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Taxonomy and distribution of termite fauna (Isoptera) in Riyadh Province, the Kingdom of Saudi Arabia, with an updated list of termite species on the Arabian Peninsula

The present study shows an updated synoptic list of the 30 known Isoptera of the Arabian Peninsula which are classified under four families and nine genera. Twenty-seven species are hitherto known from the Kingdom of Saudi Arabia (KSA). The present inventory of the termites of Riyadh Province (KSA) indicated three species, Anacanthotermes ochraceous (Burmeister 1839), Psammotermes hypostoma Desneux, 1902 and a rare species, Coptotermes heimi (Wasmann 1902). We present an illustrated key to species based on the soldier caste. Anacanthotermes ochraceous, and P. hypostoma are widely distributed Palearctic species whereas C. heimi seems rare and is a new record for KSA. Distribution maps for the three species are provided based on recently collected material and literature records and remarks on species habitat preference are given.


Introduction
Termites (Isoptera) are eusocial monophyletic insects (Legendre et al., 2008) composed of distinct castes including worker, soldier, reproductive, queen, and larva that are widely distributed in tropics and subtropics, where they can make up to 95% of the soil insect biomass (Eggleton et al., 1996;Bechly, 2007). Isoptera are closely related to the two other major lineages of Dictyoptera (Blattaria and Mantodea) (Inward et al., 2007;Engel et al., 2009) and it is thought to have evolved from cockroach-like ancestor 200 million years ago (Bechly, 2007;Djernaes et al., 2015). Phylogenetically, termites are separated into lower termites (Hodotermitidae, Kalotermitidae, Mastotermitidae, Rhinotermitidae, Serritermitidae, and Termopsidae) and higher termites (Termitidae) . Of the over 2600 termite species worldwide, belonging to 290 genera within 12 families and 14 subfamilies, 183 species are known to damage buildings and 83 species cause significant damage to wooden structures (Edwards and Mill, 1986;Krishna et al., 2013). Termites can be grouped into four ecological types: drywood, damp wood, harvester, and subterranean termites (Nutting and Jones, 1990). Only the subterranean termites continued contact with soil to complement moisture requirements. Subterranean termites are responsible for 80% of the economically important species. Unlike drywood termites that are easily transported from region to region, most subterranean species are restricted in their native distribution (Su and Scheffrahn, 1998).
Riyadh Province of the Kingdom of Saudi Arabia (KSA) is located at the eastern part of the Najd Plateau, in the center of the an-Nafud desert and has an area of 404,240 km 2 . The extensive urbanization projects coupled with reclamation have created a favorable environment for termite infestation (Faragalla and Al Qhtani, 2013). Recent surveys have shown that the number of termite species occurring in KSA have increased (Faragalla, 2002;Kaakeh, 2006;Faragalla and Al Qhtani, 2013;Khan et al., 2018). However, few reports are available on the termites of Riyadh Province, with numerous misidentifications included. Taxonomy of termites is challenging due to ambiguities in their diagnostic morphological characters and crypto-biotic social structure (Evans, 2010). The morphology of termite is an essential key in identifying termite species. While the worker and reproductive castes are extremely similar among species, the soldier castes are useful for species recognition. The current molecular techniques are also useful for species identification.
Termites have increasing become one of the most destructive pests (Wood and Sands, 1978;Faragalla, 1983;Faragalla, 1988) capable of reducing wooden structures to ''dust" in KSA (Nasr et al., 1978(Nasr et al., , 1980Su and Scheffrahn, 1990;Koehler et al., 1998). Therefore, we initiated a survey of the termites of Riyadh Province. An integral aspect of our study was to provide for the first time keys to the soldier caste of the termites of the Riyadh Province, assisting termite control strategies.

Sample collection
During the sampling more than 2000 termite specimens were collected from diverse habitats including drywood, damp wood, cartoon objects, dead wood of Acacia, Calotropis, Tamarix, imported wood, cartoons, woody building, dead date palm frond on wet soil, plywood, branch of live Cypress trees, and dead date palm trunk in 228 sites in Riyadh Province (Fig. 1). Surveyed sites in Riyadh Province and other sites, the KSA are shown in Fig. 1. The specimens/samples were collected by hand picking and using an aspirator. The specimens were taken to the Economic Entomology Research Unite (EERU), Plant Protection Department, College of Food and Agriculture Science, King Saud University, where they were sorted, mounted, identified, and conserved. The material was collected using aspirator and by hand picking, sorted, mounted, identified and preserved in the Economic Entomology Research Unite (EERU), Plant Protection Department, College of Food and Agriculture Science, King Saud University. Termite identification was made using Taxonomic identification of termite species is carried out using works of Chhotani and Bose (1979, 1982, 1991. Other unidentified termite species have been sorted to morpho-species. Species names in this work follow the termite online catalogue of Constantino (2020). Distribution maps were made using DIVA-GIS (version 7.5.0.0).

