Cicadellinae of Ecuador and Cicadellidae of Galápagos

ABSTRACT An annotated list of the Cicadellinae (Hemiptera: Auchenorrhyncha: Cicadellidae) of Ecuador is presented. The collection in the Museum of Zoology Invertebrates Section of the Pontifical Catholic University of Ecuador (QCAZ) is comprised of 3763 specimens of Cicadellidae of which 2806 were in the subfamily Cicadellinae. These specimens were identified as belonging to 87 species. The collection contains an additional 28 species that appear to represent undescribed species. The specimens were distributed among all provinces of Ecuador except the new, small province of Santa Elena on the coast. The specimens were from every broad geographic region of Ecuador: Coast, Western Cloud Forest, Highlands, Eastern Cloud Forest and Amazonia. Many species were collected in multiple geographic regions. There are 18 new country records in this collection. The literature was searched for additional species of Cicadellinae and an additional 166 species were identified as part of the Ecuadorian fauna for a total of 253 species. Twenty-four species have host records that indicate they have the potential to be pests of cultivated and orchard crops. Twenty-four species of Cicadellidae in 16 genera are listed for the Galápagos Islands and many are considered endemic.


Introduction
The Cicadellidae are the largest family in the Hemiptera with between 22,000 [1] and 19,500 [2] described species. Bartlett et al. [3] list 21,351 species of Cicadellidae. While the higher classification of this family is under debate, a recent series of papers has divided the family into 25 subfamilies [4][5][6]. They are referred to as leafhoppers and the subfamily Cicadellinae as sharpshooters. This subfamily contains about 2400 species [2]. This group is particularly diverse in the Neotropics and probably less than half of the species have been described. Dietrich and Ratikov [7] estimate that as many as 80% of the Neotropical Deltocephalinae remain undescribed. The host plants for most species are unknown as many species have only been collected from light traps, malaise traps and to a lesser extent sweep net samples. A promising method for collecting new species has been canopy fogging collections. A number of species are known only from these collections. This would indicate that there is a substantial Cicadellidae fauna high in the canopy of rain and cloud forests that are not accessible by traditional collecting methods.
Throughout the Neotropics and in Ecuador collecting efforts have centered on established scientific stations and areas accessible by road. There remain large areas that have not been explored entomologically. Unfortunately, as these areas are opened up through road building for petroleum exploitation, mining and timber extraction, colonists and agriculture have followed rapidly. In many cases these habitats are irrevocably altered before biological assessments and inventories can be made. Undoubtedly, there will be many new species described as remote areas are explored.
The objective of this paper is to catalog the known species of Cicadellinae of Ecuador and in the collection of the Museum of Zoology -Invertebrates at the Pontifical Catholic University of Ecuador (QCAZ). Additionally, we provide distribution data for biogeography studies and highlight areas of Ecuador that are underrepresented in collections. We also include in this list the Cicadellidae from the Galápagos Islands of Ecuador with notes on distribution and potential origins.

Materials and methods
The majority of the specimens are in the collection of the Pontifical Catholic University of Ecuador, Museum of Zoology-Invertebrate Section. The majority of species identifications were made by Pedro Lozada during an extended visit to the Museum. Records from the literature are annotated with the appropriate citations.
Provincial designations have been updated to current usages. Previously Santo Domingo was part of Pichincha Province; Santa Elena was part of Guayas Province but these are now autonomous provinces. Historically the northern Amazonian region was Napo Province but has since been split into Sucumbíos, Napo and Orellana Provinces. Collection records have been corrected to reflect the current provinces for ease of georeferencing.
Distributions have been noted as Province with specific localities in parentheses. These specific localities have been assigned to general biogeographic regions, Galápagos, Coast (0 to 500 m), Western Cloud Forest (500 to 1750 m), Highlands (above 1750 m), Eastern Cloud Forest (1750 to 500 m) and Amazonia (below 500 m) [8] (Figure 1). We have not attempted to further specify habitats within these general regions, (e.g. Chocó, páramo, etc.). Most frequently the label data does not permit more accurate assignments, especially in historical specimens without GPS data. We have attempted to resolve label data lacking provincial designation wherever possible.

