An extraordinary colonial spider community in Sulfur Cave (Albania/Greece) sustained by chemoautotrophy
- 1. Sapientia Hungarian University of Transylvania, Sfântu Gheorghe, Romania
- 2. University of Tirana, Tirana, Albania
- 3. Université libre de Bruxelles, Brussels, Belgium|University of Maastricht, Maastricht, Netherlands
- 4. Vrije Universiteit Brussel, Brussels, Belgium|Université libre de Bruxelles, Brussels, Belgium
- 5. University of Göttingen, Göttingen, Germany
- 6. "Grigore Antipa" National Museum of Natural History, Bucharest, Romania|Romanian Academy Cluj-Napoca Branch, Emil Racoviţă Institute of Speleology, Cluj-Napoca, Romania
- 7. Interuniversity Institute of Bioinformatics in Brussels - (IB)², Brussels, Belgium|Université libre de Bruxelles, Brussels, Belgium|Brussels Laboratory of the Universe - BLU, Brussels, Belgium
- 8. Romanian Academy Cluj-Napoca Branch, Emil Racoviţă Institute of Speleology, Cluj-Napoca, Romania
- 9. Gruppo Speleologico Archeologico Livornese of the Mediterranean Natural History Museum, Livorno, Italy
- 10. Emil Racoviţă Institute of Speleology, Biospeleology and Karst Edaphobiology Compartment, București, Romania|California State University, Chico, United States of America|Romanian Academy Cluj-Napoca Branch, Emil Racoviţă Institute of Speleology, Cluj-Napoca, Romania
- 11. Emil Racoviţă Institute of Speleology, Biospeleology and Karst Edaphobiology Compartment, București, Romania|Romanian Academy Cluj-Napoca Branch, Emil Racoviţă Institute of Speleology, Cluj-Napoca, Romania
Description
We report the discovery and detailed analysis of an extraordinary colonial spider assemblage in Sulfur Cave, a chemoautotrophic sulfidic ecosystem located on the Albania-Greece border. The colony, comprising an estimated 69,000 individuals of Tegenaria domestica (Agelenidae) and more than 42,000 of Prinerigone vagans (Linyphiidae), spans a surface area of over 100 m²—representing the first documented case of colonial web formation in these species. Stable isotope analyses (δ¹³C and δ¹⁵N) revealed that the trophic web sustaining this assemblage is fueled by in situ primary production from sulfur-oxidizing microbial biofilms then transferred through chironomid larvae and adults to higher trophic levels. Morphological and molecular data confirmed the identity of the two spider species and revealed that their populations in Sulfur Cave are genetically distinct from other populations. Regarding T. domestica, we found a seasonal pattern in fecundity, with significantly larger egg clutches in early summer. Microbiome analysis of this species also revealed a lower Shannon diversity in the cave population compared with a surface individual captured nearby. Our findings unveil a unique case of facultative coloniality in this cosmopolitan spider, likely driven by resource abundance in a chemoautotrophic cave, and provide new insights into the adaptation and trophic integration of surface species in sulfidic subterranean habitats.
Files
SB_article_162344.pdf
Files
(5.1 MB)
| Name | Size | Download all |
|---|---|---|
|
md5:1e09d23fb9d87342a0f497838b4b7ff9
|
5.1 MB | Preview Download |
System files
(168.1 kB)
| Name | Size | Download all |
|---|---|---|
|
md5:b4a4743f605dcf92f6ed8b13c443856d
|
168.1 kB | Download |
Linked records
Additional details
References
- Almeida-Silva LM, Brescovit AD, Dias SC (2009) A new species of Goeldia (Araneae: Titanoecidae) with notes on its natural history. Zoologia (Curitiba) 26: 363–368. https://doi.org/10.1590/S1984-46702009000200021
- Antić D, Turbanov IS (2022) An unexpected new cave-dwelling species of the genus Leucogeorgia Verhoeff, 1930 (Diplopoda: Julida: Julidae) from the Chechen Republic, Caucasus, Russia. Arthropoda Selecta 31: 375–383. https://doi.org/10.15298/arthsel.31.4.01
- Audy M, Bouda R, Bruthans J, Ružička V (2022) Albanian hypogene caves in the area of Vromoner thermal springs on the Sarandoporo River. Speleoforum 41: 41–51.
