The Genus Thionia Stål, 1859 (Hemiptera: Auchenorrhyncha: Issidae) in Colombia: Highlighting the Value of Entomological Collections

Entomological collections represent a key source of information about the biological heritage of a country. However, the taxonomy and knowledge of many arthropods from megadiverse countries are underrepresented in these natural history collections as is the case with several planthoppers of the suborder Auchenorrhyncha. Issidae are fulgoromorphs distributed worldwide, except the poles and Greenland. Despite this ubiquity, Colombian planthoppers remain very poorly known and studied. Our objective was to provide the first consolidated records and distributional data for Colombian Issidae. We used reports of the representative genus Thionia deposited in biological collections in Colombia. In addition, we linked voucher specimen information and Olson’s life zones showing an inter-Andean valley and Eastern Andean Cordillera distribution within Colombia. Our survey of Colombian biological collections revealed 55 individuals of the genus Thionia Stål, 1859 (53 adults, 2 immatures [nymphs]), which were collected by different methods; however, many of those records may be opportunistic. This genus (and its species) needs further study, with systematic and ecological revision, as is the case with other terrestrial Colombian hemipterans. Our consolidated records represent an advance to the knowledge of Issidae (and Thionia specifically) for the Neotropics and Colombia in particular, and a baseline for further study of distributional and biogeographic patterns of the suborder Auchenorrhyncha.


Introduction
The natural history entomological collections represent a key and scientifically important sample of the world's biological heritage and constitute the basis for fundamental and applied research (Suarez and Tsutsui 2004;Holovachov et al. 2014; National Academies of Sciences and Medicine 2020). To date, there are more than a million described insect species and more than half a billion preserved specimens, exceeding any other taxon (Short et al. 2018;Stork 2018). Some groups, such as hemipterans, lack detailed information and commonly are collected in biological expeditions but are not adequately characterized, classified, and preserved (Paradell and Defea 2017). They can be important specimens such as new species, extinct, endangered, cited, and/or historical material that should be identified and kept where they are safest or can most easily be studied (Llano et al. 2016). However, some taxonomic and societal preference biases are unavoidable (Troudet et al. 2017).
Therefore, it is our interest to promote initiatives in support of Neotropical insect taxonomy and the current status of the genus Thionia, vouchered into certified insect collection resources of Colombia, as a pioneer information source for further insect biosystematic data, training, and research. This study begins to address the paucity of available distributional and ecological data for the country. Our main objective was to analyze available distributional data and host plant associations related to the genus Thionia Stål, 1859 in Colombia based on specimens examined from certified national biological collections, and relate these data to the ecoregions presented by Olson et al. (2001).

Methods
Morphological nomenclature and taxonomy of the family follow Bartlett et al. (2014), Gnezdilov (2018a), and Gnezdilov and Dmitriev (2018). Specimens of Issidae were examined from the following Colombian collections: Geographic information was recorded from the specimens' labels (see Appendix 1). Distributional records were analyzed by matching collection records to ecoregions after Olson et al. (2001) using the freeware DIVA-GIS 7.5. Specimens of Issidae were not identified past genus because there are no modern taxonomic tools for Issidae of Colombia and primary types of relevant species are primarily in Europe. Legacy tools such as Melichar (1906) and original descriptions may have yielded speculative identifications, but we deemed these untrustworthy given the potential for many undescribed species as reported by Barringer et al. (2019) for Ecuador.

Distributional and altitudinal records
Altitudinal distributional records for Colombia range from 2 to 2550 m a.s.l. (Fig. 3). Our review revealed records associated with areas of biological importance or protected areas such as national natural parks, private ecological reserves, and/or botanical gardens (15 records; see Appendix 1). It also was apparent that Thionia was associated with forest fragments immersed in agroecosystems (8 records), which provide a refuge for these insects.

Distribution of Thionia in the Colombian Ecoregions
Mapping specimen distributional data (see Appendix 1) on ecoregional areas proposed by Olson et al. (2001) (Fig. 4).

Discussion
Although reported collecting methods follow those expected (most hand collection), many records may be opportunistic. Colombian fulgoromorphs have been underrepresented in biological (terrestrial studies) or in studies on arthropods in general, as "occasional" finds and generally are scarce in collections (Osborn 1938), despite reports that Malaise and black-light traps can be useful tools for capturing Auchenorrhyncha from the canopy (Weber and Wilson 1981;Wilson 2005;Barringer and Bartlett 2018). Barringer et al. (2019) reported a large abundance and diversity of issids from forest canopy fogging samples in Ecuador, suggesting this to be an effective collecting method for issids.

Distributional and altitudinal records
Thionia is a genus of mostly Neotropical distribution (Wheeler and Wilson 1988;Gnezdilov 2018b), reported from México, Honduras, El Salvador, Guatemala, Costa Rica, Panamá, Colombia, Venezuela, Ecuador, Perú, Bolivia, Guyana, French Guiana, Nicaragua, and Brazil (Bourgoin 2022), although some Thionia species extend into temperate North America (Bartlett et al. 2014). For Colombia, the genus is recorded for the first time at the departments of Boyacá, Magdalena, Meta, Chocó, Santander, Tolima, Bolívar, Caldas, and Antioquia. Early publications of Colombian records appear to mostly refer to the Cundinamarca department (see Fig. 2).
This distribution may be associated with the relationship between Issidae and their host plants due to the spatial distribution of plants jointly with their complexity and leaf architecture may limit the presence, richness, and abundance of Issidae and other planthoppers (Denno 1994;Wilson et al. 1994). In addition, it has been observed that fragmentation associated with the creation of agroecosystems changes the herbivorous community and multitrophic interactions with significant effects on the presence and distribution of selected taxa (Kareiva 1987;Gardarin et al. 2018).

