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Revisiting Coptotermes (Isoptera: Rhinotermitidae): a global taxonomic road map for species validity and distribution of an economically important subterranean termite genus

2015; Wiley; Volume: 41; Issue: 2 Linguagem: Inglês

10.1111/syen.12157

1365-3113

Thomas Chouvenc, Hou‐Feng Li, James W. Austin, Christian Bordereau, Thomas Bourguignon, Stephen L. Cameron, Eliana M. Cancello, Reginaldo Constantino, Ana Maria Costa‐Leonardo, Paul Eggleton, Theodore A. Evans, Brian T. Forschler, J. Kenneth Grace, Claudia Husseneder, Jan Křeček, Chow‐Yang Lee, Tim Lee, Nathan Lo, Matthew T. Messenger, Aaron Mullins, Alain Robert, Yves Roisin, Rudolf H. Scheffrahn, David Sillam‐Dussès, Jan Šobotník, Allen L. Szalanski, Yoko Takematsu, Edward L. Vargo, Akinori Yamada, Tsuyoshi Yoshimura, NAN‐YAO SU,

Animal Behavior and Reproduction

Coptotermes Wasmann (Isoptera: Rhinotermitidae) is one of the most economically important subterranean termite genera and some species are successful invaders. However, despite its important pest status, the taxonomic validity of many named Coptotermes species remains unclear. In this study, we reviewed all named species within the genus and investigated evidence supporting the validity of each named species. Species were systematically scrutinized according to the region of their original description: Southeast Asia, India, China, Africa, the Neotropics, and Australia. We estimate that of the currently 69 named species described by accepted nomenclatural rules, only 21 taxa have solid evidence for validity, 44 names have uncertain status, and the remaining species names should be synonymized or were made unavailable. Species with high degrees of invasiveness may be known under additional junior synonyms due to independent parochial descriptions. Molecular data for a vast majority of species are scarce and significant effort is needed to complete the taxonomic and phylogenetic revision of the genus. Because of the wide distribution of Coptotermes, we advocate for an integrative taxonomic effort to establish the distribution of each putative species, provide specimens and corresponding molecular data, check original descriptions and type specimens (if available), and provide evidence for a more robust phylogenetic position of each species. This study embodies both consensus and contention of those studying Coptotermes and thus pinpoints the current uncertainty of many species. This project is intended to be a roadmap for identifying those Coptotermes species names that need to be more thoroughly investigated, as an incentive to complete a necessary revision process. Termites (Isoptera) are a group of eusocial insects traditionally ranked as an insect order, but representing a subgroup within Blattodea, with Cryptocercus being their sister taxon (Lo et al., 2000; Inward et al., 2007; Cameron et al., 2012; Djernaes et al., 2015). A recent taxonomic review of termites established that there are currently 2937 described species in the world, with 104 of them considered serious pests (Krishna et al., 2013a). Twenty-three species in the genus Coptotermes (Rhinotermitidae) are among the most significant termite pests worldwide for man-made structures. Coptotermes formosanus Shiraki and Coptotermes gestroi (Wasmann) are of particular economic importance (Rust & Su, 2012) due to their ecological success and invasive ability (Evans et al., 2013). Despite the wide distribution of Coptotermes in the world, and the large body of associated scientific literature for population management, the taxonomy of Coptotermes remains unsettled and many species names may be synonyms of other species. In termites, species descriptions have historically relied upon morphological characters of the soldiers and/or alates (Fig. 1), but the seasonal occurrence of alates often prevents simultaneous collection, and therefore the simultaneous description, of both castes (Jones et al., 2005; Yang & Li, 2012). As a result, many original species descriptions are based on the soldier caste alone (Li, 2000) from geographically limited material. For Coptotermes, soldier morphology is relatively conserved across the genus, presenting a major challenge to species identification. The overdependence on soldier head shape and the number of setae around the fontanelle has resulted in taxonomic confusion – as, for example, the controversy regarding distinguishing C. formosanus and C. gestroi in Taiwan based solely on soldier morphology, which was ultimately solved by the alate morphology and additional molecular data (Li et al., 2010). Intraspecific variation in morphological characters in soldiers also complicates species identification (Emerson, 1971; Husseneder & Grace, 2001). Soldiers in Coptotermes are produced from different developmental pathways which are colony-age dependent, contributing to intracolonial variability (Ferraz & Cancello, 2004; Chouvenc & Su, 2014). Furthermore, exacerbating the confusion is the unavailability of voucher specimens with all castes in sufficient number for comparison and description of the given variability. In addition, transport by ships has led to the spread of several invasive species throughout the world (Scheffrahn, 2013). This complicates termite species identification further, as many identification guides only cover regional faunas (Kirton & Brown, 2003; Scheffrahn et al., 2004; Austin et al., 2005; Jenkins et al., 2007; Yeap et al., 2007; Husseneder et al., 2012). As a result, there are many synonyms in Coptotermes (more than 40 junior synonyms), and thus resolving Coptotermes nomenclature is a work in progress (Krishna et al., 2013b). Krishna et al. (2013b) listed 110 species names within Coptotermes that conformed to the rules of the International Code of Zoological Nomenclature (ICZN) and, among them, 69 were regarded as valid in the taxonomic literature, and 42 were listed as subjective synonyms. The list also included four objective synonyms and ten nomina nuda (not treated herein). Out of the 69 species listed as valid by Krishna et al. (2013b), about half of the species are known only from limited material (e.g., one caste described, single colony of origin, or a single alate, no comparison with previously described specimen, etc.). Some descriptions are over a century old and may not meet modern rigour. Although molecular taxonomy offers tools to validate species or synonymization, such data have yet to be collected for most species. As a result, the validity of many species names as real biological taxa is uncertain. For example, the unusually high species diversity of described Coptotermes in China (22 species) represents an anomaly that requires close scrutiny (Eggleton, 1999; Wang & Grace, 1999; Li, 2000; Yeap et al., 2009; Li et al., 2011). Krishna et al. (2013a) provided an invaluable contemporary catalogue of the Isoptera worldwide, and building on that, we focus here on the Coptotermes species names for which there is little evidence to support their validity as a biological species in light of current knowledge of inter- and intraspecific variability and worldwide geographical distribution. The phylogenetic relationships within Coptotermes are currently fragmentary and focused on a limited number of species and just a few DNA sequences per species (Lo et al., 2006; Yeap et al., 2009; Scheffrahn et al., 2015). A recent analysis using the available molecular data (Lee et al., 2015) has provided some insight into Coptotermes phylogenetics and its radiation, especially in Australian species. In light of the work by Krishna et al. (2013b), and Lee et al. (2015), it is clear that a taxonomic revision of Coptotermes is urgently needed, especially as accurate species identification can have important implications for control practices, as highlighted by Kirton (2005). However, the task will require morphological and genetic analyses from a large geographical survey that are beyond the capability of a single, localized research group. In addition, the recent phylogeny proposed by Lee et al. (2015) revealed discrepancies depending on the genetic marker used, and the limited number of DNA sequences available for most species currently prevents a robust and definitive analysis. The goal of this study is to investigate the current status of all described Coptotermes species names as a step toward a comprehensive taxonomy of the genus. Although the investigation of species names is only the first part of this conundrum, it provides a framework that focuses the attention on uncertain species names. Ultimately, we propose a road map for the taxonomic revision of the genus based on modern phylogenetic methods. We gathered the information available on all named species, using Krishna et al. (2013b) as a starting resource for Coptotermes nomenclature, and consulted original descriptions of species when available. The 69 species names given by Krishna et al. (2013b) are assumed to be valid based on their original author's scholarship. Likewise, some names listed as subjective synonyms by Krishna et al. (2013b) might actually be valid, and, conversely, some currently valid species names may actually be junior synonyms. The list includes all available names currently recognized as valid and all subjective, potentially valid, junior synonyms. There are currently many grey areas in the Coptotermes taxonomy (and more broadly in overall termite taxonomy), and we express caution from making definite statements about the validity of any given species names, as in many cases it is still a work in progress. We have compiled a list of species names that were considered to have questionable or uncertain status, based on a review of the literature about Coptotermes and the distribution of the genus. Considerations were based on the comparison of original and later descriptions, along with recent genetic data, and personal observations from various authors of this study. All 69 species names were investigated and categorized as 'valid,' 'uncertain' or 'other' according to the following guidelines, and the category attribution was the result of a consensus among all authors using these guidelines (a full description of the analysis is available in Appendix S1). Ultimately, the decision to place a species in a given category was the result of a discussion among all authors in this study and represents a compromise on the overall agreement about the uncertain status of some species. While validity of a species and quality of its description may be unrelated, the species names placed in the 'valid' category all include description of the soldier caste and/or imago, and comparisons with sympatric or widespread species. Many of these names are also