Formosan Subterranean Termite (Isoptera: Rhinotermitidae) Established in Grand Bahama

The Formosan subterranean termite, Coptotermes formosanus Shiraki (Isoptera: Rhinotermitidae), is a significant invasive pest that originates from southern China (Kistner 1985, Sociobiology 10: 93–104) and Taiwan (Li et al. 2009, Ann. Entomol. Soc. Am. 102: 684–693). It is one of the most widely distributed and destructive subterranean termite pest species in the world (reviewed by Evans et al. 2013, Annu. Rev. Entomol. 58: 455–474). It typically is found in warm, humid areas in temperate to subtropical regions within latitudes 35°N and 35°S (Su and Tamashiro 1987, Biology and Control of the Formosan Subterranean Termite, Univ. Hawaii, 3–15).

To date, C. formosanus has not been formally reported from the Caribbean Basin. An online search (16 June 2017) lists a single report of C. formosanus in the Caribbean (CABI/EPPO 2008, Distribution Maps of Plant Pests, Centre for Agriculture and Biosciences International, Map 710), but this U.S. Virgin Islands (USVI) record is in error since CABI's bibliographic reference (Su et al. 2003, Am. Entomol. 49: 20–32) describes a bait study targeting Heterotermes sp. on St. Croix, with only ancillary information regarding C. formosanus. Furthermore, C. formosanus is not reported in the two most recent termite surveys in the USVI (Nalepa and Jones 2002, Sociobiology 39: 155–163; Scheffrahn et al. 2003, Ann. Entomol. Soc. Am. 96: 181–201).

An invasive congener, Coptotermes gestroi (Wasmann), the Asian subterranean termite, is more widely distributed than C. formosanus and occurs on many islands throughout the Caribbean (Evans et al. 2013). Coptotermes gestroi is endemic to Southeast Asia and generally is found in tropical regions. In the continental United States, these two Coptotermes species are sympatric only in tropical south Florida (Scheffrahn 2013, Fla. Entomol. 96: 781–788). Although Florida and the Bahamas are separated by only 80.5 km, C. gestroi is the sole representative of the genus in the Bahama Archipelago and has been found only on Providenciales and Grand Turk (Scheffrahn et al. 2006, Ann. Entomol. Soc. Am. 99: 463–486). Coptotermes formosanus has not been formally documented from the Caribbean, and Scheffrahn et al. (2006) speculated that C. gestroi eventually would become established in the Bahamas.

Herein, we report that C. formosanus is the first member of the genus to become established in the Bahamas. H.S.F. discovered C. formosanus on Grand Bahama while inspecting a commercial establishment in Freeport on 31 August 2010. The discovery was reported 2 d later in a local Bahaman newspaper, The Freeport News.

We document C. formosanus infestation sites based on samples and records that H.S.F. and O.J.F. compiled while conducting termite inspections and treatments for their family-owned pest management company, which is the largest of six service providers on Grand Bahama and covers the entire island and cays. Termite samples were sent to S.C.J. to confirm species identification. Taxonomic characters and phylogenetic methodology were used to verify the species. We extracted DNA from termites using the DNeasy Blood and Tissue Kit (Qiagen Inc., Valencia, CA) then used polymerase chain reaction on a region of two maternal mitochrondrial genes, 16S rRNA and cytochrome oxidase subunit II (COII), for each of 18 individual termites as described in Eaton et al. (2016, J. Insect Sci. 16: 111). A phylogenetic tree was generated for each gene using our sequences and those from GenBank. Our Bahaman 16S and COII sequence data were deposited into GenBank (accession numbers: MF410719–MF410753).

Additionally, we analyzed a nuclear locus, the internal transcribed spacer (ITS) array, from 10 of the abovementioned termites, including soldiers, workers, and male and female alates. A nuclear locus provides genetic insights into both parents and therefore can reveal hybrids of C. formosanus and C. gestroi in the field. Chouvenc et al. (2015, PLoS One 10: e0120745) raised the concern of potential hybridization of these two invasive species after observing concurrent swarms in south Florida wherein C. gestroi males preferentially engaged in mating behavior with C. formosanus females. Furthermore, in the laboratory, these heterospecific incipient colonies had twice the growth rate of conspecifics, which suggested potential hybrid vigor. However, alate hybrid fertility is currently unknown, and it will take years before alates, if any, are produced in these laboratory colonies.

