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A case of mass occurrence of Sandalodesmus araujoi (Schubart, 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.) in a municipality of São Paulo, Brazil and description of the heretofore unknown female (Polydesmida, Chelodesmidae)

Um caso de ocorrência em massa de Sandalodesmus araujoi (Schubart, 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.) em um município de São Paulo, Brasil e descrição da fêmea até então desconhecida (Polydesmida, Chelodesmidae)

Abstract

Somatic characters are shared by many Chelodesmidae groups, and generic placement and species identifications traditionally have been based on gonopodal morphology. Female genitalic characters have been largely neglected and are rarely photographed or illustrated. This is rather unfortunate as the morphology of female genitalia presents important characters and may be decisive for developing a more robust family classification. We describe the heretofore unknown female of Sandalodesmus araujoi (Schubart, 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.), previously known only from the male holotype collected in São Paulo, Brazil in December 1943; discuss the utility of female genitalic characters for species delineation in Sandalodesmus; and report the first case of a mass occurrence in the Chelodesmidae. While an attempt at a formal diagnosis of Sandalodesmus females based on genitalic characters is premature, the vulvar morphology of the three taxa examined in this study suggests that female genitalia are species-specific. Some characters (i.e., asymmetric valves, presence of digitiform projections and reduction of setae on the internal basal portion of the valves) are constant between the species, suggesting utility for generic-level delineation. Mass occurrences of millipedes are typically unpredictable and likely related to variations in environmental conditions and/or anthropogenic modifications of natural habitats. Although the mass occurrence of S. araujoi reported herein was only observed once, the event coincides with the mating period of millipedes during the rainy season in Brazil. On the other hand, the region where the species was found has been the target of intense urban development, including replacement of natural habitats with residential areas, which may have influenced its population dynamics.

Keywords
millipedes; Neotropics; population outbreak; Sandalodesmini; swarming; taxonomy

Resumo

Os caracteres somáticos são compartilhados por muitos grupos de Chelodesmidae, e o posicionamento genérico e as identificações de espécies tradicionalmente têm sido baseadas na morfologia do gonópodo. Carateres genitais das fêmeas foram amplamente negligenciados e raramente são fotografados ou ilustrados. Isso é lamentável, pois a morfologia da genitália feminina apresenta características importantes e pode ser decisiva para o desenvolvimento de uma classificação mais robusta. Neste trabalho, descrevemos a até então desconhecida fêmea de Sandalodesmus araujoi (Schubart, 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.), anteriormente conhecida apenas pelo holótipo macho coletado em São Paulo, Brasil, em dezembro de 1943; discutimos a utilidade de caracteres genitais femininos para delineamento de espécies em Sandalodesmus; e relatamos o primeiro caso de ocorrência em massa para Chelodesmidae. Embora uma tentativa de diagnose formal para fêmeas de Sandalodesmus com base em caracteres genitais seja prematura, a morfologia vulvar dos três táxons examinados neste estudo, sugere que a genitália feminina é espécie-específica. Alguns caracteres (e.g. válvulas assimétricas, presença de projeções digitiformes e redução de cerdas na margem interna das válvas) são constantes entre as espécies do gênero, sugerindo utilidade para delineamento em nível genérico. Ocorrências em massa de milípedes são tipicamente imprevisíveis e provavelmente relacionadas a variações nas condições ambientais e/ou modificações antropogênicas de habitats naturais. Embora a ocorrência em massa de S. araujoi aqui relatada tenha sido observada apenas uma vez, o evento coincide com o período de reprodução dos milípedes durante a estação chuvosa no Brasil. Por outro lado, a região onde a espécie foi encontrada tem sido alvo de intenso desenvolvimento urbano, incluindo substituição de habitats naturais por áreas residenciais, o que pode ter influenciado sua dinâmica populacional.

Palavras-chave
Milípede; piolho-de-cobra; Neotrópicos; surto populacional; Sandalodesmini; taxonomia

Introduction

With over 5,000 described species, Polydesmida is the most diverse order within the class Diplopoda and includes the two most species-rich families of millipedes, Paradoxosomatidae Daday, 1889 (approx. 1,000 described species) and Chelodesmidae Cook, 1895 (750+ described species) (Hoffman 198027 HOFFMAN, R. L. 1980. Classification of the Diplopoda. Múseum d‘histoire naturelle, Genève. 237 pp., Shelley 200254 SHELLEY, R.M. 2002. A revised, annotated, family-level classification of the Diplopoda. Arthropoda Selecta 11(3): 187–207., Brewer et al. 201214 BREWER, M. S., P. SIERWALD, AND J. E. BOND. 2012. Millipede taxonomy after 250 years: classification and taxonomic practices in a mega-diverse yet understudied arthropod group. PLoS ONE 7(5): e37240. doi:10.1371/journal.pone.0037240
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, Nguyen and Sierwald 201340 NGUYEN A. D. AND P. SIERWALD. 2013. A worldwide catalog of the family Paradoxosomatidae Daday, 1889 (Diplopoda: Polydesmida). Check List 9(6): 1132–1353. doi:10.15560/9.6.1132.
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, Enghoff et al. 201522 ENGHOFF, H., S. I. GOLOVATCH, M. SHORT, P. STOEV, AND T. WESENER. 2015. Diplopoda - taxonomic overview, pp. 363 – 454. In A. Minelli (Ed), Treatise on Zoology - Anatomy, Taxonomy, Biology. The Myriapoda. Brill, Boston. 498 pp.). Chelodesmidae is divided into two subfamilies, Chelodesminae (139 genera) distributed across the Neotropical region, and Prepodesminae (37 genera) known from the Afrotropical and Palearctic regions (Hoffman 198027 HOFFMAN, R. L. 1980. Classification of the Diplopoda. Múseum d‘histoire naturelle, Genève. 237 pp.). Currently, 21 tribes are recognized within the Chelodesmidae, with 19 of them belonging to Chelodesminae, however, more than half of the described genera and species have yet to be assigned to a tribe (Bouzan et al. 202113 BOUZAN, R. S., L. F. M. INIESTA, AND A. D. BRESCOVIT. 2021. Cladistic analysis and taxonomic review of the millipede tribe Arthrosolaenomeridini Hoffman, 1976 (Polydesmida: Chelodesmidae). Zootaxa 4970(2): 201-256.).

