Notorhinus floresi sp. nov. gen. nov.: The first records of Siphonophorida in Chile and Siphonorhinidae in South America (Colobognatha)

The millipede family Siphonorhinidae (order Siphonophorida) shows a scattered distribution in South Africa, Madagascar, India, Southeast Asia


Introduction
Among millipedes (Diplopoda) the Colobognatha, with the four orders Platydesmida, Polyzoniida, Siphonocryptida and Siphonophorida, are extraordinary in many aspects. Colobognathan taxa show strongly modified heads and mouthparts for suctorial feeding (Moritz et al. 2021(Moritz et al. , 2022, some display maternal or paternal brood-care (Wong et al. 2020; Moritz et al. 2023), and they exhibit a fragmented and relictual distribution in widely separated areas (Cook and Loomis 1928;Shelley and Golovatch 2011). The interesting biogeography of the group is probably the relict of a once wider distribution (Marek et al. 2016) and might be related to their adaptation towards certain vegetation and climate, as the Colobognatha show greater ecological limitations than other Diplopoda (Cook and Loomis 1928) and are often restricted to very humid habitats . Prime examples of this scattered distribution can be found in the order Siphonophorida and especially in the family Siphonorhinidae (Fig. 1A). The Siphonophorida are characterized by separate tergites, pleurites and sternites, modification of male leg-pair 9 and 10 to leg-like gonopods, absence of ommatidia, a head, which is conical/pyriform or drawn out into a beak, and strongly modified mouthparts (Read and Enghoff 2009). The order comprises a total of 118 described species to date (Enghoff et al. 2015;Marek et al. 2016;Wesener 2023), which are classified in two families: Siphonophoridae Newport, 1844 and Siphonorhinidae Cook, 1895. The group has previously been referred to as a "taxonomist's nightmare" (Read and Enghoff 2009: 543) and got the "taxonomists' award for the least popular group among Diplopoda" (Jeekel 2001: 44). This is mainly due to the weakly modified gonopods, compared to those of other helminthomorph taxa, in which the gonopods are highly species specific (Jeekel 2001). In the Siphonophoridae the head extends into a long beak and the antennae are straight, while in the Siphonorhinidae the pyriform head lacks such a beak and carries elbowed antennae (Enghoff et al. 2015). Both groups are already known from the Cretaceous of Myanmar ca. 99 million years ago (Wesener and Moritz 2018). The Siphonorhinidae include five genera, the monotypic Kleruchus Attems, 1938and Nematozonium Verhoeff 1939, Illacme Cook and Loomis, 1928 with two species, Siphonorhinus Pocock, 1894 with eight species (Jeekel 2001;Marek et al. 2016), and Madagascarhinus Wesener, 2023 with two species (Wesener 2023). Detailed catalogues of the group have been provided by Jeekel (2001) and Marek et al. (2016). The family Siphonorhinidae is distributed in South Africa, Madagascar, India, Southeast Asia, and North America (Fig. 1A). Not a single species of the family has been recorded from South America (Jeekel 2001;Enghoff et al. 2015;Marek et al. 2016), where the family Siphonophoridae appears to be quite diverse and widespread (Shelley 1996;Read and Enghoff 2009, 2019. However, from Chile not a single representative of the order Siphonophorida, neither the families Siphonophoridae nor Siphonorhinidae, has been reported so far (Parra-Gómez 2022). With a north-south extension of more than 4,000 km, the narrow country of Chile spans a wide array of climatic conditions and biomes (Veblen et al. 2007) and contains one of the world's major biodiversity hotspots: The Chilean Winter Rainfall-Valdivian Forest hotspot (ChV) in south-central Chile, that mainly includes the Chilean matorral and Valdivian temperate forests (Arroyo et al. 2004;Mittermeier et al. 2011;Fuentes-Castillo et al. 2020). Chile, and especially this hotspot, harbor a rich biodiversity with many endemic plants and animals (Arroyo et al. 2004), including several endemic millipede species distributed in five orders (Parra-Gómez 2022). However, these areas are already threatened by habitat loss (Arroyo et al. 2004). 65 of the 75 known Diplopoda species from Chile are considered to be endemic and most of these millipedes can be found in the south-central zone (Parra-Gómez 2022), including a relatively high diversity of the colobognathan order Polyzoniida (Mauriès and Silva 1971;Golovatch 2014;Parra-Gómez 2022). This area is characterized by evergreen broadleaved trees, evergreen coniferous vegetation and a humid temperate to Mediterranean climate (Veblen et al. 2007).
Here we describe the genus Notorhinus gen. nov. and the species Notorhinus floresi sp. nov. which is the first record of the order Siphonophorida in Chile and of the family Siphonorhinidae in South America. Furthermore, we record another representative of the genus Notorhinus gen. nov. from Chile.

