A case of mass occurrence of Sandalodesmus araujoi () in a municipality of São Paulo, Brazil and description of the heretofore unknown female (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, 1946), 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.

Full text

Biota Neotropica 23(3): e20231521, 2023
www.scielo.br/bn
ISSN 1676-0611 (online edition)
Article
https://doi.org/10.1590/1676-0611-BN-2023-1521 http://www.scielo.br/bn
A case of mass occurrence of Sandalodesmus araujoi (Schubart, 1946)
in a municipality of São Paulo, Brazil and description of the heretofore
unknown female (Polydesmida, Chelodesmidae)
Rodrigo S. Bouzan1,2* , Jackson C. Means3, Kaloyan Ivanov3, Giovanni B. Pupin1,
Antonio D. Brescovit1 & Luiz F. M. Iniesta1,4
1Instituto Butantan, Laboratório de Coleções Zoológicas, Av.Vital Brasil, 1500, Butantã, 05503-900,
São Paulo, SP, Brasil.
2Universidade de São Paulo, Instituto de Biociências, Pós-Graduação em Zoologia, R. Do Matão,
Butantã, 05508-090, São Paulo, SP, Brasil.
3Virginia Museum of Natural History, Department of Recent Invertebrates, 21 Starling Ave., 24112,
Martinsville, VA, United States of America.
4Universidade Federal do Maranhão, Coordenação do Curso de Licenciatura em Ciências Naturais/Codó, Av.
José Anselmo, 2008, 65400-000, Codó, MA, Brasil.
*Corresponding author: rodrigobouzan@outlook.com
BOUZAN, R.S., MEANS, J.C., IVANOV, K., PUPIN, G.B., BRESCOVIT, A.D., INIESTA, L.F.M. A
case of mass occurrence of Sandalodesmus araujoi (Schubart, 1946) in a municipality of São Paulo, Brazil
and description of the heretofore unknown female (Polydesmida, Chelodesmidae). Biota Neotropica 23(3):
e20231521. https://doi.org/10.1590/1676-0611-BN-2023-1521
Abstract: Somatic characters are shared by many Chelodesmidae groups, and generic placement and species
identications 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 classication. We
describe the heretofore unknown female of Sandalodesmus araujoi (Schubart, 1946), 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 rst 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-specic.
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 modications 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 inuenced its population dynamics.
Keywords: millipedes; Neotropics; population outbreak; Sandalodesmini; swarming; taxonomy.
Um caso de ocorrência em massa de Sandalodesmus araujoi (Schubart, 1946) em
um município de São Paulo, Brasil e descrição da fêmea até então desconhecida
(Polydesmida, Chelodesmidae)
Resumo: Os caracteres somáticos são compartilhados por muitos grupos de Chelodesmidae, e o posicionamento
genérico e as identicações 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 classicação mais robusta. Neste trabalho, descrevemos a até então desconhecida fêmea
de Sandalodesmus araujoi (Schubart, 1946), 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