Based chiefly on gonopodal characters, Hoffman (1982)28 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259. proposed the tribe Sandalodesmini to include the South American OncoleptodesmusSchubart, 195853 SCHUBART, O. 1958. “Leptodesmidae” Brazileiras. VI: Espécies novas do Estado do Rio Grande do Sul (Diplopoda, Proterospermophora). Revista Brasileira de Biologia 18(1): 23–32. and SandalodesmusSilvestri, 190255 SILVESTRI, F. 1902. Viaggio del Dr. A. Borelli nel Matto Grosso. VII. Diplopodi. Bollettino dei Musei di Zoologia e di Anatomia Comparata R. Università di Torino 17(432): 1–25.. Members of the tribe are small to moderately sized chelodesmids (25-45mm in length) with relatively slender bodies and reduced gonopods, characterized by the presence of a shield-like acropodite which conceals the solenomere in the lateral view, a subspatulate prefemoral process that partially envelops the acropodite, the presence of a spiniform process on the gonocoxa, and a modified, hook-like cannula (Hoffman 198228 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259.). Sandalodesmus differs from Oncoleptodesmus by the presence of only two macrosetae on the dorsal side of the gonocoxae and by the absence of spinulations on the lateral margin of the acropodite [except in Sandalodesmus repandus (Schubart, 1985); Silvestri 190255 SILVESTRI, F. 1902. Viaggio del Dr. A. Borelli nel Matto Grosso. VII. Diplopodi. Bollettino dei Musei di Zoologia e di Anatomia Comparata R. Università di Torino 17(432): 1–25., Schubart 195853 SCHUBART, O. 1958. “Leptodesmidae” Brazileiras. VI: Espécies novas do Estado do Rio Grande do Sul (Diplopoda, Proterospermophora). Revista Brasileira de Biologia 18(1): 23–32., Hoffman 198228 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259., Rojas-Buffet et al. 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
]. Sandalodesmus includes 14 species distributed across Argentina, Brazil, Paraguay, and Uruguay and Oncoleptodesmus includes four species only known from the Brazilian state of Rio Grande do Sul (Attems 19313 ATTEMS, C. M. T. GRAF VON. 1931. Die Familie Leptodesmidae und andere Polydesmiden. Zoologica Stuttgart (79): 1–150., 19384 ATTEMS, C. M. T. GRAF VON. 1938. Myriapoda 3. Polydesmoidea II. Fam. Leptodesmidae, Platyrhachidae, Oxydesmidae, Gomphodesmidae. Das Tierreich 69: 1–487.; Schubart 195853 SCHUBART, O. 1958. “Leptodesmidae” Brazileiras. VI: Espécies novas do Estado do Rio Grande do Sul (Diplopoda, Proterospermophora). Revista Brasileira de Biologia 18(1): 23–32.; Hoffman 198228 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259.; Rojas-Buffet et al. 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
). Sandalodesmus was reviewed by Hoffman (1982)28 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259. and recently Rojas-Buffet et al. (2022)48 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
provided an updated key to the males.