Distribution of Thionia in the Colombian Ecoregions
The presence of Issidae in Colombia appears to be significantly correlated to climate (e.g., precipitation and temperature) and biological metrics (e.g., vegetation structure) (Holdridge 1967;De Laubenfels 1975;Schmidthüsen 1976;Walter and Box 1976;Olson et al. 2001;Bailey 2014). Likewise, ecoregions may represent areas of marked endemism and promote conservation plans at the species or community level (Noss 1994;Olson et al. 2001;Dinerstein et al. 2017  Moist Forest are transformed ecosystems (Etter et al. 2020) due to anthropogenic activities as deforestation, ampliation of the agriculture, and livestock frontier (Armenteras et al. 2003;González et al. 2011 (Etter et al. 2020).
National biological collection faunistic records can be associated with regions currently under heavy human pressure using the IUCN Red List of Ecosystems and future risks (Bland et al. 2019;Etter et al. 2020). Despite the opportunity, the genus-level determination of Thionia species may mask the vulnerability of these issids to land use and land cover changes. Moreover, the ecological importance of Auchenorrhyncha and other Colombian terrestrial and riparian hemipterans is practically unknown (Llano et al. 2016), and this makes it difficult to promote conservation programs and alternative tools to manage pests or exotic insects in agriculture areas.
An issue to consider in further analyses is that these records are associated with a higher concentration of researchers, experts, research centers, and universities mainly in the Andean region of Colombia (other issues highlighted by Arbeláez-Cortés 2013 and Arbeláez-Cortés et al. 2017), which may geographically bias these data and it should be interpreted accordingly. Likewise, despite insects being highly studied in Colombia (Arbeláez-Cortés 2013), their classification at the lowest practical taxonomical level is heterogeneous, with some taxa identified only to family or supra-family level, and others undetermined even to these levels. This is related to the lack of taxonomic experts, as is the case of Hemiptera. In addition, the highlighted biological collections represent those with higher housing history and much better systematics curatorial background, specifically related to the genus Thionia (Fig. 2).  (Wheeler and Wilson 1987;Wilson et al. 1994;Palmer and Pullen 2001). Our review includes a plant association with Theobroma cacao L. (the cocoa tree, Malvaceae), a species of great commercial value in central-west Colombia (FEDE-CACAO 2019). Nonetheless, Issidae are seldom reported as pests and have not been demonstrated to be plant-pathogen vectors ). In addition, found a "new" habitat association with a Thionia was reported from the mangrove forests of north-east Colombia (Atlántico department, Barú Island) where four mangrove species are present: Rhizophora mangle L., Avicennia germinans (L.) L., Laguncularia racemosa (L.) C.F. Gaertn., and Conocarpus erectus L. (Valle et al. 2011).

Implications for conservation
As highlighted by Gnezdilov and O'Brien (2008) and recently by Gnezdilov and Bartlett (2018) and Gnezdilov (2019), contributions to the study of Central and South American issids have been made by few authors from the 1900s. A further purpose of our work is to contribute to the knowledge of Neotropical fulgoromorphs so that revision or description of the Colombian species can occur within an established ecological framework. In this sense, our review represents an advance in the knowledge of Issidae (and Thionia specifically) in Colombia and a baseline for further study of distributional and biogeographic patterns. However, only data from the biological collection were considered and we highly recommend sampling-based fieldwork (including in Colombian ecoregions where Issidae are not yet detected) for advancing ecosystem patterns and plant associations. In addition, taxonomic and systematics studies are necessary for establishing the current or potential distributions at the species level. Despite considerable progress in taxonomic studies, no phylogenetic treatment of the group had been published until recently (Wang et al. 2016;Gnezdilov et al. 2020. While we provide plant associations for Thionia, further research is needed to confirm their true host plant affinities. Although host preference varies among planthopper families, some being inhabitants of grass, herbaceous, and small riparian plants, others can be expected to occur in the forest canopy. However, it is often poorly documented (Barringer et al. 2019). Even though taxonomic and systematics requirements about insects are recognized worldwide, these represent more requested issues in megadiverse countries; similarly, as occurs with many arthropods, planthoppers should include several undescribed species in the tropics (Barringer et al. 2019). It has been apparent that the rich Neotropical issid fauna is still in its initial stage of discovery . Additionally, knowledge of their current and future entomological biodiversity due to natural and anthropogenic impacts is still largely unknown.

Appendix 1
Examined material from Colombian departments and information extracted from the representative national collections (check collection abbreviation afore):

Appendix 2
Representativeness of the genus Thionia in arthropod' voucher specimens from Colombian biological certified collections reviewed in the present study (source main: https:// ipt. biodi versi dad. co/ sib/? reque st_ locale= en (filtered by collection acronym))