- Benassi A (2024) Lengarices 2023. Inseguendo il soffio del Drago (Albania), Speleologia SSI 89: 4–6.
- Bandelt HJ, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
- Barrett RDH, Hebert PDN (2005) Identifying spiders through DNA barcodes. Canadian Journal of Zoology 83: 481–491. https://doi.org/10.1139/z05-024
- Borko Š, Collette M, Brad T, Zakšek V, Flot J-F, Vaxevanopoulos M, Sarbu SM, Fišer C (2019) Amphipods in a Greek cave with sulphidic and non-sulphidic water: phylogenetically clustered and ecologically divergent. Systematics and Biodiversity 17: 558–572. https://doi.org/10.1080/14772000.2019.1670273
- Brad T, Iepure S, Sarbu SM (2021) The chemoautotrophically based Movile Cave groundwater ecosystem, a hotspot of subterranean biodiversity. Diversity 13: 128, https://doi.org/10.3390/d13030128
- Bristowe WS (1958) The World of Spiders. Collins New Naturalist, London, 304 pp.
- Chen Y, Wu L, Boden R, Hillebrand A, Kumaresan D, Moussard H, Baciu M, Lu Y, Colin Murrell J (2009) Life without light: microbial diversity and evidence of sulfur- and ammonium-based chemolithotrophy in Movile Cave. The ISME Journal 3: 1093–1104. https://doi.org/10.1038/ismej.2009.57
- Chervyatsova OY, Potapov SS, Kuzmina LY, Dublyansky YV, Sadykov SA, Kiseleva DV, Okuneva TG, Dzhabrailov S-EM, Samokhin GV (2020) Sulfuric acid speleogenesis in the North Caucasus: Sharo-Argun valley Caves (Chechen Republic, Russia). Geomorphology 369: 107346. https://doi.org/10.1016/j.geomorph.2020.107346
- Collard O, Tawfeeq MM, Ducret H, Flot J-F (2025) A rapid and inexpensive universal PCR protocol for DNA (meta)barcoding using a one-tube, 2-step PCR. bioRxiv: 2025.05.16.654411. https://doi.org/10.1101/2025.05.16.654411
- Curry KD, Wang Q, Nute MG, Tyshaieva A, Reeves E, Soriano S, Wu Q, Graeber E, Finzer P, Mendling W, Savidge T, Villapol S, Dilthey A, Treangen TJ (2022) Emu: species-level microbial community profiling of full-length 16S rRNA Oxford Nanopore sequencing data. Nature Methods 19: 845–853. https://doi.org/10.1038/s41592-022-01520-4
- Downes JA (1969) The swarming and mating flight of Diptera. Annual Reviews of Entomology 14: 271–298. https://doi.org/10.1146/annurev.en.14.010169.001415
- Deltshev C, Vrenozi B, Blagoev G, Lazarov S (2011) Spiders of Albania – faunistic and zoogeographical review (Arachnida: Araneae). Acta Zoologica Bulgarica 63(2): 125–144.
- Engel AS (2007) Observations on the biodiversity of sulfidic karst habitats. Journal of Cave and Karst Studies 69: 187–206.
- Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
- Flot J-F, Bauermeister J, Brad T, Hillebrand-Voiculescu A, Sarbu SM, Dattagupta S (2014) Niphargus-Thiothrix associations may be widespread in sulphidic groundwater ecosystems: evidence from southeastern Romania. Molecular Ecology 23: 1405–1417. https://doi.org/10.1111/mec.12461
- Hutchins BT, Engel AS, Nowlin WH, Schwartz BF (2016) Chemolithoautotrophy supports macroinvertebrate food webs and affects diversity and stability in groundwater communities. Ecology 97: 1530–1542. https://doi.org/10.1890/15-1129.1
- Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics 20: 1160–1166. https://doi.org/10.1093/bib/bbx108 [available online: https://mafft.cbrc.jp/align-ment/server/index.html, accessed on the 29th of March 2025]
- Kennedy SR, Tsau S, Gillespie R, Krehenwinkel H (2020) Are you what you eat? A highly transient and prey-influenced gut microbiome in the grey house spider Badumna longinqua. Molecular Ecology 29: 1001–1015. https://doi.org/10.1111/mec.15370
- Kovařík F, Audy M, Sarbu SM, Fet V (2023) , Euscorpius sulfur sp. n. (Scorpiones: Euscorpiidae), a new cave scorpion from Albania and northwestern Greece. Euscorpius 376: 1–14.