Somatic characters are shared by many genera within the Chelodesmidae and generic placement and species identification have been traditionally based on gonopodal morphology (Hoffman 197126 HOFFMAN, R. L. 1971. Chelodesmid studies V. Some new, redefined, and resurrected Brazilian genera. Arquivos de Zoologia, São Paulo 20(4): 225–277. doi:10.11606/issn.2176-7793.v20i4p225-277.
https://doi.org/10.11606/issn.2176-7793....
, Pena-Barbosa et al. 201344 PENA-BARBOSA, J. P. P., P. SIERWALD, AND A. D. BRESCOVIT. 2013. On the largest chelodesmid millipedes: taxonomic review and cladistic analysis of the genus Odontopeltis Pocock, 1894 (Diplopoda; Polydemsida; Diplopoda). Zoological Journal of the Linnean Society 169 (4): 737–764. doi:10.1111/zoj12086.
https://doi.org/10.1111/zoj12086...
, Bouzan et al. 2017a8 BOUZAN, R. S., J. P. P. PENA-BARBOSA, AND A. D. BRESCOVIT. 2017a. Two new Brazilian species of Chelodesmidae of the genera Iguazus and Tessarithys (Diplopoda: Polydesmida). Zoologia 34: 1-8. doi:10.3897/zoologia.34.e19986.
https://doi.org/10.3897/zoologia.34.e199...
). Female genitalic characters have been largely neglected, seldom examined, and rarely photographed or illustrated (Brölemann 190216 BRÖLEMANN, H. W. 1902. Myriapodes recueillis par M. E. Gounelle au Brésil. Annales de la Société Entomologique de France 71: 649–694.; Schubart 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.; Hoffman 1990a29 HOFFMAN, R. L. 1990a. Chelodesmid studies XX. Millipeds of the new Brazilian tribe Cornalatini (Polydesmida: Chelodesmidae). Papéis Avulsos de Zoología, São Paulo 37(2): 23–37., 1990b30 HOFFMAN, R. L. 1990b. Chelodesmid studies XXIII. Proposal of a new tribe for the disjunct Brasilian genus Macrocoxodesmus (Diplopoda, Polydesmida, Chelodesmidae). Papéis Avulsos de Zoologia 37(11): 167–172., 200031 HOFFMAN, R. L. 2000. A synopsis of the Telonychopodini, a tribe of Pantanalian chelodesmid millepeds (Polydesmida: Chelodesmidae). Myriapodologica 7(1): 1–13.; Pena-Barbosa et al. 201344 PENA-BARBOSA, J. P. P., P. SIERWALD, AND A. D. BRESCOVIT. 2013. On the largest chelodesmid millipedes: taxonomic review and cladistic analysis of the genus Odontopeltis Pocock, 1894 (Diplopoda; Polydemsida; Diplopoda). Zoological Journal of the Linnean Society 169 (4): 737–764. doi:10.1111/zoj12086.
https://doi.org/10.1111/zoj12086...
; Bouzan et al. 2017b9 BOUZAN, R. S., J. P. P. PENA-BARBOSA, AND A. D. BRESCOVIT. 2017b. Taxonomic review of the genus Atlantodesmus Hoffman, 2000 (Polydesmida: Chelodesmidae). Zootaxa 4236(2): 269-290. doi:10.11646/zootaxa.4236.2.3.
https://doi.org/10.11646/zootaxa.4236.2....
, 2018a10 BOUZAN, R. S., L. F. M. INIESTA, AND A. D. BRESCOVIT. 2018a. A review of the millipede genus Rupidesmus Schubart, 1952 (Polydesmida: Chelodesmidae). Zootaxa 4434(3): 589-599., 2018b11 BOUZAN, R. S., L. F. M. INIESTA, C. A. R. SOUZA, AND A. D. BRESCOVIT. 2018b. A new record after a century and description of the female of Plectrogonodesmus gounellei (Brölemann 1902) (Polydesmida: Chelodesmidae). Studies on Neotropical Fauna and Environment 54(1): 61-68. doi:10.1080/01650521.2018.1536018.
https://doi.org/10.1080/01650521.2018.15...
). Sandalodesmus is no exception, and the females of only six of the 14 known species have been described in some, often very abbreviated, manner. To date, only the females of Sandalodesmus joachimadisiRojas-Buffet and Bouzan, 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
have been described in detail, including description of genitalic characters, and illustrated (Rojas-Buffet et al. 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
). This is rather unfortunate as the morphology of the female genitalia presents important characters and may be decisive for developing a more robust classification of the Chelodesmidae (see Hoffman 201232 HOFFMAN, R. L. 2012. New genera for two poorly-known millipeds from Bahia (Polydesmida: Chelodesmidae). Papeis Avulvsos de Zoologia 52(8): 103–110.).

Mass occurrences (seemingly sudden increases in local abundance) in the Diplopoda are a result of natural cycles (reproduction swarming or lifecycle periodicity) or unpredictable changes in climate, resource availability, or fragmentation of natural habitat (David 201520 DAVID, J. F. 2015. Diplopoda – ecology, pp. 303–327. In Minelli, A., ed. Treatise on Zoology - Anatomy, Taxonomy, Biology. The Myriapoda. Boston: Brill. 498 pp., Niijima et al. 202143 NIIJIMA, K., M. NII, AND J. YOSHIMURA. 2021. Eight-year periodical outbreaks of the train millipede. Royal Society Open Science 8: 201399. doi:10.1098/rsos.201399.
https://doi.org/10.1098/rsos.201399...
). Such events have been reported from Africa, Eurasia, and The Americas, and vary in magnitude from localized occurrences of hundreds of individuals to millions of individuals covering extensive areas (Cloudsley-Thompson 194917 CLOUDSLEY-THOMPSON, J. L. 1949. The significance of migration in myriapods. The Annals and Magazine of Natural History 12(2): 947–62., Niijima et al. 202143 NIIJIMA, K., M. NII, AND J. YOSHIMURA. 2021. Eight-year periodical outbreaks of the train millipede. Royal Society Open Science 8: 201399. doi:10.1098/rsos.201399.
https://doi.org/10.1098/rsos.201399...
). While small scale swarms can occasionally be a nuisance near human habitations in urban and suburban areas, large outbreaks have been reported to impact livestock, crop production, and even interfere with transportation (Cloudsley-Thompson 194917 CLOUDSLEY-THOMPSON, J. L. 1949. The significance of migration in myriapods. The Annals and Magazine of Natural History 12(2): 947–62., Niijima et al. 202143 NIIJIMA, K., M. NII, AND J. YOSHIMURA. 2021. Eight-year periodical outbreaks of the train millipede. Royal Society Open Science 8: 201399. doi:10.1098/rsos.201399.
https://doi.org/10.1098/rsos.201399...
). In an attempt to provide a more robust classification of millipede mass occurrences, Niijima et al. (2021)43 NIIJIMA, K., M. NII, AND J. YOSHIMURA. 2021. Eight-year periodical outbreaks of the train millipede. Royal Society Open Science 8: 201399. doi:10.1098/rsos.201399.
https://doi.org/10.1098/rsos.201399...
proposed the separation of these events into swarming (hundreds of individuals), mass emergence (thousands), and outbreak (millions), based on the number of individuals observed.

