Biodiversity Data Journal :
Species Conservation Profiles
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Corresponding author: Ana Sofia P. S. Reboleira (sofiareboleira@gmail.com)
Academic editor: Ivan H. Tuf
Received: 01 Aug 2023 | Accepted: 19 Sep 2023 | Published: 10 Nov 2023
© 2023 Ana Sofia P. S. Reboleira, Rita Eusébio
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Reboleira ASPS, Eusébio RP (2023) Cave-adapted millipedes from Portugal: species conservation profiles. Biodiversity Data Journal 11: e110382. https://doi.org/10.3897/BDJ.11.e110382
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Amongst the cave-dwelling millipedes (Diplopoda), there are several endemic species in Portugal with a very small geographical distribution. These species play an important role in the decomposition of organic matter in subterranean ecosystems and are vulnerable to disturbance from human activities, such as habitat destruction, pollution infiltrating from the surface and cave tourism.
We present the IUCN Red List profiles for cave-adapted millipedes (Diplopoda) from Portugal and propose conservation measures to prevent extinction. Overall, cave-adapted millipedes from Portugal represent an endemic part of the country's biodiversity and conservation efforts will help maintain the delicate ecological balance of subterranean ecosystems.
Diplopoda, subterranean habitats, cave habitat, troglobiont, cave conservation, Iberian Peninsula
Millipedes (Diplopoda) are key animals for biodiversity conservation, as they have limited dispersal capabilities and consequently exhibit high endemism patterns (
Portugal is a hotspot region for subterranean biodiversity and, despite a long tradition of studying different groups of subterranean arthropods, as crustaceans and beetles (
The recentlydescribed endemic millipede species face tremendous conservation challenges. Therefore, we created the IUCN Red List profile for cave millipedes from Portugal. This information aims to aid decisions about land-use at surface and territory planning and management.
During the last two decades, many millipedes from caves of Portugal have been sampled. All these specimens were studied and identified to species level, which included dissection, optical and scanning electronic microscopy study and comparison with other specimens and bibliography (
Both the extent of occurrence (EOO) and area of occupancy (AOO) were computed with the Geospatial Conservation Assessment Tool (GeoCAT) using an approximation to the IUCN standard 2 km × 2 km cells (4 km2). Software QGIS 3.14.16 was used to produce all maps, using the layer of natural protected areas of Portugal (
Animals were photographed either alive in situ with a Cannon 6D mark II or preserved in alcohol with a stereomicroscope Leica DFC 420; images were processed with the Leica Application Suite, Zerene Stacker and background was cleaned in Adobe Photoshop CS5.
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Callipodida | Dorypetalidae |
Basionym: Lysiopetalum alternans Verhoeff, 1893.
Lusitanipus alternans and its congener L. xanin Gilgado, 2020 have similar gonopods, differing only in other variable characters. "Lusitanipus xanin sp. nov. differs from L. alternans in its green colour, the higher number of body rings, the shape of the gonocoxite and the curvature and shape of the processes of the tip of telopodites of gonopods" (in
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The extent of occurrence (EOO) is 2470 km2 and area of occupancy (AOO) is 32 km2.
Lusitanipus alternans is recorded from eight localities: in d’el Rey, Soprador do Carvalho, Arrifana, Cerâmica, Corujeiras, Fonte Grande and Buraco da Moura caves and in the mesovoid shallow substratum from Poios Valley in Sicó karst massif (
A decline in EOO is inferred because of the anthropogenic impact in the Soprador do Carvalho and Buraco da Moura caves. These caves show degradation signs, caused by the recreational visitation activities.
A decline in AOO is inferred due to the vulnerability of two of the caves.
