Revision of the termite family Rhinotermitidae (Isoptera) in New Guinea

Abstract Recently, we completed a revision of the Termitidae from New Guinea and neighboring islands, recording a total of 45 species. Here, we revise a second family, the Rhinotermitidae, to progress towards a full picture of the termite diversity in New Guinea. Altogether, 6 genera and 15 species are recorded, among which two species, Coptotermes gambrinus and Parrhinotermes barbatus, are new to science. The genus Heterotermes is reported from New Guinea for the first time, with two species restricted to the southern part of the island. We also provide the first New Guinea records for six species of the genera Coptotermes and Schedorhinotermes. We briefly describe soldiers and imagoes of each species and provide a key based on soldier characters. Finally, we discuss the taxonomic and biogeographical implication of our results. A replacement name, Schedolimulus minutides Bourguignon, is proposed for the termitophilous staphylinid Schedolimulus minutus Bourguignon, to solve a question of secondary homonymy.


Introduction
The Rhinotermitidae constitute one of the most widespread termite families, including numerous pest species. First established under the invalid name Mesotermitidae (Holmgren 1910a, b), then reestablished as Rhinotermitidae by Light (1921), the family originally included all termites possessing a fontanelle and a frontal gland in the imago and soldier castes, 8 malpighian tubules and hindgut with short anterior (prepaunch) sections. Later on, the Stylotermitidae and Serritermitidae were separated as distinct families (Chatterjee andThakur 1964, Emerson 1965), a position recently endorsed by Engel et al. (2009). The Rhinotermitidae now comprise several genera of uncertain affinities, such as Prorhinotermes, Termitogeton and Psammotermes, and two well-supported clades: (i) the Rhinotermitinae, including Parrhinotermes, Schedorhinotermes and the neotropical Rhinotermes-group; (ii) the Heterotermitinae + Coptotermitinae, comprising Reticulitermes, Heterotermes and Coptotermes. As presently defined, the Rhinotermitidae might still be paraphyletic with respect to the Serritermitidae or Termitidae, but the actual phylogeny of this group remains uncertain (Lo et al. 2004, Ohkuma et al. 2004, Inward et al. 2007. The Rhinotermitidae are widely distributed across tropical, subtropical and temperate regions (Eggleton 2000). Whereas the genus Prorhinotermes is notable for its pantropical insular distribution (Emerson 1952), other genera are either pantropical (e.g. Coptotermes) or limited to one (e.g. Termitogeton) or a few zoogeographic areas (e.g. Schedorhinotermes). In southeast Asia, the Rhinotermitidae are represented by six genera: Parrhinotermes, Schedorhinotermes, Coptotermes, Heterotermes, Prorhinotermes and Termitogeton. All but the last one are also present in Australia. The former two belong to the subfamily Rhinotermitinae, whose soldiers are equipped to bite and smear a poisonous liquid with their elongated brush-like labrum (Quennedey and Deligne 1975). In the other genera, soldiers can simultaneously bite and emit a toxic or sticky chemical secretion from their frontal gland (Prestwich 1979(Prestwich , Šobotník et al. 2010a. Alates are also equipped with a frontal gland, variously developed according to the genus (Šobotník et al. 2010b).

Biological material
Extensive termite collecting was carried out by J. M. Pasteels (in collection records: JMP), Y. Roisin (YR) and M. Leponce (ML) in New Guinea and some neighboring islands between 1978 and 1995 although records from Indonesian Papua are almost exclusively limited to the "bird's neck" area, around Nabire and Kaimana (Figs 30,82). Termite specimens were collected with tweezers and preserved in 80% alcohol or fixed in Bouin's fluid or in a formol-alcohol-acetic acid (20:75:5) mixture. We also had the opportunity to examine samples collected in alcohol by Alfred E. and Eleanor Emerson in 1962-1963, as well as a few samples from other sources. Localities where specimens were collected are given as well as their approximate geographic coordinates (Appendix 1), obtained by cross-checking maps, Google TM Earth positioning and the National Geospatial Agency GEOnet Names Server (http://geonames.nga. mil/ggmagaz/).

Systematic characters
This study is based on the morphology of soldier and alate castes. Soldiers supply most of the important taxonomic information at the species level. The following characters are of major interest: size, general shape of the head, shape of mandibles, shape of postmentum, pilosity of head and number of antennal articles. Alates, when available, may give taxonomic information at the species level by the general shape of their head and pronotum.

Measurements and their abbreviations
The measurements used, detailed below, follow the guidelines of Roonwal (1970).