One of the largest millipede outbreaks ever recorded, occurred in West Virginia, USA in June, 1918 when an estimated 65,340,000 Apheloria virginiensis corrugata (Wood, 1864) covered 75 acres of farmland for over a month (Cloudsley-Thompson 194917 CLOUDSLEY-THOMPSON, J. L. 1949. The significance of migration in myriapods. The Annals and Magazine of Natural History 12(2): 947–62.). During this event, farmers were reportedly nauseated by the defensive chemicals released by the millipedes and cattle refused to graze in the impacted areas (Cloudsley-Thompson 194917 CLOUDSLEY-THOMPSON, J. L. 1949. The significance of migration in myriapods. The Annals and Magazine of Natural History 12(2): 947–62.). An equally impressive series of mass outbreaks have been reported for Parafontaria laminata (Attems, 1909) in Japan where mass occurrences of this species have caused multiple road and railroad obstructions between 1920 and 1984 (Niijima and Shinohara 198842 NIIJIMA, K. AND K. SHINOHARA. 1988. Outbreaks of the Parafontaria laminata group (Diplopoda, Xystodesmidae). Journal of Ecology (Japan) 38: 257–268., Niijima 199841 NIIJIMA, K. 1998. Effects of outbreak of the train millipede Parafontaria laminata armigera Verhoeff (Diplopoda: Xystodesmidae) on litter decomposition in a natural beech forest in Central Japan. 1. Density and biomass of soil invertebrates. Ecological Research 13: 41–53. doi:10.1046/j.1440-1703.1998.00242.x.
https://doi.org/10.1046/j.1440-1703.1998...
, Niijima et al. 202143 NIIJIMA, K., M. NII, AND J. YOSHIMURA. 2021. Eight-year periodical outbreaks of the train millipede. Royal Society Open Science 8: 201399. doi:10.1098/rsos.201399.
https://doi.org/10.1098/rsos.201399...
). Interestingly, Parafontaria laminata armigera Verhoeff, 1936 was recently shown to have a lifecycle akin to periodical cicadas with an outbreak event occurring every eight years (Niijima et al. 202143 NIIJIMA, K., M. NII, AND J. YOSHIMURA. 2021. Eight-year periodical outbreaks of the train millipede. Royal Society Open Science 8: 201399. doi:10.1098/rsos.201399.
https://doi.org/10.1098/rsos.201399...
).

In Brazil, millipede population outbreaks are most commonly associated with non-native species including the Asian Oxidus gracilis (C. L. Koch, 1847) and Orthomorpha coarctata (Saussure, 1860) (Polydesmida, Paradoxosomatidae), and more recently the Portuguese millipede, Ommatoiulus moreleti (Lucas, 1860) (Julida, Julidae) (Iniesta et al. 202034 INIESTA, L. F. M., R. S. BOUZAN, P. E. S. RODRIGUES, T. M. ALMEIDA, R. OTT, AND A. D. BRESCOVIT. 2020. Ecological niche modeling predicting the potential invasion of the non-native millipede Oxidus gracilis (C. L. Koch, 1847) (Polydesmida: Paradoxosomatidae) in Brazilian Atlantic Forest. Annales de la Société entomologique de France (N.S.) 56(5): 1–8. doi:10.1080/00379271.2020.1834873.
https://doi.org/10.1080/00379271.2020.18...
, 202135 INIESTA, L. F. M., R. S. BOUZAN, P. E. S. RODRIGUES, T. M. ALMEIDA, R. OTT, A. D. BRESCOVIT. 2021. A preliminary survey and range extension of millipedes species introduced in Brazil (Myriapoda, Diplopoda). Papéis Avulsos de Zoologia 61: 1–18. doi:10.11606/1807-0205/2021.61.88.
https://doi.org/10.11606/1807-0205/2021....
, 202236 INIESTA, L. F. M., A. D. BRESCOVIT, D. G. A. JÚNIOR, AND R. S. BOUZAN. 2022. Into the New World: first report of introduction of the Portuguese millipede Ommatoiulus moreleti (Lucas, 1860) (Julida: Julidae) in South America and its potential invasion range into the continent. Annales de la Société entomologique de France (N.S.) 58(3): 187–196. doi:10.1080/00379271.2022.2084641.
https://doi.org/10.1080/00379271.2022.20...
). Although all three species reach high densities in urban areas of southeastern Brazil, O. gracilis and O. coarctata have also become established in rural and natural environments, including forests, caves, and islands (Iniesta et al. 202135 INIESTA, L. F. M., R. S. BOUZAN, P. E. S. RODRIGUES, T. M. ALMEIDA, R. OTT, A. D. BRESCOVIT. 2021. A preliminary survey and range extension of millipedes species introduced in Brazil (Myriapoda, Diplopoda). Papéis Avulsos de Zoologia 61: 1–18. doi:10.11606/1807-0205/2021.61.88.
https://doi.org/10.11606/1807-0205/2021....
). There is little published information regarding population outbreaks of native millipedes in Brazil, except for those regarded as agricultural pests. The majority of these accounts concern species of Spirostreptida (Spirostreptidae and Pseudonannolenidae) in cultivated areas where they have been reported to cause damage to seedlings, tubers, and fruits (Schubart 194249 SCHUBART, O. 1942. Os Myriápodes e suas relações com a agricultura - Com uma bibliografia completa sôbre o assunto. Papéis Avulsos do Departamento de Zoologia 2(16): 205–234.; Boock and Lordello 19527 BOOCK, O. J. AND L. G. E. LORDELLO. 1952. Diplópoda depredador de tubérculos de batatinha. Bragantia12: 343–348. doi:10.1590/S0006-87051952000400006.
https://doi.org/10.1590/S0006-8705195200...
; Lordello 195439 LORDELLO, L. G. E. 1954. Observação sobre alguns Diplópodos de interesse agrícola. Anais da Escola Superior de Agricultura “Luiz de Queiroz” 11: 69–76. doi:10.1590/S0071-12761954000100004.
https://doi.org/10.1590/S0071-1276195400...
; Boccardo et al. 19976 BOCCARDO, L., C. H. S. PENTEADO, AND R. JUCÁ-CHAGAS. 1997. Swarming of millipedes, a new case noticed in the district of Patrocínio – MG - Brazil. Journal of Advanced Zoology 18: 62–63., 20025 BOCCARDO, L., R. JUCÁ-CHAGAS, AND C. H. S. PENTEADO. 2002. Migration and Population Outbreaks of Millipedes in the Coffee Plantations, Region of Alto Paranaiba, MG, Brazil. Holos Environment 2(2): 220–223.). To date, there have been no published accounts of swarming or population outbreaks in the Chelodesmidae.