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http://www.scielo.br/bn https://doi.org/10.1590/1676-0611-BN-2023-1521
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-especíca.
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 modicações 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 inuenciado 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) (Homan 1980, Shelley 2002, Brewer et al. 2012, Nguyen
and Sierwald 2013, Engho et al. 2015). 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 (Homan 1980). 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. 2021).
Based chiefly on gonopodal characters, Hoffman (1982)
proposed the tribe Sandalodesmini to include the South American
Oncoleptodesmus Schubart, 1958 and Sandalodesmus Silvestri, 1902.
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 modied, hook-like cannula (Homan
1982). Sandalodesmus diers 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 1902,
Schubart 1958, Homan 1982, Rojas-Buet et al. 2022]. 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 1931, 1938; Schubart
1958; Homan 1982; Rojas-Buet et al. 2022). Sandalodesmus was
reviewed by Homan (1982) and recently Rojas-Buet et al. (2022)
provided an updated key to the males.
Somatic characters are shared by many genera within the
Chelodesmidae and generic placement and species identication have
been traditionally based on gonopodal morphology (Homan 1971,
Pena-Barbosa et al. 2013, Bouzan et al. 2017a). Female genitalic
characters have been largely neglected, seldom examined, and rarely
photographed or illustrated (Brölemann 1902; Schubart 1946; Homan
1990a, 1990b, 2000; Pena-Barbosa et al. 2013; Bouzan et al. 2017b,
2018a, 2018b). 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
joachimadisi Rojas-Buet and Bouzan, 2022 have been described in
detail, including description of genitalic characters, and illustrated
(Rojas-Buet et al. 2022). This is rather unfortunate as the morphology
of the female genitalia presents important characters and may be decisive
for developing a more robust classication of the Chelodesmidae (see
Homan 2012).
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 2015, Niijima
et al. 2021). 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 1949, Niijima et al. 2021).
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 1949, Niijima et al. 2021). In
an attempt to provide a more robust classication of millipede mass
occurrences, Niijima et al. (2021) 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 1949). 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 1949). 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 1988, Niijima 1998, Niijima et al. 2021). Interestingly,
Parafontaria laminata armigera Verhoe, 1936 was recently shown
to have a lifecycle akin to periodical cicadas with an outbreak event
occurring every eight years (Niijima et al. 2021).
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)

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(Polydesmida, Paradoxosomatidae), and more recently the Portuguese
millipede, Ommatoiulus moreleti (Lucas, 1860) (Julida, Julidae) (Iniesta
et al. 2020, 2021, 2022). 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. 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 1942; Boock
and Lordello 1952; Lordello 1954; Boccardo et al. 1997, 2002). To
date, there have been no published accounts of swarming or population
outbreaks in the Chelodesmidae.
We report the rst case of a mass occurrence in the Chelodesmidae
and describe the heretofore unknown female of Sandalodesmus araujoi
(Schubart, 1946), 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 (ve specimens), S.
joachimadisi Rojas-Buet and Bouzan, 2022 (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 classication.
Distribution maps were generated using the freeware DIVA-GIS
ver. 7.5.0 (Hijmans et al. 2001).
Terminology of sexual and somatic characters follows Attems
(1898), Brölemann (1900), Pena-Barbosa et al. (2013), and Koch (2015).
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 identied
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.
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 2006). 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 2006, Alvares et al. 2014, Smith and Mayle
2017). 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. 1997).
Order Polydesmida Pocock, 1887
Family Chelodesmidae Cook, 1895
Subfamily Chelodesminae Cook, 1895
Tribe Sandalodesmini Homan, 1982
Genus Sandalodesmus Silvestri, 1902
Sandalodesmus araujoi (Schubart, 1946)
(Figures 1–17)
Leptodesmus araujoi Schubart 1946: 171, gure 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
1955: 516.
Leptodesmus (Gonioleptodesmus) araujoi:-- Schubart 1958: 29.
Gonioleptodesmus araujoi:-- Homan 1967: 34.
Sandalodesmus araujoi:-- Homan 1982: 251; Bouzan et al. 2018c:
11; Rojas-Buet et al. 2022: 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, 1944) (Schubart 1944, gures
22-23) and Sandalodesmus hippocampus (Schubart, 1944) (Schubart
1944, gures 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]), based on
the rounded, mesally curving acropodite (Figures 4A, C), which is
subtriangular and curving cephalad in S. salvadorii (Homan 1982,
Rojas-Buet et al. 2022).
Description. Male (new data; IBSP 14277): With characteristics
typical for the genus. Coloration in life: body rings dark brown,

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Biota Neotrop., 23(3): e20231521, 2023
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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.
Figure 2. A–D. Living specimens of S. araujoi from Pardinho, São Paulo, Brazil.

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Description of female of Sandalodesmus araujoi
Biota Neotrop., 23(3): e20231521, 2023
https://doi.org/10.1590/1676-0611-BN-2023-1521 http://www.scielo.br/bn
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).
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 modication. 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, attened, 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.
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.

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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.