Museum abbreviations
The majority of specimens are located in the Museum of Zoology -Invertebrate Section of the Pontifical Catholic University of Ecuador in Quito, Ecuador (QCAZ). Other museums with significant holdings are as follows: These museum designations indicate holdings of specimens as noted in Dmitriev [9] or Wilson,Turner & McKamey [2] when a specimen is not in the QCAZ collection. Additional references are supplied as necessary.
Genera and species are listed alphabetically without tribal designation. The specimens in the QCAZ collection are listed with provincial and locality data. Those from the literature have the appropriate citation listing the distribution as including Ecuador. Wherever possible more precise collection localities have been included. Other countries are not included. Taxonomic authorities and spellings were verified using Dmitriev [9] and Wilson et al. [2] using the McKamey catalog [10] as the authority for terminology. Figure 1. Map of Ecuador with provincial boundaries and principal cities. The Andean highlands run down the center of the country. On each side of the cordillera is a band of cloud forest, one in the west and one in the east. The cloud forest bands typically range from 500 m to 1750 m in elevation. The central highlands are all above 1750 m with a central plateau or inter-Andean valley. Volcanic peaks in semi-isolated islands of páramo occur on both the eastern and western margins of the highlands. To the east, Ecuador contains a large area of Amazonian rainforest below 500 m in elevation. Some of this remains pristine but it is increasing dissected by small towns, agriculture and oil exploitation. The Galápagos Islands are an isolated archipelago about 1000 km to the west of the mainland.

Results
A total of 2806 specimens in the QCAZ collection were identified as belonging to 87 species. An additional 28 could only be identified to genus and probably represent new species. There remain 2957 specimens to be identified. These represent Cicadellidae not belonging to the Cicadellinae, in part. The QCAZ collection contains specimens representing 18 new country records. These are listed below. The collection is biased toward the mid-northern tier of provinces, Esmeraldas and Manabí on the coast, Pichincha (Western Cloud Forest), Napo, Sucumbíos and Orellana (Eastern Cloud Forest and Amazonia). This reflects the intensity of collecting by PUCE faculty, staff and students. Additional concentrations of specimens are from Otonga in Cotopaxi Province, Baños in Tungurahua, Santo Domingo and Pastaza. The collection has specimens from every Ecuadorian province with exception of the small new province of Santa Elena on the coast which is arid so probably contains a much smaller leafhopper fauna than other provinces.
The distribution of species by general habitat classification ( Figure 2) was interesting as most species were collected in more than one ecological zone type. For example, species collected in Amazonia were also typically collected in Eastern Cloud Forest and frequently in the Western Cloud Forest. Nevertheless, Amazonia had the majority of species (68) followed by the Western Cloud Forest (49), the Eastern Cloud Forest (36), the Coast (26) and the Highlands (19). Seven species from the Galápagos are in the collection. These species are endemic and do not occur in the Ecuadorian mainland.
With records from the literature and on-line databases, the list of Ecuadorian Cicadellinae is 253 species in 101 genera. The geographic bias in collection localities is very similar to that for the museum specimens (QCAZ). There are 24 species listed as from Galápagos. Most of the 16 genera of these Galápagos species also do not occur on the Ecuadorian mainland. The exceptions are Agallia, Balclutha and Docalidia. There are four species of Balclutha in the Galápagos and one specimen from the highlands of Ecuador that could not be determined to species. There are four relatively new species of Docalidia on the mainland and one species in the Galápagos  There are additional records for Cicadellidae from Ecuador but many of these references lack literature citations or museum records where the specimens have been deposited. If the species could not be confirmed to have a range that includes Ecuador with other sources, the species was not included in the following list. Examples of these include Agrosomna placetis, Cardioscarta flavifrons, Dilobopterus laetus, Oncometopia clarior, Sibovia prodigiosa, and Soosiulus regalis. These species are listed in the website, Entomología en Ecuador [11], without citations, geographic localities or location of voucher specimens. Many of these appear to be incidental records with identifications based on poor quality photographs. Examples of this in other leafhopper subfamilies, include Graminella striatella and Latusgallia vidua [12], Tantulidia rufifrons, Protalebrella brasiliensis and Planicephalus flavicosta [13]. Caldwelliola  Caldwelliola caucana Young 1977; Los Ríos [2]. Caldwelliola reservata (Fowler 1900) [2]. Host Plant Associations: Coffee, potential vector of Xylella fastidiosa [19].
Ecological Notes: Collected by canopy fogging in primary forest in Amazonia.
Ecological Notes: Collected by canopy fogging in primary Amazonian rainforest.
Ecological Notes: Collected by canopy fogging in primary Amazonian rainforest.
Ecological Notes: Specimens of this species have been collected in oil palm plantations, citrus plantations and by canopy fogging in primary rainforests in Amazonia.
Plant Association: Oil palm (Elaeis guineensis) [17]. Ecological Notes: Specimens of this species have been collected using canopy fogging in primary forests in Amazonia.
Ecological Notes: Collected by canopy fogging in primary Amazonian rainforest.
Ecological Notes: This species has been implicated in the spread of Xylella fastidiosa in citrus.