We report the first case of a mass occurrence in the Chelodesmidae and describe the heretofore unknown female of Sandalodesmus araujoi (Schubart, 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.), previously known only from the male holotype collected in the state of São Paulo, Brazil in 1943. In addition, we discuss the utility of female genitalic characters for species delineation in Sandalodesmus and provide additional information on male characters, including measurements and SEM images.

Materials and Methods

The material examined is deposited in the following collections (curators in parentheses): Instituto Butantan, São Paulo, Brazil (IBSP; A.D. Brescovit), Arachnida and Myriapoda collection of Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay (FCE-Myr; M. Simó). Scanning electron micrographs were taken using a FEI Quanta 250 SEM (FEI, Oregon, USA) with an attached SLR digital camera at Instituto Butantan. Specimens selected for scanning electron imaging were cleaned two times (30 sec. each) ultrasonically, transferred to an ascending series of ethanol dilutions (70, 80, 90, and 100%), bathed for 15 minutes at each step, and critical-point dried. The samples were mounted on aluminum stubs and coated with gold in a sputter coater for 240 seconds. In addition, relevant morphological features were photographed with a Leica DFC 500 digital camera mounted on a Leica MZ16A stereomicroscope and measured to the nearest 0.01 mm with Leica Application Suite ver. 2.5.0 (Leica Camera, Wetzler, Germany). Body-rings were measured in dorsal view, and antennomere lengths were measured in lateral view.

Female genitalic characters of S. araujoi (five specimens), S. joachimadisiRojas-Buffet and Bouzan, 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
(two specimens) and Sandalodesmus sp. (two specimens from Estação Ecológica Jureia/Itatins, São Paulo, Brazil) were examined and photographed in order to explore their utility in species delineation and classification.

Distribution maps were generated using the freeware DIVA-GIS ver. 7.5.0 (Hijmans et al. 200124 HIJMANS, R. J., M. CRUZ, E. ROJAS AND L. GUARINO. 2001. DIVA-GIS, Version 1.4. A geographic information system for the management and analysis of genetic resources data. Manual. International Potato Center, Lima, Peru.).

Terminology of sexual and somatic characters follows Attems (1898)2 ATTEMS, C. M. T. GRAF VON. 1898. System der Polydesmiden. I. Theil. Denkschriften der Kaiserlichen Akademie der Wissenschaften zu Wien, Mathematisch-Naturwissenschaftliche Classe 67: 221–482., Brölemann (1900)15 BRÖLEMANN, H. W. 1900. Myriapodes d’Amérique. Mémoires de la Société Zoologique de France 13: 89–131., Pena-Barbosa et al. (2013)44 PENA-BARBOSA, J. P. P., P. SIERWALD, AND A. D. BRESCOVIT. 2013. On the largest chelodesmid millipedes: taxonomic review and cladistic analysis of the genus Odontopeltis Pocock, 1894 (Diplopoda; Polydemsida; Diplopoda). Zoological Journal of the Linnean Society 169 (4): 737–764. doi:10.1111/zoj12086.
https://doi.org/10.1111/zoj12086...
, and Koch (2015)38 KOCH, M. 2015. General morphology. In: MINELLI, A. (Ed.) Treatise on Zoology – Anatomy, Taxonomy, Biology. The Myriapoda. Brill, Leiden, 7–68..

Results

The mass occurrence reported herein was brought to the lead author’s attention in October 2021 when videos of the event were sent to him by Nicoly Calcagniti (Supplementary Material 1). Subsequently, several male and female specimens were received by the authors and identified as S. araujoi. The mass occurrence took place in the municipality of Pardinho (–23.0825, –48.3852), approx. 30 km southeast of the type locality of S. araujoi in the municipality of São Manuel (–22.7423, –48.6191) (Figure 1). According to the residents of the municipality, thousands of individuals were observed around house entrances, gardens, and on pavement in the morning and afternoon hours.

Figure 1.
Known distribution of S. araujoi with the São Manuel type locality shown in yellow and the new record from Pardinho shown in red.

The locality where the mass occurrence took place is part of a transitional zone between the Cerrado and Atlantic Forest biomes in the state of São Paulo (Coutinho 200619 COUTINHO, L. M. 2006. O conceito de bioma. Acta Botanica Brasilica 20(1): 13–23. doi:10.1590/S0102-33062006000100002.
https://doi.org/10.1590/S0102-3306200600...
). The area has a subhumid temperate climate and is characterized by a patchwork of herbaceous and forested habitats which have resulted from retractions and transgressions during the Quaternary (Coutinho 200619 COUTINHO, L. M. 2006. O conceito de bioma. Acta Botanica Brasilica 20(1): 13–23. doi:10.1590/S0102-33062006000100002.
https://doi.org/10.1590/S0102-3306200600...
, Alvares et al. 2014, Smith and Mayle 201756 SMITH, R. J, AND F. E. MAYLE. 2017. Impact of mid-to late Holocene precipitation changes on vegetation across lowland tropical South America: a paleo-data synthesis. Quaternary Research 89(1): 134–155. doi:10.1017/qua.2017.89.
https://doi.org/10.1017/qua.2017.89...
). Since the second half of the 20th Century, the region has been severely impacted by human activities, including deforestation, farming practices, livestock production, and accelerated urbanization (Ratter et al. 199745 RATTER J. A., J. F. RIBEIRO, S. BRIDGEWATER. 1997. The Brazilian Cerrado vegetation and threats to its biodiversity. Annals of Botany 80: 223–230. doi:10.1006/anbo.1997.0469.
https://doi.org/10.1006/anbo.1997.0469...
).