Lusitanipus alternans occurs in eight locations in subterranean habitats, caves and mesovoid shallow substrate, in central Portugal (
In caves, it is more abundant in d’el Rey Cave in Outil-Cantanhede karst area. It is also quite abundant in some caves of Sicó-Condeixa and Alvaiázere karst chains, such as Soprador do Carvalho, Arrifana, Corujeiras I and Fonte Grande caves, while in Cerâmica Cave, only juveniles have been collected (
Lusitanipus alternans is known from subterranean habitats. It lives in temperatures ranging from 12ºC in Buraco da Moura Cave up to 16.4ºC in Cerâmica Cave (
Lusitanipus alternans is considered a troglophile species, i.e. a species whose presence is frequent in caves, but does not show specific adaptative morphologic traits to the subterranean lifestyle (
D‘el Rey Cave is located in an urbanised area, 600 m from a landfill, 1 km from a quarry and 1.2 km from highway A14. Arrifana Cave is located 190 m from a road, 370 m from the nearest village and 900 m from a quarry. Cerâmica Cave is surrounded by Eucalyptus intensive plantations and is located 270 m from a road, 550 m from an animal farm, 1.6 km from the closest village and 3.6 km from a quarry. Soprador do Carvalho Cave is surrounded by agricultural lands and is located 67 m from the closest house and 1.4 km from a quarry. This is a touristic cave, severely affected by anthropogenic activities (
Of the eight locations, only three are inside the “Rede Natura 2000” areas (
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Chordeumatida | Opisthocheiridae |
This species is included in a monospecific genus and is distinguishable from other opisthocheirids due to the “anterior male gonopods with a distinct small anterior synangiocoxite and separate, two-segmented colpocoxites enfolded by biramous, very large telepodites; posterior gonopods two-segmented, without processes; first pair of postgonopodal legs (P10) with a set of three strong setae next to coxal gland openings; vulvae without a postvulvar organ” (
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Both the extent of occurrence (EOO) and area of occupancy (AOO) are 4 km2.
Sireuma nobile is known only from a single cave, the Algar de Santo António in the Estremoz-Cano karst massif (
Sireuma nobile occurs in a single cave (
Algar de Santo António is the only known location for this species. Therefore, the trend in number of locations is stable.
Fifteen specimens have been collected from the type location (
Algar de Santo António Cave is composed of two entrances that connect at the base of the first pit and it has a a maximum depth of -52 m, currently ending in rubble blocks. Sireuma nobile specimens were collected at -20 and -52 m. Inside the cave, humidity levels reach 100% and temperature ranges from 17.7ºC up to 18.9ºC at the soil level (
Sireuma nobile is a troglobiont species, depigmented and anophthalmic (
Algar de Santo António Cave is located in the middle of an urbanised area of a village, under a building and right by a road. It has a building on top of the main entrance and its distance is 27 m from the nearest house. The location is surrounded by agricultural fields. There is a massive quarry located 3 km from the cave entrance, where stone is extracted and prepared in slabs for retail.
This cave is located out of the “Rede Natura 2000” areas (
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Chordeumatida | Chamaesomatidae |
Scutogona minor adults differ from other species in the same genus due to having 29 pleurotergites, a densely pilose head, a tridentate labrum and strongly protruding subglobular mandibular stipites (
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The extent of occurrence (EOO) is 25896 km2 and the area of occupancy (AOO) is 12 km2.
Scutogona minor is known from three caves located in the Sicó karst massif, in central Portugal: Santa Maria da Estrela, Cerâmica and Arrifana caves (
Scutogona minor occurs in three locations, three caves within the Sicó karst area (
It was found in higher numbers in Arrifana Cave, in the winter season, followed by Santa Maria da Estrela Cave (
The maximum distance of the known distribution is of 18 km between the three caves. Specimens were only collected in the deepest parts of the caves and they were collected live through active search. All caves have high humidity levels (up to 100%) and at soil level, temperature ranged from 15.3ºC to 16.4ºC (
Scutogona minor is the smallest species of its genus. It is a troglobiont species, depigmented, lacks eyes and is endemic from caves in the Sicó massif (
Arrifana Cave is located 190 m from a road, 370 m from the nearest village and 900 m from a quarry. Cerâmica Cave is surrounded by Eucalyptus intensive plantations and is located 270 m from a road, 550 m from an animal farm, 1.6 km from the closest village and 3.6 km from a quarry. Santa Maria da Estrela Cave is located 80 m from a road, 86 m from a touristic site, 220 m from agricultural fields, 230 m from the Nossa Senhora da Estrela viewpoint, 250 m from the closest urbanised area and 2.6 km from two quarries. All caves have geocaches inside, which means that their entrances are frequently visited by geocachers.
This species has a very reduced distribution, confined to three caves in the Sicó Karst Massif and face several threats. It is important to define an undisturbed surface area to ensure that no contaminants, such as pesticides from agriculture and effluents from farms do not infiltrate and impact these populations. Geocaches should be removed from the caves to prevent their use by tourists. Biological prospection in other caves within the area of distribution have the potential to expand the currently-known populations of Scutogona minor.
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Polydesmida | Paradoxosomatidae |
Distinguishable from other Boreviulisoma species by being depigmented, by “having femoral knobs on male legs 3–7 and 9–10” and by “having a hawksbill-like process on the dorsal side of the gonopod tip” (
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Both the extent of occurrence (EOO) and area of occupancy (AOO) are 4 km2.
