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Malpighian tubules in harvestmen

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Abstract

In arachnids, the Malpighian tubules (MTs), coxal glands and stercoral pockets are capable of collecting and removing excreta from the body. The presence of the MTs among Opiliones was evidenced for the first time in Amilenus aurantiacus in 2015. Individuals undergo a winter diapause subterranean habitats. Here, we provided the morphological and cytological description of the MTs and asked whether their structure and ultrastructure change during the winter diapause. We studied the changes using light and transmission electron microscopy. The MTs consisted of the ureter and a pair of long, lateral blind-ended tubules, forming a long loop in the opisthosoma, and a coiled, terminal ball in the prosoma. The MTs were uniform, composed of a single-cell type, a monolayer of cuboidal epithelial cells, and the basal lamina. The cell ultrastructure was quite comparable to those in other arthropods, except for very long infoldings of the basal membrane protruding close to the nucleus. Except for spherite exploitation, no changes were observed in the ultrastructure of the MT epithelial cells during overwintering. We suggest that the analogous MTs in A. aurantiacus, and the nephron anatomies, along with a single-cell-type MT epithelium, might be of advantage in modelled studies of the nephron.

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References

  • Baker GT, Krantz GW (1985) Structure of the male and female reproductive and digestive systems of Rhizoglyphus robini Claparède (Acari, Acaridae). Acarologia 26:55–65

    Google Scholar 

  • Berridge MJ, Oshman JL (1972) A structural basis for fluid secretion by Malpighian tubules. Tissue Cell 1:247–272

    Article  Google Scholar 

  • Besenhofer LM, McLaren MC, Latimer B, Bartels M, Filary MJ, Perala AW, McMartin KE (2011) Role of tissue metabolite accumulation in the renal toxicity of diethylene glycol. Toxicol Sci 123:374–383. https://doi.org/10.1093/toxsci/kfr197

    Article  CAS  PubMed  Google Scholar 

  • Beyenbach KW, Skaer H, Dow JAT (2010) The development, molecular, and transport biology of Malpighian tubules. Annu Rev Entomol 55:351–374. https://doi.org/10.1146/annurev-ento-112408-085512

    Article  CAS  PubMed  Google Scholar 

  • Bourne, J.D., 1978a. Données préliminaires sur l’écologie et la biologie de l’opilion trogloxène Amilenus aurantiacus (Simon). Actes 6e Congrès Suisse de Spéléologie. Porrentruy, 17−24.

  • Bourne JD (1978b) Observations préliminaires sur l’intestin de l’opilion trogloxène Amilenus aurantiacus (Simon) pendant son sejour souterrain. Mém. Biospéol. 8:39–42

    Google Scholar 

  • Bradley TJ (1985) The excretory system: structure and physiology. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology, biochemistry and pharmacology. Pergamon Press, New York, pp 421–465

    Google Scholar 

  • Bradley TJ (2008) Active transport in insect recta. J Exp Biol 211:835–836. https://doi.org/10.1242/jeb.009589

    Article  PubMed  Google Scholar 

  • Bradley TJ (2009) Excretion. In: Resh VH, Carde RT (eds) Encyclopedia of insects, 2nd edn. Academic Press, San Diego, pp 334–339

    Chapter  Google Scholar 

  • Chapman RF (2008) The insects: structure and function. Cambridge University Press, New York, pp 478–508

    Google Scholar 

  • Chen YH, Liu HP, Chen HY, Tsai FJ, Chang CH, Lee YJ, Lin WY, Chen WC (2011) Ethylene glycol induces calcium oxalate crystal deposition in Malpighian tubules: a Drosophila model for nephrolithiasis/urolithiasis. Kidney Int 80:369–377. https://doi.org/10.1038/ki.2011.80

    Article  CAS  PubMed  Google Scholar 

  • Chen WC, Lin WY, Chen HY, Chang CH, Tsai FJ, Man KM, Shen JL, Chen YH (2012) Melamine-induced urolithiasis in a Drosophila model. J Agric Food Chem 60:2753–2757. https://doi.org/10.1021/jf204647p

    Article  CAS  PubMed  Google Scholar 

  • Cohen E, Sawyer JK, Peterson NG, Dow JAT, Fox DT (2020) Physiology, development, and disease modeling in the Drosophila excretory system. Genetics 214:235–264

    Article  CAS  Google Scholar 

  • Dow JAT (2009) Insights into the Malpighian tubule from functional genomics. J Exp Biol 212:435–445

    Article  CAS  Google Scholar 

  • Foelix RF (1996) Biology of spiders. In: Oxford University Press, G. Thieme Verlag, New York, Oxford

    Google Scholar 

  • Furtado WCA, Azevedo DO, Martins GF, Zanuncio JC (2013) Histochemistry and ultrastructure of urocytes in the pupae of the stingless bee Melipona quadrifasciata (Hymenoptera: Meliponini). Microsc Microanal 19:1502–1510

    Article  CAS  Google Scholar 

  • Gillott, C., 2005. Entomology: The Third Edition. Springer, Netherlands.