Order Polydesmida Pocock, 1887

Family Chelodesmidae Cook, 1895

Subfamily Chelodesminae Cook, 1895

Tribe Sandalodesmini Hoffman, 198228 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259.

Genus SandalodesmusSilvestri, 190255 SILVESTRI, F. 1902. Viaggio del Dr. A. Borelli nel Matto Grosso. VII. Diplopodi. Bollettino dei Musei di Zoologia e di Anatomia Comparata R. Università di Torino 17(432): 1–25.

Sandalodesmus araujoi (Schubart, 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.)

(Figures 1–17)

Leptodesmus araujoiSchubart 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.: 171, figure 4 (male holotype from São Manuel [-22.7423, -48.6191], São Paulo, Brazil, 09–11.xii.1943, R. L. Araujo leg., deposited at MZSP, examined); Schubart 195552 SCHUBART, O. 1955. Materiais para uma fauna do Estado de Sao Paulo - os Leptodesmidae. Arquivos do Museu Nacional, Rio de Janeiro 42: 507–540.: 516.

Figure 4.
A–F. SEM images of genitalic characters of S. araujoi (IBSP 14279). A, Left gonopod, ectal view. B, Detail of mesal portion of the acropodial process, ectal view. C, Right gonopod, mesal view. D, Left vulva, ectal view. E, Right vulva, ventral view. F, Detail of the junction of the valves, ventral view. Abbreviations: ap= acropodital process, ca= cannula, cx= gonocoxa, ev= external valve, iv= internal valve, op= operculum, pf= prefemur, pfp= prefemoral process, s= solenomere, sg= seminal groove. The subtriangular secondary process is hidden by the prefemoral process in ectal and mesal view.

Leptodesmus (Gonioleptodesmus) araujoi:-- Schubart 195853 SCHUBART, O. 1958. “Leptodesmidae” Brazileiras. VI: Espécies novas do Estado do Rio Grande do Sul (Diplopoda, Proterospermophora). Revista Brasileira de Biologia 18(1): 23–32.: 29.

Gonioleptodesmus araujoi:-- Hoffman 196725 HOFFMAN, R. L. 1967. Chelodesmid Studies III. Notes on the status of Gonioleptodesmus, the description of a new species from Minas Gerais, and a key to the presently known members of the genus (Diplopoda, Polydesmida). Papéis Avulsos de Zoología 21(4): 33–42.: 34.

Sandalodesmus araujoi:-- Hoffman 198228 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259.: 251; Bouzan et al. 2018c12 BOUZAN, R. S., L. F. M. INIESTA, J. P. P. PENA-BARBOSA, AND A. D. BRESCOVIT. 2018c. Annotated checklist of the millipede family Chelodesmidae Cook, 1895 from São Paulo state, Brazil (Diplopoda: Polydesmida). Papéis Avulsos de Zoologia 58: 1–19. doi:10.11606/1807-0205/2018.58.06.
https://doi.org/10.11606/1807-0205/2018....
: 11; Rojas-Buffet et al. 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
: 266.

New record. BRAZIL, São Paulo, Pardinho; –23.0825, –48.3852; 900 m; October 2021; N. Calcagniti leg.; in urban areas, around house entrances, gardens, and on pavement; 1♂ (IBSP 14277); 1♀ (IBSP 14278); 6♂♂, 6♀♀ (IBSP 14279).

Diagnosis. Males of S. araujoi can be separated from those of Sandalodesmus gasparae (Schubart, 194450 SCHUBART, O. 1944. Os Diplopodos de Pirassununga. Acta Zoologica Lilloana 2: 321–440.) (Schubart 194450 SCHUBART, O. 1944. Os Diplopodos de Pirassununga. Acta Zoologica Lilloana 2: 321–440., figures 22-23) and Sandalodesmus hippocampus (Schubart, 194450 SCHUBART, O. 1944. Os Diplopodos de Pirassununga. Acta Zoologica Lilloana 2: 321–440.) (Schubart 194450 SCHUBART, O. 1944. Os Diplopodos de Pirassununga. Acta Zoologica Lilloana 2: 321–440., figures 25-26), the only other Sandalodesmus species known from the state of São Paulo, by the presence of a prominent subtriangular, secondary process on the lateral side of the acropodite (Figures 4A, C). In addition, males of S. araujoi can be separated from those of Sandalodesmus salvadorii (Silvestri, 1895), the only other member of the salvadorii species group (see Hoffman [1982]28 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259.), based on the rounded, mesally curving acropodite (Figures 4A, C), which is subtriangular and curving cephalad in S. salvadorii (Hoffman 198228 HOFFMAN, R. L. 1982. Chelodesmid studies. XVIII. A synopsis of the genus Sandalodesmus Silvestri, 1902, and proposal of the new tribe Sandalodesmini (Polydesmida: Chelodesmidae). Spixiana 5(3): 247–259., Rojas-Buffet et al. 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
).

Description. Male (new data; IBSP 14277): With characteristics typical for the genus. Coloration in life: body rings dark brown, head, antennae, and legs reddish-brown, paranota tips yellowish (Figures 2A–D). Head: epicranial macrosetae 2–2, interantennal macrosetae 1–1, frontal macrosetae 1–1. Body: rings smooth; paranota subtriangular, with standard polydesmidan pore formula (5, 7, 9, 10, 12, 13, 15–19; Figures 3B–D); ozopores situated posteriorly (Figure 3C); sternite of 4th body ring with two pairs of partly appressed projections (Figure 3A). Legs: with ventral tibial pads, except for the last leg pair (Figures 3E–F).