Boreviulisoma barrocalense occurs in Vale Telheiro Cave, in the Algarve karst massif, southern Portugal (
Boreviulisoma barrocalense occurs in one location (
Vale Telheiro Cave is the only known location for this species. Therefore, the trend in number of locations is stable.
Five specimens have been collected from the type locality (
Vale Telheiro Cave, is currently the most biodiverse cave in terms of troglobiont species in Portugal (Reboleira & Enghoff 2013), accounting now for more than 25 species, which turns it into a world hotspot for subterranean biodiversity. It has high humidity levels and very stable environment conditions (Reboleira et al. 2017), as well as reduced levels of oxygen in its deeper parts.
Boreviulisoma barrocalense is a troglobiont species (
Vale Telheiro is located 290 m from the closest house and 745 m from the closest urbanisation. The immediate surface of the cave has recently been subject to landfills and the closest road has been enlarged and tarred, facilitating the access to the cave area.
Vale Telheiro Cave, where these single cave endemics occur must be protected. As the terrain where the cave is located was acquired by the Loulé Town Hall in order to establish a protected area, it is possible to foresee more conservation efforts in the near future. The surface area should be maintained with its natural vegetation cover and cave visitation should be limited. Efforts should be made to understand the spacio-temporal dynamics and life cycle of this species, also the population trends should to be monitored. This species, together with the cave-adapted millipede Acipes machadoi, inhabits the richest cave for troglobiont species in Portugal and protecting this species implies the protection this important habitat.
Kingdom | Phylum | Class | Order | Family |
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Animalia | Animalia | Diplopoda | Julida | Julidae |
Distinguishable from all other species of the Cylindroiulus madeirae-group by the hook-shaped and higher than promerite gonopod mesomerite (
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Both the extent of occurrence (EOO) and area of occupancy (AOO) are 4 km2.
Cylindroiulus julesvernei is endemic from São Vicente Cave, in the Madeira Archipelago (
A decline in EOO is inferred due to the anthropogenic impact on the cave, as the visitors directly trample on the cave substrate.
The decline of AOO is inferred due to current threats to the habitat.
Cylindroiulus julesvernei occurs in one location (
São Vicente Cave is the only known location for this species. Therefore, the trend in number of locations is stable.
All three known specimens have been collected from the type locality (
São Vicente Cave is a lava tube, formed 890 thousand years ago after a volcanic eruption at Paul da Serra (
This species is a troglobiont species, blind and depigmented (
This is a show cave, opened since 1996 to the public and can be visited by tourists through a route of 700 m. The cave has artificial light and, as a consequence, lampenflora proliferate around the light sources. This cave is located at the centre of an urbanised area, close to roads.
This cave is a show cave and is not protected under legislation by the “Rede Natura 2000” (
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Julida | Julidae |
Distinguished from all species of the Cylindroiulus madeirae-group, except Cylindroiulus julesvernei Reboleira & Enghoff, 2014, by depigmented body and lack of eyes. It is also distinguished from C. julesvernei by having the mesomere not hooked (male gonopod) (
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Both the extent of occurrence (EOO) and area of occupancy (AOO) are approximately 4 km2.
Cylindroiulus oromii occurs in Landeiros Cave, in the Madeira Archipelago (
Cylindroiulus oromii occurs in one location (
Landeiros Cave is the only known location for this species. Therefore, the trend in number of locations is stable.
All known specimens have been collected from the type locality (
Landeiros Cave is a lava tube, located within the volcanic complex of São Roque/Paúl (SRP), in the Santo da Serra lava flow. The mean temperature inside the cave is 16ºC to 17ºC (
C. oromii is bilnd and depigmented and shares habitat with the troglobiont carabid beetle Thalassophilus pieperi Erber, 1990 and several troglophile species, like the snail Oxychilus draparnaudi (Beck, 1837), the mites Veigaia uncata Farrier, 1957 and Uroseius acuminatus (Koch, 1847), the spider Steatoda grossa (Koch, 1838), the terrestrial isopod Soteriscus sp., the centipede Lithobius sp., two species of springtails from the genus Onychiurus Gervais, 1841, the carabid beetle Trechus fulvus Dejean, 1831 and several Phoridae and Psychodidae dipterans (
Landeiros Cave is located below agricultural terrains and right by urbanised areas and roads, in the island of Madeira.