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Description of female of Sandalodesmus araujoi
Biota Neotrop., 23(3): e20231521, 2023
https://doi.org/10.1590/1676-0611-BN-2023-1521 http://www.scielo.br/bn
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 dierence 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 prole 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).
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 1946).
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-Buet et al. 2022:
gure 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-specic. In addition, some characters, such as the asymmetric (to
dierent 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
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.

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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 modications 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. 2013). 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
inuenced 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 1985, Durigan et al.
2007). To date, approximately 50% of the Cerrado has been destroyed
by human activities (Rodriguez-Zorro et al. 2022), and only 10% of the
original vegetation of the Atlantic Forest remains (Colombo and Joly
2010, Joly et al. 2014, Rezende et al. 2018). 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. 2023).
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-Buet 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
Cientíco 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 nanced in
part by the Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior - Brasil (CAPES - Finance Code 001).
Associate Editor
Gustavo Graciolli
Author Contributions
Rodrigo Salvador Bouzan: formulated the idea; data collection;
manuscript preparation and revision.
Jackson C. Means: data collection; manuscript preparation and
revision.
Kaloyan Ivanov: data collection; manuscript preparation and
revision.
Giovanni B. Pupin: manuscript preparation and revision.
Antonio D. Brescovit: manuscript preparation and revision.
Luiz F. M. Iniesta: data collection; manuscript preparation and
revision.
Conicts of Interest
The authors declare that there is no conict of interest related to
the publication of this manuscript.
Data Availability
The data used in this study are available at Biota Neotropica
Dataverse
https://doi.org/10.48331/scielodata.W9CXON
References
ALVARES, C. A., J. Z. STAPE, P. C. SENTELGA, J. L. MORAES-
GONÇALVES, AND G. SPAROVEK. 2013. Köppen’s climate classication
map for Brazil. Meteorologische zeitschrift 22(6): 711–728.
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.
ATTEMS, C. M. T. GRAF VON. 1931. Die Familie Leptodesmidae und andere
Polydesmiden. Zoologica Stuttgart (79): 1–150.
ATTEMS, C. M. T. GRAF VON. 1938. Myriapoda 3. Polydesmoidea II. Fam.
Leptodesmidae, Platyrhachidae, Oxydesmidae, Gomphodesmidae. Das
Tierreich 69: 1–487.
BOCCARDO, L., R. JUCÁ-CHAGAS, AND C. H. S. PENTEADO. 2002.
Migration and Population Outbreaks of Millipedes in the Coee Plantations,
Region of Alto Paranaiba, MG, Brazil. Holos Environment 2(2): 220–223.
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.
BOOCK, O. J. AND L. G. E. LORDELLO. 1952. Diplópoda depredador
de tubérculos de batatinha. Bragantia12: 343–348. doi:10.1590/S0006-
87051952000400006.
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.
BOUZAN, R. S., J. P. P. PENA-BARBOSA, AND A. D. BRESCOVIT.
2017b. Taxonomic review of the genus Atlantodesmus Homan, 2000
(Polydesmida: Chelodesmidae). Zootaxa 4236(2): 269−290. doi:10.11646/
zootaxa.4236.2.3.
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.
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.

