A preliminary survey and range extension of millipedes species introduced in Brazil (Myriapoda, Diplopoda)

The present study provides historical and new records of the introduced millipedes species in Brazil, Oxidus gracilis (C.L. Koch, 1847), Orthomorpha coarctata (Saussure, 1860) (Paradoxosomatidae), Prosopodesmus jacobsoni Silvestri, 1910 (Haplodesmidae), Trachyjulus calvus (Pocock, 1893a), Glyphiulus granulatus (Gervais, 1847) (Cambalopsidae), Trigoniulus corallinus (Gervais, 1842), Leptogoniulus sorornus (Butler, 1876), Epitrigoniulus cruentatus (Brölemann, 1903) (Pachybolidae), Paraspirobolus lucifugus (Gervais, 1837) (Spirobolellidae), Cylindroiulus britannicus (Verhoeff, 1891), Cylindroiulus truncorum (Silvestri, 1896) (Julidae), and Rhinotus purpureus (Pocock, 1894) (Siphonotidae). Among the 27 federative units in Brazil, 21 states present at least one record of a non‐native species. Orthomorpha coarctata was the most widely distributed species, occurring in 15 states. Glyphiulus granulatus (state of Rio Grande do Sul), C. truncorum (São Paulo), and R. purpureus (Amazonas) were recorded from only one Brazilian state. The Southeast region concentrates most of the compiled records (42,6%) and richness by grid (5‐7 species), mainly in urban areas of the states of Rio de Janeiro and São Paulo.

Introduced species are widely accepted as one of the main direct causes of biodiversity loss and habitat alteration (Didham et al., 2005). In addition, non-native species have been reported as widely introduced around the world by human activities such as gardening, cultivation of plants, and soil transport. Numerous studies have reported the presence of millipedes in man-made habitats (Vicente & Enghoff, 1999;Golovatch & Kime, 2009;Shelley & Golovatch, 2011), including well-established populations in urban and rural areas (Hopkin & Read, 1992;Korsós et al., 2002;Bogyó et al., 2015). Some millipedes have been reported as pests causing significant economic damage (Butcher, 1936;Kuria & Eijnatten, 1981;Brunke et al., 2012). In Brazil, some introduced millipedes are considered agricultural pests in polyor monocultures based on observations of immatures and adults feeding on seedlings, tubers, and fruits (Schubart, 1942b;Boock & Lordello, 1952;Lordello, 1954). Importantly, the identification of a given species as introduced depends on the ISSN On-Line: 1807-0205 ISSN Printed: 0031-1049 ISNI: 0000-0004-0384-1825 availability of taxonomic data across large geographical regions. However, except for descriptive papers and taxonomic revisions made mainly by the authors Schubart, Brölemann, and Hoffman in the last century, there is no an updated list of millipede species for Brazil.
Based on a substantial material of millipedes from Brazilian collections, new records of non-native species were detected. In this perspective, to promote further studies regarding the millipedes in the country, the current study presents a preliminary survey of introduced millipedes species and their distribution. Maps for each species and comments on their identifications are provided here.

MATERIAL AND METHODS
The occurrence data for the introduced species was extracted from the literature and material deposited in the following institutions (curators in parentheses): Morphological observations and drawings were made using a Leica MZ 12 stereomicroscope. Photographs were taken with a Leica DFC 500 digital camera mounted on a Leica MZ 16A stereomicroscope and extended focal range images were composed with Leica Application Suite version 2.5.0, at IBSP. The specimens are preserved in 70% or 80% ethanol. The determination of the species was based on the descriptive notes and revisions performed by Schubart (1942cSchubart ( , 1946a, Mauriès (1980), Blower (1985, Korsós & Enghoff (1990), Shelley & Lehtinen (1999), Likhitrakarn et al. (2011), Golovatch et al. (2007, 2012, Wesener (2014) and Nguyen et al. (2017). All records obtained are mapped in the Figs. 1-2 and Table 1.
The geographical coordinates and collection data were obtained from the original literature (when provided) or the labels for each specimen consulted. We used the centroids of the municipalities when the exact locality was not provided. The data of the species are noted for each taxon according to the following pattern: Material examined: State: County, locality [geographical coordinates], data, collector (voucher); Historical records: State: County, locality [geographical coordinates], data, collector (reference consulted). The records gathered from the literature were compiled with all information provided by their respective authors, although some of these records only the localities were informed.

Order Polydesmida Family Paradoxosomatidae
Oxidus Note: Based on examined material, immatures and females of O. gracilis cannot be identified and morphologically distinguished from those of Orthomorpha coarctata.

