The alien species Stenochrus portoricensis (Schizomida: Hubbardiidae): decreasing the Wallacean shortfall in the New World

ABSTRACT The widely distributed species, Stenochrus portoricensis Chamberlin, 1922, is recorded for the first time from Costa Rica and Venezuela, and new occurrences from Brazil and Colombia are presented. Morphology of spermathecae from 14 localities is compared and illustrated. The need for studies to evaluate the potential status as an invasive species of S. portoricensis is commented on and a distribution map of the species in southern Central America and South America is given.

However, S. portoricensis is not restricted to Central America, North America, and the Antilles since it is also widely distributed across many countries in two additional continents: Europe and South America.In Europe, this species appears to be common among greenhouses, as reported from many countries (e.g., Czech Republic, England, Germany, Poland, Slovakia, Switzerland, and Spain) (Reddell & Cokendolpher, 1995;Blick, 2006;Christophoryová et al., 2013;Zawierucha et al., 2013;Barranco et al., 2014;Armas & Rehfeldt, 2015;Lauterbach et al., 2020;Krajčovičová et al., 2021).On the other hand, in South America, this species has been recorded from three countries: Ecuador (Galapagos Islands, Guayaquil in mainland Ecuador), Brazil, and Colombia (World Schizomida Catalog, 2022).In Brazil, the populations of S. portoricensis seem to be established in anthropized areas in the states of São Paulo, Rio de Janeiro, Bahia, Pernambuco, and Tocantins (Tourinho & Kury, 1999;Souza & Lira, 2015), and in hypogean habitats in the state of Goiás (Gallão et al., 2015).Likewise, in Colombia this species has been recorded in anthropized areas of cities, such as Armenia (Department of Quindío) and Cali (Department of Valle del Cauca) (Reddell & Cokendolpher, 1995;Armas & Delgado-Santa, 2012).
In the present contribution, the first records of Stenochrus portoricensis from Costa Rica (Guanacaste province) and Venezuela (Mérida state) are presented.Besides, we provide seven new records from Brazil (in the states of Bahia, Minas Gerais, Pará, Rio de Janeiro, and Pernambuco) and four new records from Colombia (departments of Valle del Cauca and Santander).
The morphology of the female spermathecae across 14 localities is presented and compared.Considering the dispersal capabilities and wide distribution exhibited by Stenochrus portoricensis, its status as an alien species is discussed.

MATERIALS AND METHODS
For the species identification, external morphology was examined under a Leica MZ75 or Zeiss Discovery V12 stereoscope.Spermathecae of specimens from Colombia and Venezuela were dissected and cleared with Lactic Acid (60%) at room temperature for about 3 h; then, washed with ethanol at 70% and mounted onto a temporal slide.Spermathecae slides were observed under a Zeiss Axio Scope A1 microscope.For the Colombian specimens, permanent slides were prepared using Hoyer's medium.Spermathecae of specimens from Brazil were dissected and cleared with a pancreatin solution, prepared as described by Álvarez-Padilla & Hormiga ( 2007), for about 12 h.Temporary slides containing the spermathecae of these specimens were mounted using 70% alcohol gel-only.After examining, the spermathecae were removed from the slides and stored in microtubes, along with the remaining body parts.