Discussion
It was not uncommon, especially in species represented by a large series of specimens, for there to be outliers from the distribution of the majority of specimens. In distributions that include the eastern or western cloud forests, these outliers have been collected in the highlands and probably represent wind-assisted dispersion. It was common for most of the species in the QCAZ collection to have distributions that encompass two, three or even four of the general biotic habitat zones. Some species have apparently followed the expansion of agriculture and inhabit these areas regardless of original habitat type. Another explanation for these wide distributions is that these insects are wind dispersed and can passively colonize a wide geographic region.
Some genera are conspicuously missing from the Ecuadorian fauna, e.g. Fusigonalia, Isogonalia. Species in these genera are noted in the literature as being present in every country surrounding Ecuador; Colombia, Brazil, Perú, but not in Ecuador. Comparison with the Colombian fauna [1] is interesting. For the Cicadellini and Proconiini in the Cicadellinae, our listing contains 64 of 157 genera (41%) and 27 of 56 genera (48%) found in Colombia, respectively. Conversely, most of the genera on our list are reported from Colombia. Only six of the genera (6%) in our list are not listed by Freytag and Sharkey [1] as found in Colombia. These genera are Agallia, Cicadella, Lanceoscarta, Lautereria, Stictoscarta and Tretogonia. However, Wilson et al. [2], citing Young [24], list one species of Cicadella, two species of Lautereria (one species, L. dietzi, that occurs in Ecuador), two species of Stictoscarta (the same two that occur in Ecuador) and two species of Tretogonia from Colombia. This leaves only Agallia from Galápagos and Lanceoscarta as two genera not shared with Colombia. The two species of Lanceoscarta, L. bilobata and L. ecuadoriana, were only collected by canopy fogging in primary Amazonian rainforest and were only recently described in 2005 [35].
Of the genera found in Galápagos, few have been recorded from the Ecuadorian mainland with the exception of Docalidia (four new species described by Nielson in 2007), a single specimen of Balclutha in the collection that could not be identified to species, and Agallia. This suggests that the Galápagos Cicadellidae dispersed to the Galápagos from other countries either by wind dispersion or in plant material shipped to Galápagos. The other genera (Circulifer, Coelidiana, Empoasca, Jikradia, Macrosteles, Sanctanus, Scaphoideus, Scaphytopius and Xestocephalus) found in Galápagos are all represented in the mainland of Colombia but not in Ecuador.
The collecting locale bias noted for the Cicadellinae of Ecuador is not unique to this subfamily. This pattern of intense collecting at only a few sites favored by easy road access or infrastructure of established scientific stations is widespread throughout the Neotropics. Donoso et al. [52] noted a similar pattern for type specimens collected in Ecuador. In all probability, this list represents a fraction of the total Cicadellinae fauna of Ecuador. Much of the collecting activity for this group has been centered on established sites with relatively easy access. Much of the collecting in the Amazonian rainforest has been near the Estación Científica Yasuní, the Tiputini Biodiversity Station in Orellana and the Villano site in Pastaza. Vast areas of Amazonia in Ecuador remain unexplored entomologically. Although every province of Ecuador except Santa Elena is represented in this list, many areas remain under collected. We have a small section of the Chocó coastal forest in Esmeraldas province that represents a threatened habitat with unknown biodiversity. In general, the south of Ecuador including dry coastal areas, cloud forest, especially in the east, Podocarpus National Park and the Amazonian provinces of Zamora Chinchipe and Morona Santiago have not been adequately investigated or surveyed. Cloud forest habitats on both the eastern and western slopes of the central cordillera of the Andes have been sampled at only a few locations. It is likely that there is substantial undocumented biodiversity, not only in the Cicadellidae, in these areas.
Sixteen species were collected in canopy fogging samples taken in primary rainforest, Acrobelus rakitovi, Acrogonia lobulata, Ciccamera hamata, Dichrophleps boliviana, Diestotemma dubium, Diestostomma olivia, Icthyobelus regularis, Lanceoscarta bilobata, Lanceolata ecuadoriana, Lissocarta caututaria, Molomea fatalis, Molomea virescens, Omagua fitchii, Paromenia rossi, Raphirhinus phosphoreus and Teletusa limpida. Several of these are reported as feeding on oil palm and probably also feed on other palm species high in the canopy. Several others represent new country records for Ecuador. Six are new species only described from canopy fogging samples. These canopy samples were taken at only two sites in the Ecuadorian Amazon, Tiputini Biodiversity Station and the Okanegare site near the Estación Científica Yasuní. Canopy samples taken from other locations using fogging or other techniques are likely to yield additional new species. There is a large collection of unsorted canopy samples from Dr. Terry Erwin's canopy fogging program over a number of years. These samples are primarily stored at the Museum of the Escuela Politécnica Nacional (EPNC) in Quito and a smaller, more recent group (2019) at the Pontifical Catholic University of Ecuador Museum of Zoology -Invertebrate Section (QCAZ). The samples at EPNC are unsorted and uncurated (Dr. David Donoso, Personal Communication) but probably contain a number of new Cicadellinae taxa. The canopy represents an important habitat for entomological sampling of the Cicadellidae that should be explored further.