- Langel R, Dyckmans J (2014) Combined 13C and 15N isotope analysis on small samples using a near-conventional elemental analyzer/isotope ratio mass spectrometer setup. Rapid Communications in Mass Spectrometry 28: 1019–1022. https://doi.org/10.1002/rcm.6878
- Kumaresan D, Wischer D, Stephenson J, Hillebrand-Voiculescu A, Murrell JC (2014) Microbiology of Movile Cave - A chemolithoautotrophic ecosystem. Geomicrobiology Journal 31: 186–93. https://doi.org/10.1080/01490451.2013.839764
- Malek-Hosseini M, Brad T, Fatemi Y, Kuntner M, Fišer C (2023) A new cave-dwelling hadzioid amphipod (Senticaudata, Hadzioidea, Melitidae) from sulfidic groundwaters in Iran, Contributions to Zoology 93: 107–126. https://doi.org/10.1163/18759866-bja10054
- Mammola S, Isaia M (2017) Spiders in caves. Proceedings of the Royal Society B: Biological Sciences 284(1853): 20170193. https://doi.org/10.1098/rspb.2017.0193
- Mammola S, Cardoso P, Ribera C, Pavlek M, Isaia M (2018) A synthesis on cave-dwelling spiders in Europe. Journal of Zoological Systematics and Evolutionary Research 56(3): 301–316. https://doi.org/10.1111/jzs.12201
- Mammola S, Pavlek M, Huber BA, Isaia M, Ballarin F, Tolve M, Čupić I, Hesselberg T, Lunghi E, Mouron S, Graco-Roza C, Cardoso P (2022) A trait database and updated checklist for European subterranean spiders. Scientific Data 9: 236. https://doi.org/10.1038/s41597-022-01316-3
- Maraun M, Thomas T, Fast E, Treibert N, Caruso T, Schaefer I, Lu J-Z, Scheu S (2023) New perspectives on soil animal trophic ecology through the lens of C and N stable isotope ratios of oribatid mites. Soil Biology and Biochemistry 177: 108890. https://doi.org/10.1016/j.soilbio.2022.108890
- Nentwig W, Ansorg J, Cushing PE, Kranz-Baltensperger Y, Kropf C (2024) Funnel-web spiders (Agelenidae). In: Nentwig W, Ansorg J, Cushing PE, Kranz-Baltensperger Y, Kropf C (Eds) House Spiders - Worldwide. Springer Nature Switzerland, Cham, 45–53. https://doi.org/10.1007/978-3-031-70448-2_5
- Nentwig W, Blick T, Bosmans R, Hänggi A, Kropf C, Stäubli A (2025) Spiders of Europe, version 04.2025. [https://www.araneae.nmbe.ch accessed on 25 April 2025] https://doi.org/10.24436/1
- O'Leary NA, Wright MW, Brister JR, Ciufo S, Haddad D, McVeigh R, Rajput B, Robbertse B, Smith-White B, Ako-Adjei D, Astashyn A, Badretdin A, Bao Y, Blinkova O, Brover V, Chetvernin V, Choi J, Cox E, Ermolaeva O, Farrell CM, Goldfarb T, Gupta T, Haft D, Hatcher E, Hlavina W, Joardar VS, Kodali VK, Li W, Maglott D, Masterson P, McGarvey KM, Murphy MR, O'Neill K, Pujar S, Rangwala SH, Rausch D, Riddick LD, Schoch C, Shkeda A, Storz SS, Sun H, Thibaud-Nissen F, Tolstoy I, Tully RE, Vatsan AR, Wallin C, Webb D, Wu W, Landrum MJ, Kimchi A, Tatusova T, DiCuccio M, Kitts P, Murphy TD, Pruitt KD (2016) Reference sequence (RefSeq) database at NCBI: current status, taxonomic expansion, and functional annotation. Nucleic Acids Research 44: D733–D745. https://doi.org/10.1093/nar/gkv1189
- Peterson BJ, Fry B (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics, 18: 293–320. https://doi.org/10.1146/annurev.es.18.110187.001453
- Pollierer MM, Langel R, Scheu S, Maraun M (2009) Compartmentalization of the soil animal food web as indicated by dual analysis of stable isotopes (15N/14N and 13C/12C). Soil Biology and Biochemistry 41: 1221–1226. https://doi.org/10.1016/j.soilbio.2009.03.002
- Popa I, Brad T, Vaxevanopoulos M, Giurginca A, Baba Ș, Iepure S, Plăiașu R, Sarbu SM (2020) Rich and diverse subterranean invertebrate communities inhabiting Melissotrypa Cave in Central Greece. Travaux de l'Institut de Spéologie Émile Racovitza 58: 65–78.