9
Description of female of Sandalodesmus araujoi
Biota Neotrop., 23(3): e20231521, 2023
https://doi.org/10.1590/1676-0611-BN-2023-1521 http://www.scielo.br/bn
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.
BOUZAN, R. S., L. F. M. INIESTA, AND A. D. BRESCOVIT. 2021. Cladistic
analysis and taxonomic review of the millipede tribe Arthrosolaenomeridini
Homan, 1976 (Polydesmida: Chelodesmidae). Zootaxa 4970(2): 201-256.
BREWER, M. S., P. SIERWALD, AND J. E. BOND. 2012. Millipede taxonomy
after 250 years: classication and taxonomic practices in a mega-diverse
yet understudied arthropod group. PLoS ONE 7(5): e37240. doi:10.1371/
journal.pone.0037240
BRÖLEMANN, H. W. 1900. Myriapodes d’Amérique. Mémoires de la Société
Zoologique de France 13: 89–131.
BRÖLEMANN, H. W. 1902. Myriapodes recueillis par M. E. Gounelle au Brésil.
Annales de la Société Entomologique de France 71: 649–694.
CLOUDSLEY-THOMPSON, J. L. 1949. The significance of migration
in myriapods. The Annals and Magazine of Natural History 12(2):
947–62.
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.
COUTINHO, L. M. 2006. O conceito de bioma. Acta Botanica Brasilica 20(1):
13–23. doi:10.1590/S0102-33062006000100002.
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.
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.
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.
FONSECA, G. A. B. 1985. The vanishing Brazilian Atlantic forest. Biological
Conservation 34: 17–34. doi:10.1016/0006-3207(85)90055-2.
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.
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.
HOFFMAN, R. L. 1971. Chelodesmid studies V. Some new, redened, and
resurrected Brazilian genera. Arquivos de Zoologia, São Paulo 20(4):
225–277. doi:10.11606/issn.2176-7793.v20i4p225-277.
HOFFMAN, R. L. 1980. Classication of the Diplopoda. Múseum d‘histoire
naturelle, Genève. 237 pp.
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.
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.
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.
HOFFMAN, R. L. 2000. A synopsis of the Telonychopodini, a tribe of
Pantanalian chelodesmid millepeds (Polydesmida: Chelodesmidae).
Myriapodologica 7(1): 1–13.
HOFFMAN, R. L. 2012. New genera for two poorly-known millipeds from
Bahia (Polydesmida: Chelodesmidae). Papeis Avulvsos de Zoologia 52(8):
103–110.
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.
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:10.1
080/00379271.2020.1834873.
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.
INIESTA, L. F. M., A. D. BRESCOVIT, D. G. A. JÚNIOR, AND R. S. BOUZAN.
2022. Into the New World: rst 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:10.1080/00
379271.2022.2084641.
JOLY, C. A., J. P. METZGER, M. TABARELLI. 2014. Experiences from the
Brazilian Atlantic Forest: ecological ndings and conservation initiatives.
New Phytologist 204: 459–473. doi:10.1111/nph.12989.
KOCH, M. 2015. General morphology. In: MINELLI, A. (Ed.) Treatise on Zoology
– Anatomy, Taxonomy, Biology. The Myriapoda. Brill, Leiden, 7–68.
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.
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.
NIIJIMA, K. 1998. Eects 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.
NIIJIMA, K. AND K. SHINOHARA. 1988. Outbreaks of the Parafontaria
laminata group (Diplopoda, Xystodesmidae). Journal of Ecology (Japan)
38: 257–268.
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.
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.
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.
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.
RODRÍGUEZ-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.

10
Bouzan R.S. et al.
Biota Neotrop., 23(3): e20231521, 2023
http://www.scielo.br/bn https://doi.org/10.1590/1676-0611-BN-2023-1521
ROJAS-BUFFET, C., R. S. BOUZAN, P. SIERWALD, A. D. BRESCOVIT, M.
SIMÓ. 2022. Sandalodesmus joachimadisi n. sp., the rst 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.
SCHUBART, O. 1942. Os Myriápodes e suas relações com a agricultura - Com
uma bibliograa completa sôbre o assunto. Papéis Avulsos do Departamento
de Zoologia 2(16): 205–234.
SCHUBART, O. 1944. Os Diplopodos de Pirassununga. Acta Zoologica Lilloana
2: 321–440.
SCHUBART, O. 1946. Contribuição ao conhecimento do gênero Leptodesmus
(Família Leptodesmidae, Diplopoda). Anais da Academia Brasileira de
Ciências 18: 165–202.
SCHUBART, O. 1955. Materiais para uma fauna do Estado de Sao Paulo - os
Leptodesmidae. Arquivos do Museu Nacional, Rio de Janeiro 42: 507–540.
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.
SHELLEY, R.M. 2002. A revised, annotated, family-level classication of the
Diplopoda. Arthropoda Selecta 11(3): 187–207.
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.
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.
Received: 01/06/2023
Accepted: 03/08/2023
Published online: 09/10/2023