Microscopy
For scanning electron microscopy, specimens were dehydrated in a conventional ethanol series, impregnated for 24 h in hexamethyldisilazane, air dried and gold coated. Digital images were taken with a Philips XL 30 ESEM.

Collections and their abbreviations
Species determinations were carried out after comparison with type series or identified specimens kept in the following museums hairy. Fontanelle very large, directed forward, through which the latex-like secretion of the frontal gland is discharged. Labrum short, triangular-shaped. Mandibles narrow and elongated, curved at tip; right mandible without subsidiary teeth and serrations; left one with a basal tooth and serrations. Antennae with 12 to 16 articles.
Distribution. The genus Coptotermes is broadly distributed, occurring in all tropical and subtropical regions. It comprises species adapted to all major biomes, from tropical rainforest to arid steppes and deserts. Nests are generally found in logs, in the heartwood of living trees, or underground (Emerson 1971). Several species, such as Coptotermes formosanus, are major pests of buildings (Su and Scheffrahn 2000).
Distribution. (Fig. 30). This species is widespread in New Guinean forests. It also occurs in New Ireland. It has also been reported from the following localities, but the relevant material was not examined: Bukaua (as C. hyaloapex : Holmgren 1911a), Popondetta (Gay 1963). According to Gathorne-Hardy (2004), it is present from Peninsular Malaysia throughout Sundaland.

Coptotermes remotus
Soldier. (Figs 12-15). Soldiers of small size. Head slightly longer than broad, covered by about 20 setae. Fontanelle with opening directed forward, not visible from above. Antennae generally with 14 articles, but occasionally with only 13 articles. Pronotum larger anteriorly than posteriorly, trapezoid-shaped, covered by about 50 setae. Mandibles with tips extremely curved. Right mandible with four serrations. Measurements (mm) of 5 soldiers from the type colony and 72 soldiers from 24 colonies (parentheses): HLF: 1.11-1. 19  Comparisons. This species shows variation in size along its distribution range although no consistent characters allowed us to split it up. Coptotermes remotus most resembles the Australian species C. lacteus and the Malayan ones C. bentongensis and C. sepangensis. These last two species occur in sympatry and are morphologically undistinguishable, making them probable synonyms. Soldiers of C. remotus can be distinguished from other New Guinean species by their small size and mandibles curved at the tip.
Distribution. This species, originally described from Kavieng, New Ireland, is widespread throughout New Guinean forests. It is abundant in the bird's neck area of Indonesian Papua, but only a few specimens were collected from Papua New Guinea (Fig. 31). Termitophiles. Coptophysella pulposa (Coleoptera: Staphylinidae) was found in colony #PNGT795 of this species in Hatzfeldthafen (Roisin and Pasteels 1990). A possibly new species of Coptophysella was also found in colony #IRJT12 in Pusppenssat-IrJa (new record). New synonymy. In his revision of termites from Australia, Hill (1942) mentioned that soldiers of C. grandiceps and C. obiratus are morphologically indistinguishable, the two species being potential synonyms. After examining material of the two species, we reached the same conclusion and therefore consider C. obiratus as a junior synonym of C. grandiceps.

Coptotermes grandiceps
Imago. (Figs 16-17). Head moderately hairy. Pronotum covered by many setae of medium size. Antennae with 20 articles. Measurements (mm) of 6 imagoes from one colony: TBL: 6.08-7.55; HLC: 1. 19 Comparisons. This species is closely allied to C. pamuae from which it can be distinguished by its larger soldiers with more curved mandibles.
Distribution. (Fig. 30). C. grandiceps, originally described from the Solomon Islands, occurs in southern New Guinea and the Papuan peninsula.  Comparisons. This species is closely related and imperfectly separated from Coptotermes grandiceps. However, the size and morphological differences between the two species are high enough to retain them as distinct taxa, even though some individuals cannot be unambiguously assigned. The same was already observed in the related Australian species Coptotermes acinaciformis Froggatt, which is believed to form a species complex (Brown et al. 1990). The main criteria differentiating C. pamuae from C. grandiceps are its smaller soldiers with less hairy pronotum and less curved mandibles.