The only known locality for this species is a non-protected cave; therefore, C. oromii is a single cave endemic living in a Darwinian island. The cave and its respective surface should be priority targets for conservation, in order to prevent infiltration from pesticides and insecticides used in agriculture. More research is needed to understand the life cycle of this species.
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Julida | Julidae |
Distinguishable from other species of the Cylindroiulus perforatus-group by being blind and by “the shape of the gonopod mesomerite, which is shorter than the promerite and apically rounded” (
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Both the extent of occurrence (EOO) and area of occupancy (AOO) are 4 km2.
Cylindroiulus villumi occurs in the Algar do Pena Cave, located in the Santo António Plateau, the central sub-unit of the Estremenho karst massif (
Cylindroiulus villumi occurs in a single cave (
This species only occurs in Algar do Pena Cave; therefore, the trend in number of locations is stable.
Eleven specimens have been collected from the type locality (
This species was collected from the largest underground chamber of Portugal, where relative humidity close is up to saturation and temperature is very constant at 13ºC (with a variation of ± 1ºC). Specimens were collected inside a piece of decaying wood, at the base of the entrance pit of the cave, 33 m depth (
Cylindroiulus villumi is a small to medium-sized blind and depigmented millipede species. Both the holotype and a juvenile male paratype had fungi present on the head and antenna (
Algar do Pena is located 300 m from a quarry, where intense quarry activity is currently ongoing, being a source of residues' infiltration and uncontrolled dust release.
The habitat of this single cave endemism is inside the Serra de Aire e Candeeiros; however, the species lacks protection status. Measures need to be taken in order to prevent the infiltration of residues from the nearby quarries into the cave. The cave hosts a laboratory for research and has a stainless steel platform that allows touristic visits. Measures to prevent contamination of the cave are already in place (
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Julida | Blaniulidae |
Distinguishable from the other two known blind species, Acipes andalusius Enghoff & Mauriès, 1999 and Acipes bifilum Enghoff & Reboleira, 2013, by its larger body, less modified first pair of legs in males and by its smooth, rounded apical flange and a very long filamentous tip of the posterior gonopod (
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Both the extent of occurrence (EOO) and area of occupancy (AOO) are 4 km2.
Acipes machadoi occurs in Vale Telheiro Cave, in the Algarve karst massif, southern Portugal (
Acipes machadoi occurs in one location (
Vale Telheiro Cave is the only known location for this species. Therefore, the trend in number of locations is stable.
Only one specimen has been collected from the type locality (
Acipes machadoi was collected on the walls of the cave, in the area where roots were hanging from the ceiling. In this cave, humidity levels reach 100% and temperature varies 1ºC throughout the year, with an average of 17.4ºC (
Acipes machadoi is a blind and depigmented troglobiont millipede and it is a detritivore species, occupying a basal position in the cave's trophic chain (
Vale Telheiro is located 290 m from the closest house and 745 m from the closest urbanisation. The immediate surface of the cave has recently been subject to landfills and the closest road has been enlarged and tarred, facilitating the access to the cave area.
As the terrain where the cave is located was acquired by the Loulé Town Hall in order to establish a protected area, it is possible to foresee more conservation efforts in the near future. The surface area should be maintained with its natural vegetation cover and cave visitation should be limited. More knowledge on the biology of this species is needed. This species inhabits the richest cave for troglobiont species in Portugal, protecting this species implies the protection this important habitat.
Kingdom | Phylum | Class | Order | Family |
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Animalia | Arthropoda | Diplopoda | Julida | Blaniulidae |
Distinguishable from the other two known blind Acipes by the shape of the posterior gonopod which is “curved in the sagittal plane, apically divided into two thread-like structures, one of which corresponds to the apical flange, the other to the filamentous tip” (
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Both the extent of occurrence (EOO) and area of occupancy (AOO) are 4 km2.
Acipes bifilum occurs in Senhora Cave, in the Algarve karst massif (
Acipes bifilum is known from one single cave location (
Senhora Cave is the only known location for this species. Therefore, the trend in number of locations is stable.
Two specimens have been collected from the type locality, despite recurrent sampling efforts, no further specimens have been observed since its description.