General morphology photographs (Figs 1-10) were taken with a Nikon DS-series camera attached to a Nikon SMZ1500 stereoscope with trinocular tube, integrated to the NIS-Elements software of Nikon.Spermathecae photographs were taken using a Zeiss AxioCam MR R3 adapted on a trinocular tube (photographs shown in Figs 13-17), a Canon Powershot SX510 manually adapted on a GS-10x stereoscope (photographs shown in Fig. 12 Works merely citing the species as the type-species of the genus are not considered in logonymy.Distribution.NORTH AMERICA: Bermuda, Mexico, and the USA (Florida).THE ANTILLES: Cuba, Dominica, the Dominican Republic, Jamaica, Puerto Rico, Saint Barthélemy, and Virgin Islands.CENTRAL AMERICA: Belize, Costa Rica (new country record), Guatemala, Honduras, Nicaragua, and Panama.SOUTH AMERICA: Brazil, Colombia, Ecuador (Galapagos Islands and mainland: Guayaquil), and Venezuela (new country record).EUROPE: Czech Republic, Germany, Great Britain, Poland, Slovakia, Switzerland, and Spain (Canary Islands and mainland: Sevilla).Remarks.The external morphology and genitalia did not differ from other populations of S. portoricensis from other countries (Figs 1, 2).Spermathecae from 14 localities were dissected, prepared and studied , but no relevant differences were found.The internal lobes in the Colombian populations from Dagua (Fig. 15) and El Vínculo (Fig. 14) and the Costa Rican specimen from Santa Cecília (Fig. 11) are straighter and shorter than the remaining populations (Figs 12,13,(16)(17)(18)(19)(20)(21)(22)(23)(24).In the female studied from El Vínculo, the outer lobes have a slightly more anterior position compared to the chitinized arch and the internal lobes, and the shape of the arch is a bit longer and more opened in the anterior branch.However, as only one female was studied per location, it is impossible to know if these variations are constant in the populations, or even if it could be due to the effects of preparing the spermathecae for study.The populations studied presented a large variation in the shape of the chitinized arch.The Brazilian specimens from Marabá and São Vicente Ferrer have a shorter and wider arch (Figs 18-20), whereas the specimens from Mérida, Venezuela and some Colombian populations (Girón, El Vínculo, Cali) have a deeper arch 17).Another variable aspect is the shape of the posterior branch of the chitinized arch, which is generally rounded (e.g., Figs 11,16,[22][23][24].However, in the Colombian specimens from Girón and Cali it is acute (Figs. 13,17).

DISCUSSION
The presence of Stenochrus portoricensis in Costa Rica and Venezuela is not surprising due to the previous records in neighboring countries with similar ecological conditions (Figs 32-34).From Costa Rica, 15 species distributed in four genera have been recorded.The current main component of the short-tailed whip scorpions from this country is the genus Surazomus, which is the second-most diverse in America (behind Rowlandius Reddell & Cokendolpher, 1995), originally distributed in South America, but recently recorded from Mexico (Monjaraz-Ruedas et al., 2020).The other genera present in Costa Rica are common elements in northern South America and the Antilles (Armas & Víquez, 2011, 2014).This is the first record of Stenochrus for this country.
The new record from Venezuela is based on four females collected in an anthropized forest fragment in Lagunillas near Laguna de Urao (Mérida state) , which could correspond to the Thorn Shrub forest biome (Ataroff & Sarmiento, 2004).Although efforts have been made to collect within preserved Thorn Shrub forest fragments, no specimens of S. portoricensis or any other schizomid species were observed whatsoever.So, the distribution of S. portoricensis is apparently restricted to anthropized forest fragments.
The introduction of S. portoricensis in Lagunillas may be related to agricultural activities carried out in an experimental station near the anthropized forest fragment.Although this species has not been collected in other regions of the country, the heterogeneous sampling in Venezuela prevents ruling out its presence in areas adjacent to some cities, mainly in the coast and center of the country.However, further efforts are needed to detect this species in urban areas in Venezuela, given that most of the efforts to sample short-tailed whip scorpions have focused on pristine humid forests or cave environments (e.g., González-Sponga, 1997; Armas & Colmenares- García, 2006;Villarreal & Teruel, 2006;Armas et al., 2009;Villarreal et al., 2014).
Moreover, one of the new records from Colombia represents a female population inside an urban area in Girón (department of Santander), similar to that recorded from other cities, such as Cali (department of Valle del Cauca) (Fig. 4D-G) and Armenia (department of Quindío) (e.g., Reddell & Cokendolpher, 1995;Delgado-Santa & Armas, 2012).However, the most interesting new records probably correspond to those from the seasonally dry tropical forest (SDTF) relics from Buga, Cerrito, and Dagua (department of Valle del Cauca).These records represent well-established populations of an alien species in a native and endangered Colombian ecosystem (García et al., 2014).