Specimen collecting
Specimens were collected by hand during trips throughout 2019 and 2020 to El Natri and near Caramavida in the Biobio region, Chile. Specimens were preserved in 70% ethanol and are stored at the MNHNC and ZFMK.

Distribution map
Worldwide distribution of the Siphonorhinidae (Fig. 1A) and the records of Siphonorhinidae from Chile (Fig. 1B, C) were mapped in QGIS 3.28.1 based on literature records (Pocock 1894;Silvestri 1895;Attems 1930Attems , 1936Attems , 1938Turk 1947;Shelley and Hoffman 2004;Shelley and Golovatch 2011;Marek et al. 2012Marek et al. , 2016Wesener 2014Wesener , 2023 and the data presented here. Where no coordinates were given, approximate coordinates were taken based on the locality descriptions. A distributional map of the species from Chile was made based on the ecoregions provided by Olson et al. (2001) and satellite data from Maptiler and OpenStreetMap contributors.

Examination and photographs
Specimens were examined with a Zeiss Discovery V12 stereo microscope. Photographs were taken at different focus planes and stacked with MicroPublisher 5.0 RTV  Attems (1930Attems ( , 1936Attems ( , 1938; Turk (1947); Shelley and Hoffman (2004); Shelley and Golovatch (2011); Marek et al. (2012Marek et al. ( , 2016; Wesener (2014Wesener ( , 2023. Where no coordinates were available, approximate coordinates were taken based on the locality description. Map data from NaturalEarth. B Distribution of Notorhinus sp. nov. in Chile. Map data from Olson et al. (2001). camera (Q Imaging) mounted to a Leica Z6 imaging system with AUTO-MONTAGE PRO version 5.03.0061 (Synoptics Ltd). The number of body-rings was counted (including the collum, excluding the telson), and the length of the animals were measured from the photographs, and body-width was measured based on SEM images (see below) in IMAGEJ 1.53c (Schneider et al. 2012). Additional images are deposited on Zenodo (https://doi.org/10.5281/zenodo.7515111). According to a key provided by Shelley (1996: 23) members of the family Siphonorhinidae lack sensory pits on antennomeres 5 and 6 (see also Marek et al. 2012), as is the case in the specimens studied here (Figs 3E, 8C). However, lack of these sensory pits seems to apply only to the North American genus Illacme (Marek et al. 2012(Marek et al. , 2016, the Malagasy genus Madagascarhinus (Wesener 2023) and the South African genus Nematozonium (Shelley and Hoffman 2004), as these sensory pits have been reported for Siphonorhinus (Attems 1930(Attems , 1938 and

Scanning electron microscopy (SEM)
Kleruchus (Attems, 1938).  norhinus) and Kleruchus) numerous sensilla basiconica are located in sensory pits (Sinnesgruben sensu Attems 1930) on antennomeres 5 and 6. In Illacme few sensilla basiconica are arranged in rows along the apical margin of antennomeres 5 and 6 (Marek et al. 2012(Marek et al. , 2016 and in Madagascarhinus sensilla basiconica are arranged in 2 -3 rows on antennomeres 5 and 6 (Wesener 2023). In Nematozonium no sensory structures are evident on the antennae according to Shelley and Hoffman (2004). Notorhinus gen. nov. differs from Illacme by the fusion of the first legs' coxae to the sternite (Fig. 3G), forming a coxosternite (see Marek et al. 2012Marek et al. , 2016 for Illacme), as is the case in Siphonorhinus (see Enghoff et al. 2015). Furthermore, the specimens differ from Kleruchus by the presence of an anal scale/hypoproct (Figs 4F, 8I) (Analschuppe sensu Attems 1938). apically laminate/flattened branches and a single posterior spine-like branch (Fig. 5F). However, some of these characters are not well studied in the remaining genera of the Siphonorhinidae.