Senhora Cave is located in the Cerro da Cabeça Mountain in Moncarapacho, Algarve, the southernmost province of Portugal. Acipes bifilum was collected on the cave soil, where humidity levels range between 98 and 100% and has an average temperature of 17.7ºC (
Acipes bifilum is a blind and depigmented troglobiont millipede (
Senhora Cave is located 168 m from the closest house and 900 m from an intensive agricultural complex, where strawberries and raspberries are mass-produced. It was subject to profound changes in a failed attempt to transform it into a show cave in the past century, metal and concrete are now in the vertical opening of the cave. This entrance is also used to dump garbage.
The only locality known for this species, the Senhora Cave, is not protected and this single cave endemic millipede lacks protection status.
Eight troglobiont species (orders Chordeumatida, Polydesmida and Julida) and one troglophile species (order Callipodida) are known from Portugal. Six troglobiont and one troglophile species occur on the Portuguese mainland and two troglobiont on the Atlantic Island of Madeira. There are no records of cave-dwelling millipede species on the Azores Archipelago (
Cave-adapted millipedes from Portugal are confined to very limited geographical distributions and ecological features of their subterranean compartments, such as high humidity and lack of light. These troglobiont millipedes ocuppy a basal position in the trophic chains of caves, they are detritivores, which means they feed on decaying organic matter like leaf litter, plant debris and decaying animal remains and excrement (
The order Julida is the most well represented, with three Cylindroiulus species (Julidae), one from the Estremenho karst massif (central continental Portugal), two from Madeira Island and two Acipes species (Blaniulidae) from the Algarve karst massif (southern continental Portugal) (
The callipodid Lusitanipus alternans is endemic to central Portugal and, despite being a troglophile species, has only been sampled in caves and in the mesovoid shallow substratum, where it establishes stable populations and has its complete life cycle (
Except Scutogona minor, which is found in several caves in the Sicó karst massif, all other troglobiont species of millipedes from continental Portugal are single cave endemics, which entails a great challenge for conservation (
All cave-adapted millipedes from Portugal face ongoing threats related to land-use at surface, pollution infiltration, cave disturbance by visitation and mining and climate change. As for other troglobiont species in Portugal, there is an urgent need to improve the knowledge about population sizes and spacio-temporal dynamics and to understand the limits of their subterranean distribution (
Protection measures for cave-adapted millipedes in Portugal should include the delimitation of safety areas for conservation perimeters at the surface to avoid infiltration of contaminants, the preservation of natural vegetation at surface to ensure proper nutrient flow towards the underground and to limit the visitation to the caves (
All specimens were collected under permits of the Instituto de Conservação da Natureza e das Florestas. This work was supported by the VILLUM FONDEN (research grant 15471) and by Portuguese National Funds through “Fundação para a Ciência e a Tecnologia” (FCT) within the cE3c Unit funding UIDB/00329/2020 and PhD grant (2021.04868.BD). We are grateful to reviewers Sergei Golovatch and Dragan Antić for suggestions that improved the manuscript.
This work was supported by the VILLUM FONDEN (research grant 15471) and by Portuguese National Funds through “Fundação para a Ciência e a Tecnologia” (FCT) within the cE3c Unit funding UIDB/00329/2020 and PhD grant (2021.04868.BD).
(A) Distribution of cave-adapted millipedes in continental Portugal; (B) Distribution of cave-adapted millipedes in Madeira Island, Portugal.
Species: Lusitanipus alternans (pink circle), Sireuma nobile (green diamond), Scutogona minor (blue cross), Boreviulisoma barrocalense (yellow triangle), Cylindroiulus julesvernei (light purple hexagon), Cylindroiulus oromii (dark purple hexagon), Cylindroiulus villumi (blue hexagon), Acipes machadoi (red square), Acipes bifilum (orange square).
Lusitanipus alternans distribution: d'el Rey, Arrifana, Cerâmica, Soprador do Carvalho, Corujeiras, Fonte Grande and Buraco da Moura caves and Vale do Poio mesovoid shallow substratum.
Sireuma nobile distribution: Algar de Santo António, Estremoz-Cano karst massif.
Scutogona minor distribution: Santa Maria da Estrela, Cerâmica and Arrifana caves, Sicó karst massif.
Boreviulisoma barrocalense distribution: Vale Telheiro Cave, Algarve karst massif.
Cylindroiulus julesverne distribution: São Vicente Cave, Madeira Archipelago.
Cylindroiulus oromii distribution: Landeiros Cave, Madeira Archipelago.
Cylindroiulus villumi distribution: Algar do Pena Cave, Estremenho karst massif.
Acipes machadoi distribution: Vale Telheiro Cave, Algarve karst massif.
Acipes bifilum distribution: Senhora Cave, Algarve karst massif.