Coptotermes pamuae
Distribution. (Fig. 31). This species, originally described from the Solomon Islands, was only collected in southern Papua New Guinea (Fly savannas and the Port Moresby region).
Distribution. (Fig. 31). This species occurs in Eastern New Guinea and in New Britain. Etymology. We named this species in honor of Gambrinus, a legendary character from Flanders, famous for enjoying life.  Type species. Heterotermes platycephalus Froggatt, 1897, by monotypy.
Diagnosis. Imago head roughly oval, narrower anteriorly than posteriorly. Fontanelle small, located in the middle of the head. Eyes small and flat. Ocelli situated in front of the head, before eyes. Antennae generally with 15 to 19 articles. Pronotum elongated, narrower than head. Soldier head long and narrow, rectangular-shaped. Fontanelle small, circular, situated forward. Labrum short to medium-sized, about half as long as mandibles. Mandibles sabre-shaped, slightly curved at tips. Left mandible with a tooth and some serrations at the base. Right mandible without basal tooth and serrations. Antennae with 13 to 18 articles.
Distribution. Most species of Heterotermes are tropical (Emerson 1971). This genus was known from the Neotropics, northern Africa, Asia (from the Arabic peninsula to Indonesia), and Australia, occurring from humid forests to desert edges. Here, we extend its known distribution to southern New Guinea. (Hill, 1927) http://species-id.net/wiki/Heterotermes_vagus New synonymy. Hill (1942) pointed out the similarity of H. venustus and H. vagus, but maintained both names arguing that H. venustus has a larger labrum and antennae with more articles. However, after comparing the type series of both species, we did not notice any difference in these characters, nor in any other morphological feature. For this reason, we consider these two species as synonyms and hereby give precedence to Heterotermes vagus.

Heterotermes vagus
Imago. Unknown from New Guinea (see Hill 1942 for further details). Distribution. (Fig. 44). This species was collected in Sourthern Papua New Guinea. It is also known from northernmost Queensland and Northern Territory (Australia) (Watson & Abbey 1993 Comparisons. Morphological variation occurs along the distribution range of H. paradoxus, though it appears insufficient to recognize distinct species. H. paradoxus differs from H. vagus by the larger size of its soldiers, its less elongated labrum with rounded end and its antennae with 16 or 17 articles. Distribution. (Fig. 44). This species is widespread in southern Papua New Guinea, and was found on both coasts of the "bird's neck" in Indonesian Papua. It is also known from northern Australia, especially Queensland (Watson & Abbey 1993). It occurs in savanna as well as in forest. Diagnosis. Imago head approximately circular, with fontanelle situated between eyes. Frons with a slightly visible groove. Labrum short, inclined downward, without groove. Antennae with 16 or 17 articles. Pronotum relatively short, generally of the same width or slightly narrower than head. Soldier head rectangular to ovoid. Frons and clypeus with a groove, from the narrow fontanelle to the beginning of the labrum. Labrum elongated, crossed by a groove in the middle, and garnished with an apical brush. Base of mandibles serrated. Left mandible with two subsidiary teeth. Right mandible with one subsidiary tooth. Antennae with 13 articles.

Genus
Distribution. This genus is known from the Oriental region, northeastern India, the Papuan region and northern Australia (in northern Queensland) (Emerson 1955, Tho 1992. It occurs in tropical rainforest where it nests in dead logs. (Harris, 1958  Distribution. (Fig. 55). This species, originally described from the Solomon Islands, is common in Northern New Guinea and in the bird's neck area.