- Por F, Dimentman C, Frumkin A, Naaman I (2013) Animal life in the chemoautotrophic ecosystem of the hypogenic groundwater cave of Ayyalon (Israel): A summing up. Natural Science 5: 7–13. https://doi.org/10.4236/ns.2013.54A002
- Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83: 703–718. https://doi.org/10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2
- Potapov AM, Tiunov AV, Scheu S (2019) Uncovering trophic positions and food resources of soil animals using bulk natural stable isotope composition. Biological Reviews 94: 37–59. https://doi.org/10.1111/brv.12434
- R Core Team (2024) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
- Ratnasingham S, Wei C, Chan D, Agda J, Agda J, Ballesteros-Mejia L, Boutou HA, El Bastami ZM, Ma E, Manjunath R, Rea D, Ho C, Telfer A, McKeowan J, Rahulan M, Steinke C, Dorsheimer J, Milton M, Hebert PDN (2024) BOLD v4: A centralized bioinformatics platform for DNA-based biodiversity data. In: DeSalle R (Ed.) DNA Barcoding: Methods and Protocols. Springer US, New York, NY, 403–441. https://doi.org/10.1007/978-1-0716-3581-0_26
- Reineking A, Langel R, Schikowski J (1993) 15N, 13C-On-line measurements with an elemental analyser (Carlo Erba, NA 1500), a modified trapping box and a gas isotope mass spectrometer (Finnigan, MAT 251). Isotopenpraxis Isotopes in Environmental and Health Studies 29: 169–174. https://doi.org/10.1080/10256019308046151
- Riesch R, Plath M, Schlupp I (2010) Toxic hydrogen sulfide and dark caves: life-history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae). Ecology 91: 1494–1505. https://doi.org/10.1890/09-1008.1
- Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA Sequence Polymorphism Analysis of Large Data Sets. Molecular Biology and Evolution 34: 3299–3302. https://doi.org/10.1093/molbev/msx248
- Rypstra AL (1979) Foraging flocks of spiders (a study of aggregate behaviour in Cyrtophora citricola in West Africa). Behavioral Ecology and Sociobiology 5: 291–300. https://doi.org/10.1007/BF00293677
- Sarbu SM (1990) The unusual fauna of a cave with thermomineral waters containing H2S from Southern Dobrogea, Romania. Mémoires de Biospéologie 17: 191–195.
- Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272: 1953–1955. https://doi.org/10.1126/science.272.5270.1953
- Sarbu SM, Galdenzi S, Menichetti M, Gentile G (2000) Geology and biology of the Frasassi caves in Central Italy: An ecological multi-disciplinary study of a hypogenic underground karst system. In: Wilkens H, Culver DC, Humphreys WF (Eds) Ecosystems of the world: Subterranean Ecosystems. Elsevier, 359–378.
