCR Institut des Parcs Nationaux du Congo et du Rwanda, Tervuren, Belgium = Musée
Royal de l’Afrique Centrale PU Princeton University, Princeton, New Jersey QITC Quzhou Institute of Termite Control, Quzhou, Zhejiang Province, China RGMC Musée Royal de l’Afrique Centrale, Tervuren, Belgium RIB Institut Royal des Sciences Naturelles de Belgique, Bruxelles, Belgium RIOU Riou, B., collection, Laboratoire de Prehistorie, Institut des Sciences de la Terre,
Dijon, France (pers. coll.) RMNH Nationaal Natuurhistorisch Museum (formerly Rijksmuseum van Natuurlijke
Historie), Leiden, the Netherlands ROMTE Royal Ontario Museum, Department of Entomology, Toronto, Ontario, Canada SAM South African Museum, Cape Town, South Africa SAMA South Australian Museum, Adelaide, SA, Australia SBP Sociedade Brasileira de Paleoartropodologia, Brazil SCSC Department Biology, St. Cloud State College, St. Cloud, Minnesota SEMK Snow Entomological Museum, University of Kansas, Lawrence SFRI Sichuan Forestry Research Institute, Chengdu, Sichuan Province, China SHNM Shangdong Natural History Museum, Jinan, Shandong Province, China SIES Shanghai Institute of Entomology, Academia Sinica, Shanghai, China SKU Syiah Kuala University, Darussalam, Banda Aceh, Indonesia SMNS Staatliches Museum für Naturkunde, Stuttgart , Germany STI Swiss Tropical Institute, Basel, Switzerland, SUM Stellenbosch University, Cape Town, South Africa TFRI Taiwan Forestry Research Institute, Taipei, Taiwan TTMB Természettudom nyi Múzeum, Budapest, Hungary UCB University of California, Berkeley, California UCRs University of California, Riverside, California UCV Universidad Central de Venezuela, Maracay, Venezuela UDLZ Universite de Dakar, Laboratorie de Zoologie, Dakar, Senegal UEFS Universidade Estadual de Feira de Santana, Brazil UFPB Universidade Federal da Paraíba, Paraíba, Brazil UGB Universidade Guarulhos, Paleontological collection, Geosciences, Guarulhos, Brazil UGCA University of Georgia, Museum of Natural History Collection of Arthropods, Athens,
Georgia UKZI Department of Zoology, University of Kerala, Trivandrum, India ULK Université Lovanium, Kinshasa, Zaire UMMZ University of Michigan, Michigan, Ann Arbor, Michigan UMZC University Museum, Department of Zoology, Cambridge, UK UONZ Depatment of Geology, University of Otago, Dunedin, New Zealand UOP University of Panama, Panama, Panama UPLE Laboratoire d’Evolution des Etres Organises (University of Paris), Paris, France UPLM Univeristy of Philippines Los Banos Museum of Natural History, Los Banos, Laguna
Province, Philippines USNM US National Museum, Smithsonian Institution, Washington, DC WITC Wuhan Institute of Termite Control, Wuhan, Hubei Province, China
YITC Yichang Institute of Termite Control, Yichang, Hubei Province, China
YPM Yale University, Peabody Museum, New Haven, Connecticut
ZAHC Zhejiang Agricultural University, Plant Protection Department, Hangzhow, China ZIHS Zoötomiska Institute, Hogskolas, Stockholm, Sweden
ZIL Academy of Sciences, Zoological Institute, St Petersburg, Russia
ZIUL Zoologischen Institut der Universität, Leipzig, Germany
ZMA Zoölogisch Museum, Universiteit van Amsterdam, Amsterdam, the Netherlands
ZMB Museum für Naturkunde an der Universität Humbolt zu Berlin, Berlin, Germany ZMH Zoologisches Museum für Hamburg, Hamburg, Germany
ZMLP Department of Zoology, University of Punjab, Lahore, Pakistan
ZMLU Zoologiska Instituet, Universitets Lund, Lund, Sweden
ZMM Moscow State University, Moscow, Russia
ZMUC Zoological Museum, University of Copenhagen, Copenhagen, Denmark
ZSI Zoological Survey of India, Calcutta, West Bengal, India
ZSID Northern Regional Station, Zoological Survey of India, Dehra Dun, Uttarkhand, India ZSIN Zoological Survey of India, Northern Regional Station, Dehradun, Uttarkhand, India ZSM Zoologische Staatssammlung des Bayerischen Staates, München, Germany
ZTI Eidgenössischen Polytechnikums (Technical Institute), Zurich
ZUPL Department of Zoology, University of Punjab, Lahore, Pakistan
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