Parrhinotermes barbatus
Distribution. (Fig. 55). This species is common in southern New Guinean forests, and was also collected once in Indonesian Papua.
Termitophiles. The four species of Parrhinopsenius found with Parrhinotermes browni were also found with this species, previously referred to as Parrhinotermes nr. queenslandicus (Bourguignon et al. 2007).
Etymology. We named this species after the latin "barba", referring to the postmentum of its soldiers fully covered by setae.   Diagnosis. Imagoes very similar to those of Parrhinotermes. Head approximately circular in shape. Fontanelle situated in the middle of the head. Frons with a slightly visible groove. Labrum short, inclined downward, without groove. Soldiers generally dimorphic and sometimes trimorphic. All species described here have dimorphic soldiers, excepted S. seclusus in which the minor soldiers can sometimes be further separated into two morphs (Miller 1987). Minor soldiers with elongated head. Frons and clypeus with a groove in the middle that joins the opening of the fontanelle to the labrum. Labrum elongated, crossed by a groove in the middle, ending in a brush. Mandibles long and slender. Left mandible with two short subsidiary teeth. Right mandible with one short subsidiary tooth. Major soldiers with labrum proportionally shorter than in minor soldiers. Frons and clypeus with a groove in the middle, from the fontanelle to the labrum. Labrum short and large, with a groove in the middle and an apical brush. Mandibles stout and strongly curved. Left mandible with two large subsidiary teeth. Right mandible with one large subsidiary tooth, as well as a hump at the base. Major soldiers supply more relevant systematic information to distinguish species.
Distribution. This genus is known from Africa, Southeast Asia, the Papuan region and Australia (Emerson 1955, Harris 1968 (Hill). Watson et al. 1998: 197. Comparisons. This species is easily distinguishable from others by its large size and its densely hairy abdomen in the minor and major soldier castes. Minor soldiers are highly variable in size, indicating the likely presence of two developmental subcategories (Miller 1987).
Distribution. (Fig. 82). This species is widespread throughout southern Papua New Guinea. It is also known from Queensland, Australia.
Major soldier. (Figs 69, 71-72). Soldiers of small size. Head, excluding labrum, square-shaped, slightly longer than wide, covered by about 10 setae. Labrum slightly longer than wide, reaching the tip of mandibles. Antennae with 15 or 16 articles. Pronotum covered by 6 long setae disposed in each corners. Mesonotum and metanotum with 4 long setae. Abdomen with 6 long setae per segment, plus sometimes 1 or 2 smaller ones. Mandibles strongly curved at tip with short subsidiary teeth. Left mandible with 2 subsidiary teeth of the same length. Right mandible without hump at the basis. Measurements (mm) of 1 major soldier from the type colony of S. longirostris, 2 major soldiers from the type colony of S. dimorphus [brackets], and 77 major soldiers from 29 colonies (parentheses) Comparisons. This species can be distinguished from other New Guinean species by the number of setae on the pronotum (6 per segment), mesonotum (4), metanotum (4) and abdomen (6) in the major soldier caste.
Distribution. (Fig. 82). This species is common in forested areas throughout New Guinea. It probably also occurs in Indonesia, since it was described from the Nicobar islands.
Termitophiles. Several Aleocharinae (Coleoptera, Staphylinidae) were found with this species. Schedotermoecia kaimanensis (Coptotermoeciina) was described from colony #IRJT142, and its congener S. papuana from #PNGT1165 (Bourguignon & Roisin 2006). The following Trichopseniini also occur with this species: Schedolimulus elongatus, S. planus and S. minutides Bourguignon, nomen novum (here proposed as replacement name for S. minutus Bourguignon, 2007, to     S. marjoriae was described by Snyder (1925) based on specimens collected in the Solomon Islands. He pointed out its resemblance with S. translucens and gave as sole character to distinguish these species the morphology of major soldier mandibles. After examination of samples of S. marjoriae and S. translucens, we found that differences between soldier mandibles of the two alleged species are by far smaller than variation observed among New Guinean specimens. For this reason, we also consider S. marjoriae as a junior synonym of S. translucens.

Type species. Prorhinotermes inopinatus
Diagnosis. Imago head oval to circular-shaped, with ocelli located before the well developed eyes. Fontanelle situated in the middle of the head. Antenna with 19 to 22 articles. Pronotum narrower than head. Soldier head variable in shape, often larger posteriorly than anteriorly. Fontanelle narrow, placed at anterior third of the head. Frons with a groove in the middle from opening of fontanelle to clypeus. Eyes present as hyaline spots, more or less developed. Antennae with 13 to 20 articles. Pronotum generally wide. Mandibles elongated, left one with a short marginal tooth at the basis, right one without marginal teeth. Soldiers and workers very variable in size (Tho 1992).

Prorhinotermes inopinatus
Diagnosis. Imagoes densely hairy. Head larger posteriorly than anteriorly. Fontanelle very narrow, placed in the middle of the head. Eyes small. Antennae with 10 to 15 articles. Pronotum very small, half as broad as head. Wings without median and radial vein (Krishna 1970). Soldiers densely hairy, with characteristic heart-shaped, dorsoventrally flattened head. Antennae generally with 13 to 15 articles. Labrum roughly triangular-shaped. Mandibles elongated, without marginal teeth. Pronotum half as broad as head.
Distribution. (Fig. 93). In New Guinea, this species was only collected in the bird's neck area (western Indonesian Papua). Originally described from from Sarawak (Haviland 1898), it is also known from Sabah (Thapa 1982) and Peninsular Malaysia (Tho 1992). 1 Mandibles sabre-like, without subsidiary teeth (Figs 14-15 Head rounded to ovoid, with broad fontanelle opening in front (Fig. 12)  Soldier flattened with heart-shaped head (Fig. 88)  Head with a small hump anteriorly (Fig. 33) Postmentum completely covered by setae (Fig. 52)  -Postmentum covered by setae only in the anterior part (Fig. 47)  Major soldier head rounded, with stout mandibles (Fig. 62)  Abdomen of major soldier with more than 20 setae per segment ..S. seclusus -Abdomen of major soldier with less than 20 setae per segment ...S. translucens