Identification:
The species can be easily separated from autochthones Neotropical paradoxosomatids mainly by gonopod features (Fig. 5B). Males of O. coarctata are recognized by a single terminal lobule on gonopod tip; spikes and denticles either missing or nearly missing (Likhitrakarn et al., 2011(Likhitrakarn et al., , 2019.
Identification: T. calvus is easily separated from Brazilian species of Spirostreptida by having tergites longitudinally crested (Golovatch et al., 2012: fig. 8) and the presence of posterior gonopod. According to the diagnosis made by Golovatch et al. (2012), males are recognized by lateral coxal process of the anterior gonopod being very slender (Fig. 6C); slender and conical medial coxal process; posterior gonopod with axe-shaped flagellum extended and with microgranulate distal lobules (Fig. 6D).
Identification: Males of G. granulatus are recognized by a median outgrowth of the coxosternum in the anterior gonopods (Golovatch et al., 2007: fig. 5a, b; Fig. 6B) and the typical pattern of carinotaxy. As in T. calvus, the species is easily identified when compared with Brazilian species of Spirostreptida by having tergites longitudinally crested (Fig. 4C-D) and the presence of posterior gonopod (see Golovatch et al., 2007: 12).
Distribution: G. granulatus has been recorded in SE Asia and in islands in the Pacific and Indian oceans (Shelley, 1998a;Jeekel, 2004;Enghoff et al., 2015). In Brazil, the species occurs only in urban areas in Santa Maria, state of Rio Grande do Sul. Descriptive notes: See Shelley & Lehtinen (1999: 1389.

Material examined: Rio Grande do Sul
Note: An overview of its taxonomic status was made by Shelley & Lehtinen (1999).

Identification:
The species is easily recognized by the strongly reddish color in life (Fig. 9e). According to the diagnosis made by Shelley & Lehtinen (1999, figs. 11-13), males of T. corallinus are recognized by the coxae of the anterior gonopods narrowly separated by subtriangular sternum indented in midline; telopodites subtriangular, extending directly mediad (Fig. 5C), telopodites of the posterior gonopods rounded and with broad medial lobe at midlength; two inner projections arising basally from lobe and directed distad; and outer projection with notch on inner margin, expanded distad (Fig. 5D).
Identification: Members of Julida are easily recognized by stipites of gnathochilarium in contact in the midline in their basal part (symphyognathous condition). The species is recognized by three pairs of setae on the anal valves (Blower, 1985: fig. 49a); opisthomerite with finger-shaped projection (Blower, 1985: fig. 49b); promerite simple; mesomerite shorter than promerite (Fig. 7E).

Distribution:
The order Julida is distributed in the Holarctic region, marginally also in SE Asia and Central America (Enghoff et al., 2015). Cylindroiulus britannicus is widespread in Europe and predominantly distributed in the Northwest region (Blower, 1985). The species has been recorded in southern India, New Zealand, South Africa (Hoffman, 1999), Chile, and Argentina (Golovatch, 2014;Shelley et al., 2014). In Brazil, the species has been recorded only in urban areas in the states of São Paulo and Rio de Janeiro. All records of the species were obtained from the literature.  (Schubart, 1947).

Distribution:
The range extension of R. purpureus is not known and its native area is still uncertain (Hoffman, 1999). The species has been recorded in the Neotropical region (Shelley, 1998c), West Africa, Mauritius, East Indies (Hoffman, 1999), Madagascar (Wesener, 2014), and Asia (Hoffman, 1977;. In Brazil, the species has been recorded in urban areas from Manaus and from uncertain localities in the state of Amazonas (see Hoffman et al., 1996Hoffman et al., , 2002.  (Hoffman et al., 2002).

DISCUSSION
According to our results, the species richness varies substantially among the federative units in Brazil, with the Southeast region concentrating 42, 6% of the compiled records and 5-7 species recorded by grid ( Fig. 3A-C). Some hypotheses have been made to determine wheth-er the geographic expansion of some species in Brazil is a consequence of human-assisted introduction (Schubart, 1942b(Schubart, , 1946a. For instance, Schubart (1946b) suggested that the trade route of Portuguese colonies between South America and Asia indirectly influenced the spreading of T. calvus throughout the Neotropical region. Based on our results, T. calvus has been reported only in cities with maritime commercial facilities, including the new records from Salvador, Bahia.

CONCLUSIONS
Although there are still gaps in knowledge about the millipede fauna in the Neotropical region, this study presents one of the first efforts for a survey of introduced species in Brazil. The findings presented here report 12 introduced species in 21 Brazilian states, with a significant portion of these records related to rural and urban areas. However, our results are far from complete since the number of known introduced species in Brazil is still incipient. In this perspective, additional studies should expand our list of millipede with the inclusion of possible other species.