Figure 2.
A–D. Living specimens of S. araujoi from Pardinho, São Paulo, Brazil.
Figure 3.
A–F. SEM images of somatic characters of S. araujoi (IBSP 14279). A, Projections of sternite 4, ventral view. B, Midbody rings, dorsal view. C, Paranota with ozopore, dorsal view. D, Paranota, dorsal view. E, Midbody leg. F, Detail of tibial ventral pad. Abbreviations: vp= ventral pad, oz= ozopore.

Gonopods: prefemoral process (pfp) subtriangular, slightly twisted, and parallel to acropodite (ap) (Figures 4A, C); cannula (ca) hook-shaped (Figure 4C); seminal groove (sg) S-shaped along the acropodite, ending at apex of solenomere (Figure 4C); prefemoral region (pf) densely setose (Figures 4A, C); acropodite (ap) broad, elongated, strongly curved mesad (Figures 4A, C), with part of its margin serrated mesally (Figures 4A–B, white arrow), and with a prominent subtriangular secondary process; solenomere (s) sickle-shaped, curved mesad (Figure 4C).

Measurements (mm): Body: total length (n = 3), average = 34.1 (range = 29.1 – 38.5); width of 10th body ring (n = 3), average = 3.6 (range = 3.3–3.8). Antennomere lengths (1–7): 0.33, 0.91, 0.87, 0.80, 0.88, 0.82, 0.21. Telson length: 0.6.

Female (IBSP 14278): Coloration in life as in male. Similar to male in general body outline and somatic characters, except sternite of 4th body ring with less conspicuous and separate projections, all remaining sternites and all legs without modification. Posterior margin of vulvar aperture smooth, without projections. Vulvae (Figures 4D–F): densely setose, ovoid in ventral view and subrectangular in lateral view. External and internal valves asymmetrical, projecting ventrad. External valve (Ev) projecting distad, distinctly longer than the internal valve (Iv). Internal margins of valves irregular medially, with digitiform projections (Figure 4F). Internal basal portion of valves, in ventral view without setae. Operculum (Op): small, flattened, with setae at the base, approximately 1/6 size of valves.

Measurements (mm): Body: total length (n = 3), average = 30.1 (range = 29.2 – 30.8); width of 10th body ring (n = 3), average = 3.3 (range = 3.2–3.4). Antennomere lengths (1–7): 0.32, 0.81, 0.67, 0.70, 0.74, 0.73, 0.20. Width of posterior margin of vulvar aperture 1.4. Vulvae: ventral length 0.88, ventral width 0.53. Valves asymmetrical. External valve: lateral length 0.72, lateral width 0.61. Internal valve: lateral length 0.61, lateral width 0.59. Operculum: ventral length 0.14, ventral width 0.34. Telson length: 0.6.

In comparison to S. araujoi, the size difference between the external and internal valves of Sandalodesmus sp. (from Estação Ecológica Jureia/Itatins, São Paulo, Brazil) is less pronounced, and those of Sandalodesmus sp. have larger and fewer digitiform projections which continue to the apical portion of the valves (Figures 4E-F; 5B, 5D-F). In addition, the vulvae of Sandalodesmus sp. have a pronounced horizontal ridge spanning both valves and delineating the bottom third of each (Figures 5C–D). As compared to the previous two species, the valves of S. joachimadisi are relatively symmetrical, with only a slight enlargement of the external valve, and with fewer and more robust digitiform projections on the internal margin (Figures 5A–B). In addition, the lateral profile of the valves of S. joachimadisi is distinctly subtriangular while those of both S. araujoi and Sandalodesmus sp. are subrectangular, narrower near the operculum and widening towards the apex (Figures 4D, 5A, 5C).

Figure 5.
A–F. Steromicroscope (5A–B) and SEM images (5C–F) of vulvae of Sandalodesmus species: A, Right vulva of S. joachimadisi (FCE-Myr 0664), ectal view; B, Right vulva of S. joachimadisi (FCE-Myr 0664), ventral view. C, Left vulva of Sandalodesmus sp. (IBSP 3741), ectal view. D, Right vulva of Sandalodesmus sp. (IBSP 3741), ventral view. E, Detail of the junction of the valvae of Sandalodesmus sp. (IBSP 3741), ventral view. F, Detail of the operculum of Sandalodesmus sp. (IBSP 3741), ectal view. Abbreviations: ev= external valve, iv= internal valve, op= operculum.

Discussion

Although numerous collection events have targeted the area surrounding the type locality of S. araujoi, until the mass occurrence reported herein, this species was known only from the single male holotype collected in the municipality of São Manuel in December 1943 (Schubart 194651 SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus (Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de Ciências 18: 165–202.).

Millipede female genitalia undoubtedly contain valuable taxonomic information, however, they have been historically neglected and have been rarely included in species descriptions. Genitalic characters of female Sandalodesmus remain poorly known, and only those of S. joachimadisi have been described and properly illustrated (Rojas-Buffet et al. 202248 ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M. SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the first Chelodesmidae member from Uruguay with an updated key to species of the genus (Diplopoda: Polydesmida). Zootaxa 5150(2): 260–268. doi:10.11646/zootaxa.5150.2.5.
https://doi.org/10.11646/zootaxa.5150.2....
: figure 3D). While an attempt at a formal diagnosis of females based on genitalic characters is premature, the vulvar morphology of the three taxa examined herein suggests that Sandalodesmus female genitalia are species-specific. In addition, some characters, such as the asymmetric (to different degrees) valves, and the presence of digitiform projections and the reduction or absence of setae on the internal basal portion of the valves, are constant between the species, suggesting utility for generic-level delineation. Additional studies on the morphology of Sandalodesmus female genitalia are needed to assess their systematic importance.