well established in the Coptotermes literature and most have a well-known distribution. The intraspecific morphological variability was expanded over time due to author interpretation and known range expansion. Most species in this category were also confirmed using molecular tools. Historically, there is a long list of names that were synonymized owing to the precedence of older names. Therefore, currently valid species names may be junior synonyms of less well known older names, but availability, quality and erosion of samples may preclude such synonymization. To our current knowledge, there is sufficient evidence to confirm their validity, although we do not exclude potential synonymization in light of future morphological and/or molecular studies. The status of subspecies was also discussed when necessary. For the majority of uncertain species, type specimens were not compared with any other material at the time of their description or subsequently. Some species in this category were only mentioned in various catalogues and no specimens were independently collected to confirm their validity. Moreover, there are currently no available molecular data to support their validity. Species in this category will require further study to confirm their validity, or to relegate them to junior synonym status. Alternatively, such poorly defined species may be senior synonyms of currently 'valid' species, but the current absence of data forced us to place these species names in the 'uncertain' list by default, at least until further investigation is performed. In this respect, while we may suspect a case of senior synonymy for a name that was not used for several decades, we presently consider them as 'uncertain' in the hope that future work will resolve their nomenclatural position. When a synonymy is suspected for a questionable name, we indicate if junior or senior synonymy would apply. Although there is currently little evidence to support the validity of some taxa, we express caution about interpreting our opinion as a 'nonvalid' statement, because there are simply not enough data to resolve the ambiguity. Species listed as nomina nuda by Krishna et al. (2013b) and species names due to misspellings (lapsus calami) are unavailable and therefore ten names were not included in the current study. Fossil species are included in this study. A consensus regarding the evidence for the validity of all potential Coptotermes species was formulated in Appendix S1. The analysis was structured by grouping species by their putative geographical origin. To summarize, out of 69 Coptotermes species, only 21 species currently have some evidence to support their validity (Table 1), 44 names need additional work to confirm their validity or their potential junior/senior synonymy (24 outside China, 20 from China), and all remaining species names were confirmed as junior synonyms or were unavailable. Type localities and putative distributions of all 69 potential species are shown in Fig. 2, with an emphasis on their validity status. Among the 21 species with a valid status, eight are native to Southeast Asia, one is from China, one from India, four from Africa, one from the Neotropics, and six are from Australia. All 44 species with uncertain status, fossils and all junior synonyms are discussed in Appendix S1. Of the 21 Coptotermes species we considered valid, 16 species currently have major pest status according to Krishna et al. (2013a). This observation supports the ecological success of the genus and its ability to establish in disturbed environments. It also confirms the economic impact the genus has around the world (Rust & Su, 2012). However, the general perception that the genus is a major invader may have been distorted due to the extensive research of some of these species in non-native areas. While it is widely accepted that Coptotermes is a 'great invader' when associated with human activity (Evans, 2011; Evans et al., 2013), our review actually points toward only two species that have this ability: C. formosanus and C. gestroi. The invasive status of C. formosanus and C. gestroi has long been a source of taxonomic confusion in many parts of the world, and, to some extent, still is. Historically, both species have at least eight junior synonyms. Both species were themselves confused as a single species in Taiwan for a long time (Li et al., 2010). As discussed in this study, there is a strong suspicion that several species described from India, from the islands around Madagascar and some islands from Southeast Asia could be synonyms of C. gestroi. Coptotermes heimi is invasive to the Arabian subcontinent to a small extent, whereas C. acinaciformis in New Zealand and the Pacific Islands, and C. sjostedti in Guadeloupe could be considered as 'chance invasions' with little to no local expansion. Therefore, besides C. formosanus and C. gestroi, Coptotermes as a genus has very few species with a history of successful introduction and establishment. It may be that the number of introductions by Coptotermes is correlated with the amount of historical sea travel between areas, where the propagule pressure is different (Lockwood et al., 2005; Su, 2013). Alternatively, the dispersal flight behaviour (diurnal vs nocturnal) of some species may influence the chance for alates to fly towards artificial lights. For example, C. testaceus