Discussion
This study reveals that the richness of Rhinotermitidae in New Guinea is much higher than the 8 species previously recognized. Overall, we found 6 genera and 15 species, a diversity which appears slightly lower than that of neighboring areas such as Peninsular Malaysia (6 genera, 24 species (Tho 1992)), Sabah (6 genera, 19 species (Thapa 1982)) and Australia (5 genera, 23 species (Watson and Abbey 1998)). However, these richness figures deserve closer scrutiny, because several species are known only from their original description. Furthermore, the Rhinotermitidae display several characteristics predisposing them to synonymy. (i) In several genera, soldiers may be derived from a series of larval or worker instars, producing a substantial variation in size and number of antennal articles (Hanus et al. 2006). Differences are especially conspicuous between incipient and mature colonies. Therefore, these criteria, though frequently used, are of limited value for species discrimination. (ii) Wood feeders are generally good dispersers and can easily cross salt water gaps by rafting (Eggleton and Tayasu 2001). Extensive colonization of islands and large intercolonial variability favored multiple descriptions of single species under different names along their distribution range. Some pruning, as initiated by Gathorne-Hardy (2004) who placed 11 species of Rhinotermitidae from Sundaland and the western Pacific into synonymy, is clearly needed. On the other hand, the existence of cryptic species has been documented in several Rhinotermitidae (Heterotermes, Watson et al. 1989;Coptotermes, Brown et al. 1990;Reticulitermes, Copren et al. 2005) and Termitidae (Macrotermes, Bagine et al. 1994;Cubitermes, Roy et al. 2006), so that morphologically homogenous taxa might have to be split when submitted to detailed chemical or molecular analyses. The distribution patterns of rhinotermitid species match those found in termitids (Roisin 1990, Roisin and Pasteels 1996, 2000, Bourguignon et al. 2008. The central mountain range constitutes a barrier for several species, as in the genus Parrhinotermes where P. browni occurs almost exclusively on the north slope, while P. barbatus occurs in the south. In a similar way, Heterotermes is completely missing in the northern part of New Guinea but is represented by two species, also present in Australia, in the south, like the nasute genus Niuginitermes (Roisin and Pasteels 1996). Interestingly, northern and southern species meet in the bird's neck area, where several low valleys connect the two coasts. A second barrier shaping termite species distribution in New Guinea is the ecotone between southern Papuan savannas and the forest-covered areas to the north. Typically, the invertebrate fauna of Papuan savannas shows close affinities with that of northern Australia, whereas forested areas of New Guinea mainly harbor species with Oriental affinities (Gressitt 1982). This situation is illustrated by Heterotermes vagus and Coptotermes pamuae, which were only found in southern Papuan savannas but also occur in Australia (Hill 1942). Among the Termitidae, at least 11 species (e.g., Amitermes arboreus, Nasutitermes triodiae, Microcerotermes taylori, Lophotermes aduncus) are in this case (Roisin 1990, Miller 1994, Roisin and Pasteels 1996, 2000, Bourguignon et al. 2008. Fewer species inhabiting Papuan and northern Australian savannas penetrate deep into southern forests, but Schedorhinotermes seclusus and the termitid Ephelotermes cheeli do (Bourguignon et al 2008). Heterotermes paradoxus was also found in forests in the bird's neck area. East-west patterns are less conspicuous than north-south ones, but some termitid species show a longitude-restricted range: the genus Hospitalitermes, of clear oriental origin, was not found east of Nomad (Roisin and Pasteels 1996), whereas Microcerotermes piliceps is restricted to eastern Papua New Guinea and islands further east (Roisin and Pasteels 2000). Here, two species known from as far west as the Malay peninsula, Schedorhinotermes malaccensis and Termitogeton planus, were recorded only from the bird's neck area, but their eastern limits are unknown due to the near absence of termite samples from the huge area between the bird's neck region and the Papua New Guinean border (141° E meridian).
We expect the rhinotermitid diversity found in this study to reflect the overall richness of the island, although it is inevitable that some rare or locally distributed taxa escaped detection. Two regions are particularly likely to host undiscovered taxa: (i) southern Papuan savannas, in which our collecting effort was limited, possibly host additional taxa of Australian affinities; (ii) as stated above, the western half of New Guinea (Indonesian Papua) was also poorly explored and is therefore likely to conceal further taxa of Oriental origin, in the vein of Termitogeton planus and Schedorhinotermes malaccensis.