Figs 32-34.Geographical distribution of Stenochrus portoricensis Chamberlin, 1922 in South America and part of Central America (mainland and some islands): 32, South America and the southernmost portion of Central America; 33, Colombia; 34, Brazil.Iheringia, Série Zoologia, 113: e2023005 The SDTF presents a wide and fragmented distribution ranging from Mexico to Argentina (including the Antilles) (Pennington et al., 2009).It comprises one of the most threatened tropical biomes in the world (Miles et al., 2006) with less than 10% of its original extent remaining in a few countries (Pennington et al., 2009).When compared with other humid counterparts, such as tropical rain forests, the remaining area and the conservation efforts to protect the SDTF seem to be smaller (Sánchez-Azofeifa et al., 2005;Miles et al., 2006).In Colombia, the SDTF do not represent an exception and have also been considered among the most threatened ecosystems due to human activities that have diminished to 46% of its original extension of 7,172 km 2 (García et al., 2014).
The presence of S. portoricensis may constitute a threat to native schizomids inhabiting the SDTF or moist biomes.For example, in the department of Valle del Cauca, eight protected SDTF fragments exist; all surrounded by massive sugar cane crops: Colindres (Jamundí), El Vínculo Natural Regional Park (Buga), Las Chatas (Buga), El Medio (Zarzal), Las Pilas (La Victoria), Juan María Céspedes Botanical Garden, El Hatico Farm (Cerrito), and El Tiber (San Pedro) (Alvarado-Solano & Ospina, 2015).According to personal field observations by the last author (JAMG), El Medio and the Juan María Céspedes Botanical Garden have native populations of two undescribed species of Piaroa Villarreal, Giupponi & Tourinho, 2008 each, and have no populations of S. portoricensis, yet.Other fragments, such as El Vínculo Natural Regional Park (Buga) and El Hatico Farm (Cerrito), have well-established populations of S. portoricensis, but not native schizomid populations.
In the Amazon forest, several species of short-tailed whip scorpions are known (see, Ruiz & Valente, 2017 for a list) and the low number of species described might be due to sampling bias, widely reported for Brazil (Oliveira et al., 2016).In the Atlantic Forest, however, only one endemic or native species is known, Rowlandius linsduarte Santos, Dias, Brescovit & Santos, 2008.This species was described from Mata do Buraquinho, a forest reserve in the state of Sergipe (Santos et al., 2008), located less than 100 km from at least three records of S. portoricensis, in the state of Pernambuco (see Souza & Lira, 2015 and records in the present study).
As well as other introduced populations of S. portoricensis, the new records presented here are composed only of female populations.It may be due to the presumably parthenogenetic abilities of this species (Ruiz & Valente, 2017;Teruel & Questel, 2019;Monjaraz-Ruedas et al., 2022).This particular reproduction strategy of S. portoricensis can facilitate a rapid and massive expansion abroad, in nonnative biomes and anthropogenic areas.This hypothesis is also suggested for other taxa.For example, the goblin spiders Triaeris stenaspis Simon, 1891 and Heteroonops spinimanus (Simon, 1891) are considered parthenogenetic species with pantropical distribution, thus, raising concerns of the impact of these species on natural ecosystems (Brescovit et al., 2019).
There is no study on competition nor interactions between S. portoricensis and local schizomid species, hampering further assessments of their impacts.An important question remains open as to whether this species could become a harmful invasive exotic species that competes for resources or even takes advantage of local species, affecting their populations, but until there are studies in this regard, any assumption would be merely speculative.
Stenochrus portoricensis is a widely distributed species in the New World, with populations introduced in the Old World.Although its presence in Costa Rica and Venezuela is not surprising, the occurrence of this species in both countries is confirmed for the first time.Additionally, new records are presented for Colombia and Brazil.New records from the Brazilian Amazon region help to fill some distributional gaps for the species.This wide distribution suggests a possible status as an invasive species, thus, future studies should evaluate the ecological role played by S. portoricensis in other biomes where it has been introduced, emphasizing its influence on native populations and the risk that this introduction would represent to the local fauna.Furthermore, spermathecal morphology was evaluated in some individuals over a wide geographic range and no substantial differences were detected.Small variations were observed in the shape of the chitinized arch and the length of the lobes, however, the low number of samples studied per locality, as well as the differences in the preparation methods of the spermathecae, do not allow assessing whether they are population variations or an artifact of preparation.The species is reported for the first time in a bromeliad on a tree, a fact that -together with previous reports in heavily antropized places, forest litter or caves -allows evidence of ecological plasticity in the species.