Fig. 1 indicates localities with C. formosanus in Freeport, Grand Bahama, from its discovery in May 2010 through mid-June 2017. To date, the majority of C. formosanus infestations and sites with identified alates have occurred in the general vicinity of Lucaya Beach and the Port Lucaya Marina in southcentral Freeport. This marina or the associated inlet may represent the initial introduction site of the species on Grand Bahama. Maritime activities play an important role in the spread of Coptotermes spp., and land-based infestations often are near marine docks with infested boats (Hochmair et al. 2013, Fla. Entomol. 96: 746–755). The three Bahaman infestations that are farthest from the marina include two near the western boundary of Freeport and one at the eastern boundary of the city, suggesting that humans are further spreading the species on Grand Bahama. In the United States, the Formosan subterranean termite has spread inland primarily through movement of infested wood, especially reused railway ties, potted plants, and furniture (Evans et al. 2013).

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The first alates (winged reproductives, imagos) of C. formosanus were collected in 2015 at two localities shown in Fig. 1. The initial collection was from a swarm that occurred at approximately 9–10 p.m. on 6 May 2015 at a residence in the Arden Forest subdivision inland from the marina; swarmers were reported as being seen for at least 2 yr at this residence. A week later, on 12 May 2015, C. formosanus swarmers, soldiers, and workers were collected from a condominium situated approximately 2 km SSE of the residence. In May, the wind direction is generally ESE or SE, and it is highly unlikely that swarmers were blown from a distant location to the condo. A recent study in Hawaii found that swarming of C. formosanus was reduced at higher wind speeds (Tong et al. 2017, Insects 8: 58). In 2017, C. formosanus alates were collected from late May through mid-June at three of four sites, including in multiple buildings on a large property indicated by the “X” (Fig. 1).

The presence of alates is significant because they indicate a mature parent colony, and swarms allow for potential outbreeding and further dispersal of the species. Colonies of C. formosanus take 5 to 10 yr to begin producing alates (King and Spink 1974, Ann. Entomol. Soc. Am. 67: 953–958), and the discovery of C. formosanus on Grand Bahama occurred 5 yr before swarms were recognized, indicating that this species may have been detected shortly after its introduction. Evans et al. (2013) note that new termites on islands tend to be more rapidly detected than those on continents. Nonetheless, the year and mode of this species' introduction into Grand Bahama are unknown.

Phylogenetic analyses revealed that alates from the 2015 collection sites in Freeport shared identical gene sequences at the 16S locus and the COII locus. The C. formosanus samples from Grand Bahama grouped together in a single, large haplotype (F) with 69 of 89 16S sequences from GenBank (Fig. 2), which represent C. formosanus samples from China, Japan, Taiwan, and the continental United States, including Florida, Georgia, and Louisiana. Similarly, C. formosanus samples from Grand Bahama grouped together in a single, large haplotype with 54 of 170 COII sequences from GenBank, which also included collections from China, Japan, Taiwan, and the United States. This haplotype includes GenBank number EU805770, which is the C. formosanus mitochondrial marker inherited by hybrid offspring fathered by C. gestroi (Chouvenc et al. 2015). Neither of our two phylogenetic trees showed divergence of the C. formosanus haplotypes. This indicates low genetic diversity, which is a characteristic of invasive populations of C. formosanus (Husseneder et al. 2012, Biol. Invasions 14: 419–437).

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Coptotermes formosanus alates from Grand Bahama are somewhat variable in color, but they tend to be very dark brown. The color of their head and thorax (dorsal view) is very similar to that of C. gestroi shown in Scheffrahn et al. (2015, Arthropod Syst. Phylo. 72: 333–348), although they lack the two lighter “antennal spots” of C. gestroi (Su and Scheffrahn 1998, Proc. Hawaii. Entomol. Soc. 33: 13–18). By contrast, in south Florida, the golden brown abdomen of the Formosan subterranean termite alate is easily distinguished from the nutty brown abdomen of the Asian subterranean termite alate (see supplemental data in Chouvenc et al. 2015). Although Scheffrahn et al. (2015) assert that Coptotermes spp. imagos can be “easily identified by wing and body coloration,” our data indicate that imago body coloration is not a reliable character for distinguishing C. formosanus and C. gestroi in some regions. These similarities in imago body coloration may hamper the rapid detection of a future introduction of C. gestroi into the Bahamas.

Wing coloration is useful for identification of Bahaman C. formosanus alates, particularly if one focuses on venation near the basal suture of the forewings. In Bahaman C. formosanus, the media, cubitus, and subordinate veins are darker for approximately the first millimeter of their length whereas these veins are lighter and less obvious in C. gestroi. Alates have a brownish tint beneath the radial sector vein, but the brownish halo associated with the costal margin of the C. formosanus wing (Scheffrahn et al. 2015) is so limited on Bahaman alates as to have almost no utility in identification.

The darker color of C. formosanus alates from the Bahamas may indicate that the Bahaman population is a hybrid with C. gestroi, but our analyses of the ITS array from Bahaman alates do not seem to support this hypothesis because one allele, rather than two, is evident in the sequence chromatograms. Investigations are underway using microsatellites, which may shed additional insights into potential hybridization.