With the exception of the population outbreaks of the Japanese P. laminata armigera, mass occurrences of millipedes are typically unpredictable and likely related to variations in environmental conditions and/or anthropogenic modifications of natural habitats. Although the mass occurrence of S. araujoi reported herein was only observed once, the timing of the event coincides with the mating period of millipedes during the rainy season (October–April) in Brazil (see Alvares et al. 20131 ALVARES, C. A., J. Z. STAPE, P. C. SENTELGA, J. L. MORAES-GONÇALVES, AND G. SPAROVEK. 2013. Köppen’s climate classification map for Brazil. Meteorologische zeitschrift 22(6): 711–728.). On the other hand, the region where the species was found has been the target of intense urban development, including replacement of natural vegetation with residential areas, which may have influenced its population dynamics. More detailed studies are needed to tease apart the factors contributing to these largely unpredictable events.

The original communities of the Cerrado and the Atlantic Forest in southeastern Brazil, two of the world’s premier biodiversity hotspots, have been severely altered by anthropogenic activities, such as medium to large-scale farming practices, livestock production, and accelerated urbanization, and are rapidly disappearing (Fonseca 198523 FONSECA, G. A. B. 1985. The vanishing Brazilian Atlantic forest. Biological Conservation 34: 17–34. doi:10.1016/0006-3207(85)90055-2.
https://doi.org/10.1016/0006-3207(85)900...
, Durigan et al. 200721 DURIGAN, G., M. F. SIQUEIRA, G. A. D. C. FRANCO. 2007. Threats to the Cerrado remnants of the state of São Paulo, Brazil. Scientia Agricola 64(4): 355–363. doi:10.1590/S0103-90162007000400006.
https://doi.org/10.1590/S0103-9016200700...
). To date, approximately 50% of the Cerrado has been destroyed by human activities (Rodriguez-Zorro et al. 202247 RODRI´GUEZ-ZORRO P. A., M. P. LEDRU, C. FAVIER, E. BARD, D. C. BICUDO, M. GARCIA, G. MARQUARDT, F. ROSTEK, A. O. SAWAKUCHI, Q. SIMON, K. TACHIKAWA. .2022. Alternate Atlantic forest and climate phases during the early Pleistocene 41 kyr cycles in southeastern Brazil. Quaternary Science Reviews 286:107560. doi:10.1016/j.quascirev.2022.107560.
https://doi.org/10.1016/j.quascirev.2022...
), and only 10% of the original vegetation of the Atlantic Forest remains (Colombo and Joly 201018 COLOMBO, A. F., AND C. A. JOLY. 2010. Brazilian Atlantic Forest lato sensu: the most ancient Brazilian forest, and a biodiversity hotspot, is highly threatened by climate change. Brazilian Journal of Biology 70: 697–708. doi:10.1590/S1519-69842010000400002.
https://doi.org/10.1590/S1519-6984201000...
, Joly et al. 201437 JOLY, C. A., J. P. METZGER, M. TABARELLI. 2014. Experiences from the Brazilian Atlantic Forest: ecological findings and conservation initiatives. New Phytologist 204: 459–473. doi:10.1111/nph.12989.
https://doi.org/10.1111/nph.12989...
, Rezende et al. 201846 REZENDE, C. L., F. R. SCARANO, E. D. ASSAD, C. A. JOLY, J. P. METZGER, B. B. N. STRASSBURG, M. TABARELLI, G. A. FONSECA, R. A. MITTERMEIER. 2018. From hotspot to hopespot: an opportunity for the Brazilian Atlantic Forest. Perspectives in Ecology and Conservation 16: 208–214. doi:10.1016/j.pecon.2018.10.002.
https://doi.org/10.1016/j.pecon.2018.10....
). The region, long known for its vertebrate and invertebrate diversity and high levels of endemicity, was also recently shown to contain the highest species richness and the highest concentration of threatened Spirostreptida in Brazil making its conservation vital for the protection of numerous plant and animal taxa (Iniesta et al. 202333 INIESTA, L. F. M., R. S. BOUZAN, J. MEANS, K. IVANOV, AND A. D. BRESCOVIT. 2023. Where are they from and where are they going? Detecting areas of endemism, distribution patterns and conservation status of the order Spirostreptida in Brazil (Diplopoda, Juliformia). Biodiversity and Conservation. doi:10.1007/s10531-023-02566-2.
https://doi.org/10.1007/s10531-023-02566...
).

Supplementary Material

The following online material is available for this article:

Supplementary Material 1

Acknowledgments

We thank Beatriz Mauricio (Laboratório de Biologia Celular of the Instituto Butantan) for her help with the SEM imaging, Carolina Rojas-Buffet for the S. joachimadisi vulvae photographs, and Nicoly Calcagniti and Leandro Lisardo for alerting us regarding the mass occurrence of S. araujoi and for sending us the specimens used in this study. Comments from Antonio Parra-Gomez and an anonymous reviewer improved the manuscript. This study was financially supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (grant to RSB; 88887.510007/2020-00). LFMI was supported by grant 162977/2020-4 from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and ADB by the grant CNPq (303028/2014-9) and by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP; 2022/12588-1). This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES - Finance Code 001).

Data Availability

The data used in this study are available at Biota Neotropica Dataverse

https://doi.org/10.48331/scielodata.W9CXON

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Edited by

Associate Editor
Gustavo Graciolli

Publication Dates

  • Publication in this collection
    09 Oct 2023
  • Date of issue
    2023

History

  • Received
    01 June 2023
  • Accepted
    03 Aug 2023
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