Remarks. Several characters are shared with the genus
Etymology. Noto is derived from the ancient greek νότος (nótos) meaning south and refers to the distribution of the genus in South America and the fact that it is the most southern record of the family Siphonorhinidae. Rhinus is derived from the ancient Greek ῥῑς (rhīś; genitive: ῥῑνός (rhīnós)), meaning nose, and refers to the acuminate head shape. Rhinus is often part of taxonomic names in the group (e.g. Siphonorhinidae Cook, 1895, Siphonorhinus Pocock, 1894, Madagascarhinus Wesener, 2023).

Affinities of Notorhinus gen. nov. to Illacme Cook and Loomis, 1928
Notorhinus gen. nov. is distinct from the remaining Siphonorhinidae genera in its morphology as pointed out in the genus diagnosis. However, it shows morphological similarities to the North American genus Illacme Cook and Loomis, 1928 or at least one of its members ( Table 1). Notorhinus gen. nov. shares with Illacme the structure of the gonopods with 7 podomeres in both pairs, the absence of sensory pits on the antennae and the presence of a lateral group of spiniform sensilla basiconica on antennomere 7, reaching between the apical cones. Furthermore, the single isolated spiniform sensilla basiconica on the anterior and posterior margin of antennomere 7 might also be present in Illacme plenipes Loomis, 1928 (compare Marek et al. 2012, fig. 13).
Notorhinus gen. nov. shares with Illacme plenipes the two backwards projecting spines behind the ozopores with three setae in between, but the spines are shorter and stouter than in I. plenipes. Notorhinus gen. nov. also shares with I. plenipes the projections on the posterior margin of the metazonites (limbus), but in Notorhinus gen. nov. these projections are rather fluke-shaped and not as well developed as in I. plenipes, in which these have been described as anchor-shaped (Marek et al. 2012(Marek et al. , 2016. Moreover, Notorhinus floresi sp. nov. shares with I. plenipes the presence of 3 branches (articles) on the posterior gonopod's apical podomeres, two laminate flattened ones and one spinous. N. floresi sp. nov. also shares with I. plenipes the straight posterior margin of the metazonite, while the margin is sinuate in Illacme tobini Marek, Shear and Krejca, 2016 and Notorhinus sp. (MNHNC 8390). Therefore, we suggest that the South American Notorhinus gen. nov. is more closely related to the North American Illacme, than to the Asian and African genera. However, most of these characters are not well studied in Siphonorhinidae, except for Illacme thanks to Marek et al. (2012Marek et al. ( , 2016.