- Sarbu SM, Brad T, Băncilă RI, Ştefan A (2024) Exploring biodiversity and food webs in Sulfur Cave in the Vromoner Canyon on the Greek-Albanian Border, Diversity 16: 477. https://doi.org/10.3390/d16080477
- Sayers EW, Bolton EE, Brister JR, Canese K, Chan J, Comeau DC, Connor R, Funk K, Kelly C, Kim S, Madej T, Marchler-Bauer A, Lanczycki C, Lathrop S, Lu Z, Thibaud-Nissen F, Murphy T, Phan L, Skripchenko Y, Tse T, Wang J, Williams R, Trawick BW, Pruitt KD, Sherry ST (2022) Database resources of the national center for biotechnology information. Nucleic Acids Research 50: D20–D26. https://doi.org/10.1093/nar/gkab1112
- Schmitt M (2004) Larinioides sclopetarius, eine parasoziale Spinne Mitteleuropas? Arachnologische Mitteilungen 27/28: 55–67. https://doi.org/10.5431/aramit2702
- Schoch CL, Ciufo S, Domrachev M, Hotton CL, Kannan S, Khovanskaya R, Leipe D, Mcveigh R, O'Neill K, Robbertse B, Sharma S, Soussov V, Sullivan JP, Sun L, Turner S, Karsch-Mizrachi I (2020) NCBI Taxonomy: a comprehensive update on curation, resources and tools. Database 2020: baaa062. https://doi.org/10.1093/database/baaa062
- Shannon CE (1948) A mathematical theory of communication. The Bell System Technical Journal 27: 379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
- Spöri Y, Flot J-F (2020) HaplowebMaker and CoMa: Two web tools to delimit species using haplowebs and conspecificity matrices. Methods in Ecology and Evolution 11: 1434–1438. https://doi.org/10.1111/2041-210X.13454
- Stoddard SF, Smith BJ, Hein R, Roller BRK, Schmidt TM (2015) rrnDB: improved tools for interpreting rRNA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Research 43: D593–D598. https://doi.org/10.1093/nar/gku1201
- Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biology Bulletin 34: 395–407. https://doi.org/10.1134/S1062359007040127
- Tobler M, Passow CN, Greenway R, Kelley JL, Shaw JH (2016) The evolutionary ecology of animals inhabiting hydrogen sulfide-rich environments. Annual Review of Ecology, Evolution, and Systematics 47: 239–262. https://doi.org/10.1146/annurev-ecolsys-121415-032418
- Trabalon M, Bautz AM, Moriniere M, Porcheron P (1992) Ovarian development and correlated changes in hemolymphatic ecdysteroid levels in two spiders, Coelotes terrestris and Tegenaria domestica (Araneae, Agelenidae). General and Comparative Endocrinology 88(1): 128–136. https://doi.org/10.1016/0016-6480(92)90201-T
- Uetz GW (1983) Sociable spiders. Natural History 92: 62–79.
- Uetz GW, Hodge MA (1990) Influence of habitat and prey availability on spatial organization and behavior of colonial web-building spiders. National Geographic Research 6: 22–40.
- Uetz GW, Hieber CS (1997) Colonial web-building spiders: balancing the costs and benefits of group-living. In: Crespi BJ, Choe JC (Eds) , The Evolution of Social Behaviour in Insects and Arachnids. Cambridge University Press, Cambridge, 458–475. https://doi.org/10.1017/CBO9780511721953.023
- Vierstraete AR, Braeckman BP (2022) Amplicon_sorter: A tool for reference-free amplicon sorting based on sequence similarity and for building consensus sequences. Ecology and Evolution 12: e8603. https://doi.org/10.1002/ece3.8603
- World Spider Catalog (2025) World Spider Catalog Version 26. Natural History Museum Bern. [online at http://wsc.nmbe.ch, accessed on 25 April 2025] https://doi.org/10.24436/2
- Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer International Publishing, Cham. https://doi.org/10.1007/978-3-319-24277-4
- Wickham H, François R, Henry L, Müller K, Vaughan D (2023) dplyr: a grammar of data manipulation. R package version 1.1.4. https://github.com/tidyverse/dplyr, https://dplyr.tidyverse.org
- Zhang J (2024) phylotools: phylogenetic tools for eco-phylogenetics. R package version 0.2.5. https://github.com/helixcn/phylotools