Abbreviation of museums
KSMA: King Saud University Museum of Arthropods, Plant Protection Department, College of Food and Agriculture Science, King Saud University, Riyadh, The Kingdom of Saudi Arabia. Throughout the work, ''s" stands for soldier(s), ''w" stands for worker(s), and SE for ''sexual(s).

Family Hodotermitidae
Members of this family feed on damp wood, with a single exception (subfamily Hodotermitinae or harvester termites), which feed on vegetation. Species of this family forage above ground. They are easily separable from other termites by the well-developed eyes. The geographic occurrence ranges from the Palaearctic Region through North Africa, the East African savannas to southern Africa.
Type locality: Egypt. Local distribution. This species occurs widely throughout the various regions of KSA, while it has a limited occurrence in the southwestern mountains (Chhotani and Bose, 1979, Nasr et al., 1978, 1980Badawi et al., 1986b) (Fig. 3).
Geographic range. A well-known Palearctic species that is wide-spread in the arid regions of North Africa, the Middle East, the Arabian Peninsula (Kuwait, Oman, Qatar, Saudi Arabia), Iraq, Iran, Afghanistan (Cowie1989), and Sudan (Sjostedt 1925;Harris 1968;Pearce et al., 1986).
Foraging/feeding substrate. The feeding and nesting habits of A. ochraceus is diverse including dead wood, dead date palm fronds, imported wood, dry grass, cartoon bags, dead Acacia, camphora, Cinnamomum and Tamarix, and sheep dung.

Family Rhinotermitidae (subterranean termites)
Species of this family build nests underground in moist soil, in buried wood or in wood lying on the ground. Geographic range. Bangladesh, Bhutan, India, Indonesia, Nepal, Oman, Pakistan, UAE. This species is recorded for the first time from the KSA (Fig. 4).
Foraging/feeding substrate. This species was found nesting in dead wood of Acacia, and Tamarix, plywood, imported wood, dead date palm trunk and date palm fronds.

Discussion
There is a specific difference between the armature of the right mandible and the left mandible of A. ochraceous and P. hypostoma, the former species has the left mandible with 5-7 teeth, and the right mandible with 4-5 teeth, whereas the later species has the left mandible with a terminal tooth and three marginal teeth while the right mandible with a terminal tooth and two marginal teeth.
This morphological mandibular asymmetrical trait is used to dismember ants (Seid et al., 2008).
The geographic location of the Arabian Peninsula at the interchange of three zoogeographical realms, the Palearctic, the Afrotropical and the Oriental, results in a mixing of faunal elements from these regions, especially from the Palearctic and the Afrotropical. In addition, there are limited number of endemic taxa (Larsen, 1984;Cowie 1989;Delany, 1989;Penati and Vienna, 2006;Sharaf et al., 2020). The lack of systematic revisions and taxonomic keys is a challenge toward the identification of Arabian termite species. During the present work only two Palearctic species were collected from the Riyadh Province, A. ochraceous and P. hybostoma which are fairly abundant in the deserts of the Arabian Peninsula and their geographical range extends south to several locations in the southwestern mountains (Chhotani and Bose, 1979).
According to literature records and our records, it is apparent that A. ochraceous and P. hybostoma are the two most widely occurring termite species in the KSA but the later species has apparently a wider geographical distribution, no doubt because of available habitats. Psammotermes hybostoma prefers the dry habitats therefore it is rarely represented in the southwestern mountains of the KSA due to the higher percentage of precipitation, moist soils, and lower air temperatures .
Coptotermes heimi is a common invasive species native to India, Nepal, and Pakistan (Chouvenc et al., 2016) thriving in deserts habitats of countries of the Arabian Peninsula including the United Arab Emirates (UAE) and Oman. It is anticipated that this species occurring over a wider geographic range, especially in the vast desert regions of the KSA and the rest of the neighboring countries such as Kuwait, Qatar and Bahrain.

Conclusions
In the present study an updated synoptic list of the 30 hitherto known Arabian Isoptera is given of which 27 species are recorded from the KSA. During our survey in Riyadh Province three species are sampled, keyed and illustrated, A. ochraceous (Burmeister), P. hypostoma Desneux, and C. heimi (Wasmann). Anacanthotermes ochraceous, and P. hypostoma are widely distributed on the Arabian Peninsula whereas C. heimi appears rare in the region. We give distribution maps for the collected species and present notes on species habitat preference. It is hoped that future collecting will add additional records of termites for the Arabian Peninsula.

Funding
This work was funded by the National Plan for Science, Technology and Innovation (MAARIFAH), King Abdul-Aziz City for Science and Technology, Kingdom of Saudi Arabia (Award Number 13-BIO1410-02).

Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.