is a diurnal flier and may not have had many opportunities to infest boats (Scheffrahn et al., 2015). In addition to its underground foraging ability, Coptotermes is also a genus where most species have evolved to eat heartwood in living trees, with extreme examples in some Australian 'tree-piping' termites. Such a trait could have allowed for the transport of infested logs and good survival of colonies for the establishment in non-native areas. Future studies should focus on the differences in biology of all described species to explain why these two species are exceptions and why they thrive so well when associated with human activity. Movement of species around the world and novel interactions among allopatric species may also have unexpected consequences. Chouvenc et al. (2015) recently observed in south Florida (where both specie are invasive) that C. formosanus and C. gestroi have a long overlapping swarming season in south Florida with field observation of interspecies mating behaviour. Colonies with high hybrid vigour were obtained under laboratory conditions, which raises questions about the barriers between species in endemic areas that are potentially absent in their invasive range. It also implies that gene flow among various populations might have occurred in the past among other Coptotermes species. However, genetic determination of taxa has historically used mitochondrial markers, comparing maternal lineage, which cannot be used for the investigation of potential gene flow among different populations of Coptotermes. The future clarification of the species complex within Coptotermes will provide valuable insight into the definition of species in Coptotermes, as seen in C. acinaciformis (Lee et al., 2015), and could solve the question of how Coptotermes evolved and radiated in the past, and predict how it will spread in the future. Our study reveals major problems in Coptotermes taxonomy. The validity of each described species name as a biological taxon varies tremendously in level of support, from full evidence to no data. Krishna et al. (2013b) listed 69 Coptotermes names that were regarded as valid in the taxonomic literature and took into account various subjective synonymies over the past century. While the nomenclatural work of Krishna et al. (2013b) provides the biogeographical details concerning all known Coptotermes species names, there is still research needed to clarify the biological reality of each Coptotermes species name. The current effort to clarify the taxonomy of the Coptotermes genus needs to be intensified, as the use of molecular tools now enables us to distinguish taxa with much greater certainty (Bourguignon et al., 2015). Such tools should also allow for the discovery of potentially new cryptic species (Lee et al., 2015). In addition, recent surveys revealed that some species have yet to be discovered (Bourguignon & Roisin, 2011), while more synonymy is expected to be found (Scheffrahn et al., 2015). We assume that a clarification of the taxonomic status of species within the Coptotermes genus will take place in the near future. Clearly, soldier morphology alone is insufficient to establish a species, as the wide intraspecific soldier morphological variability has long been the source of inaccurate species descriptions. Alate descriptions should be encouraged in the description process along with soldiers, and molecular data using a range of genetic markers. Any novel description, synonymizations or re-descriptions may also use quantitative morphometrics in the case of large samplings. As the number of diagnostic sequences available to termite researchers will inevitably increase in the foreseeable future, this is a good time to clarify the taxonomy of this important pest genus and to complete the story of the evolutionary radiation of the genus throughout the world. Owing to the high number of available species names from Southeast Asia, Emerson (1971) suggested that Coptotermes may have originated from this area and then radiated to the rest of the world. However, we argue in this review that the diversity in Southeast Asia may be lower than previously accepted. Genetic data from African termites (C. sjostedti, C. amanii, C. intermedius) suggest that they are basal within the Coptotermes phylogeny, followed by the Neotropical Coptotermes, and then went through rapid radiation throughout Asia and Australia (Lee et al., 2015). The phylogeography of Coptotermes is still in its infancy, as the taxonomic complexity of geographic populations within a species has only been partially described in Australian termites (Brown et al., 2004; Lee et al., 2015). However, such studies offer unique perspectives on other Coptotermes species (Vargo & Husseneder, 2009). We therefore expect extensive taxonomic and phylogeographic studies of Coptotermes on a global scale in the near future and we hope that the consensus reached in this article concerning the uncertain status of some species will provide an incentive to achieve this goal. This study is dedicated to Kumar Krishna (1928–2014) for his lifelong contributions to termite taxonomy. This study was partially supported by a grant (MOST 102-2313-B-005-037-MY2) from the Taiwan Ministry of Science and Technology. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. 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