Biogeography and habitat preferences of Siphonorhinidae in the Americas
Notorhinus floresi sp. nov. and the undescribed Notorhinus species (MNHNC 8390) occur in Chile at ca. 38° South, while Illacme plenipes and Illacme tobini occur  in California (USA) at ca. 37° North (Marek et al. 2012(Marek et al. , 2016. All three species occur close to the Pacific coast mostly in wet subterranean/poorly lighted microhabitats within temperate to Mediterranean humid native woodlands (Veblen et al. 2007;Marek et al. 2012). Thus, the known distribution of Siphonorhinidae in America is antitropical (amphitropical), meaning that the taxon shows a disjunct distribution with representatives occurring at similar latitudes in the northern and southern hemisphere, but not in the tropical region in between (Hubbs 1952). Examples of antitropical distributions include many marine taxa, like fishes (Randall 1981), whales (Barnes 1985), echinoderms (Naughton et al. 2014), mollusks (Koufopanou 1999;Hilbish et al. 2000), and terrestrial plants from North and South America (Raven 1963;Simpson et al. 2017), but also terrestrial insects like some wingless darkling beetles from Africa and Europe (Kamiński et al. 2021) and bees from North and South America (Wilson et al. 2014;Freitas et al. 2022). Observing such a distribution in millipedes is remarkable as these soil-organisms show a very limited dispersal ability and are often adapted to certain micro-habitats (Sierwald and Bond 2007;Golovatch and Kime 2009). The exchange between the North and South American flora and fauna, referred to as Great American Biotic Interchange (GABI), is often associated with the rise of the Isthmus of Pana-   (Leigh et al. 2014). However, for some taxa it has been shown that this exchange probably already started earlier in the Miocene (Cody 2010;Pinto-Sánchez et al. 2011;Wilson et al. 2014). The antitropical distribution of the American Siphonorhinidae might be explained by a once wider distribution in North and South America followed by extinction events in the tropics due to changes in climate and environmental conditions. However, the observed pattern might also be due to incomplete sampling, as these enigmatic animals, typically restricted to small soil habitats, are often overlooked, with I. plenipes collected for the first time since its description (Cook and Loomis 1928) in 2006 (Marek and Bond 2006), a second Illacme species only described recently (Marek et al. 2016), and the specimens described here only discovered in 2019 and 2020. Due to their restriction to very small habitats, Shelley (1996: 22) concluded that to find Siphonophorida "one must not only investigate the right habitat but also fortuitously dislodge the one or few rocks or logs that shelter them". Thus, "the probability of discovering siphonophorids is low and apparently chiefly a matter of chance" (Shelley 1996: 22). Furthermore, the group received only little attention by taxonomists (Jeekel 2001). Antitropical distributions have been assumed for other taxa, which had to be corrected later, when species were discovered in the tropics (e.g. Harris and Armitage 1997;Holzenthal and Harris 2002). Currently, we exclude an anthropogenic introduction of the species to Chile, as there is no species of the order known to have been expanded through human activities. This is further supported by the rarity of these millipedes across the globe (Marek et al. 2012), and the habitat in a small relict of native forest in which they were found. Specimens of N. floresi sp. nov. were encountered in a small, fragmented patch of native forest between eucalypt plantations near Camaravida, which lays within the Chilean Winter Rainfall-Valdivian Forest hotspot. The temperature and precipitation in this biodiversity hotspot is affected by anthropogenic climate change, and especially smaller protected areas appear to be vulnerable in this region (Fuentes-Castillo et al. 2020). The siphonorhinid millipedes might have evolved in mild consistent habitats and climate for hundred millions of years and thus they are dependent on certain microhabitats and climatic conditions (Marek et al. 2012). Therefore, climate change and habitat loss pose a serious risk to them, thus protection and preservation of these habitats is essential.

The Diplopoda fauna of Chile
The Chilean Diplopoda fauna shows predominantly Gondwanan affinities, with closely related taxa occurring in South Africa, Australia, and other Gondwanan landmasses, rather than in other South American regions (Shelley and Golovatch 2011;Golovatch 2014). With the addition of Siphonophorida a total of six native orders can be found in Chile (Chordeumatida, Polydesmida, Polyxenida, Polyzoniida, Siphonophorida and Spirost-reptida) (Parra-Gómez 2022). This is the first record of a new millipede order for the country in 65 years, the last addition was the order Polyzoniida in 1957 (Chamberlin 1957). Furthermore, the order Julida has been introduced to Chile, with 5 species native to Europe, and can even be found in natural habitats inside national parks (Golovatch 2014;Parra-Gómez 2022). The native millipede species usually have a narrow distribution, and are often endemic, with the highest diversity in the temperate regions at mid-latitudes (Parra-Gómez and Fernández 2022). However, the knowledge on their distribution remains obscure, with several latitudinal gaps without any records and fragmentary distributions for various taxa (Parra-Gómez 2022).

Conclusion
The discovery and description of Notorhinus gen. nov. is a significant contribution to our knowledge of the Colobognatha, as this is the first record of the order Siphonophorida in Chile and of the family Siphonorhinidae in South America. Notorhinus gen. nov. represents the most southern occurrence of the family Siphonorhinidae. While Notorhinus gen. nov. is morphologically distinct from the remaining Siphonorhinidae genera it shares several somatic and sexual characters with the North American genus Illacme Cook and Loomis, 1928.