  • Giribet G, Edgecombe GD (2019) The phylogeny and evolutionary history of arthropods. Curr Biol 29:592–602. https://doi.org/10.1016/j.cub.2019.04.057

    Article  CAS  Google Scholar 

  • Green LBS (1979) The fine structure of the light organ of the New Zealand glow-worm Arachnocampa luminosa (Diptera: Mycetophilidae). Tissue Cell 11:457–465

    Article  CAS  Google Scholar 

  • Hazelton SR, Felgenhauer BE, Spring JH (2001) Ultrastructural changes in the Malpighian tubules of the house cricket, Acheta domesticus, at the onset of diuresis: a time study. J Morphol 247:80–92. https://doi.org/10.5038/1827-806X.41.2.5

    Article  CAS  PubMed  Google Scholar 

  • Jequier J-P (1964) Étude écologique et statistique de la faune terrestre d’une caverne du Jura Suisse au cours d’une année d’observations. Rev Suisse Zool 71:13–370

    Article  Google Scholar 

  • Kaestner A (1969) Lehrbuch der Spezielen Zoologie. In: I: Wirbellose. Jena, Gustav Fischer Verlag, 898 pp

    Google Scholar 

  • Kalender Y, Kalender S, Candan S (2002) Fine structure of Malpighian tubules in the Agrotis segetum (Lepidoptera: Noctuidae) pupae. Acta Zool Bulg 54:87–96

    Google Scholar 

  • Köhler H-R, Alberti G (1992) The effect of heavy metal stress on the intestine of Diplopods. Berichte des natur-medizinishes Vereins Innsbruck. Suppl 10:257–267

    Google Scholar 

  • Landry GM, Hirata T, Anderson JB, Cabrero P, Gallo CJ et al (2016) Sulfate and thiosulfate inhibit oxalate transport via a dPrestin (Slc26a6)-dependent mechanism in an insect model of calcium oxalate nephrolithiasis. Am J Physiol Ren Physiol 310:152–159. https://doi.org/10.1152/ajprenal.00406.2015

    Article  CAS  Google Scholar 

  • Lipovšek S, Letofsky-Pabst I, Novak T, Hofer F, Pabst MA (2009) Structure of the Malpighian tubule cells and annual changes in the structure and chemical composition of their spherites in the cave cricket Troglophilus neglectus Krauss, 1878 (Rhaphidophoridae, Saltatoria). Arthropod Struct. Dev. 38:315–327. https://doi.org/10.1016/j.asd.2009.02.001

    Article  CAS  Google Scholar 

  • Lipovšek S, Novak T, Janžekovič, Leitinger G (2015) Changes in the midgut diverticula in the harvestmen Amilenus aurantiacus (Phalangiidae, Opiliones) during winter diapause. Arthropod Struct Dev 44:131–141. https://doi.org/10.1016/j.asd.2014.12.002

    Article  PubMed  Google Scholar 

  • Lipovšek S, Novak T, Janžekovič F, Weiland N, Leitinger G (2016) Malpighian tubule cells in overwintering cave crickets Troglophilus cavicola (Kollar, 1833) and T. neglectus Krauss, 1879 (Rhaphidophoridae, Ensifera). PLoS One 11(7):e0158598

    Article  Google Scholar 

  • Lipovšek S, Janžekovič F, Novak T (2017) Ultrastructure of fat body cells and Malpighian tubule cells in overwintering Scolyopterix libatrix (Noctuoidea). Protoplasma 254:2189–2199. https://doi.org/10.1007/s00709-017-1110-3

    Article  PubMed  Google Scholar 

  • Martens J (1969) Systematische Stellung von Amilenus aurantiacus (Simon) (Opiliones, Phalangiidae). Senckenberg Biol 50(3/4):219–224

    Google Scholar 

  • Martens J (1978) Weberknechte, Opiliones. In: Die Tierwelt Deutschlands 64. Fischer, Verlag

    Google Scholar 

  • Martoja R, Ballan-Dufrançais C (1984) The ultrastructure of the digestive and excretory organs. In: King RC, Akai H (eds) Insect ultrastructure. Plenum, New York, pp 199–268

    Chapter  Google Scholar 

  • Mello ML (1979) A mucous secretion in the Malpighian tubes of a neotropical bumblebee, Bombus atratus Franklin. Protoplasma 99:147–158

    Article  Google Scholar 

  • Mello ML, Kerr WE (1984) Histochemistry of salivary gland and Malpighian tubule secretions contributing to the cocoon in Plebeia droryana and Scaptotrigona postica (Hym., Apoidea). Zool Anz 213:177–189

    Google Scholar 

  • Nocelli RCF, Cintra-Socolowski P, Roat TC, Silva-Zacari ECM, Malaspina O (2016) Comparative physiology of Malpighian tubules: form and function. Open Access Insect Physiol 6:13–23. https://doi.org/10.2147/OAIP.S72060

    Article  Google Scholar 

  • Novak T, Gruber J, Slana L (1984) Remarks on Opiliones from cavities in Slovenia (Yugoslavia). Mém Biospéol 11:185–197

    Google Scholar 

  • Novak T, Perc M, Lipovšek S, Janžekovič F (2012) Duality of terrestrial subterranean fauna. Int J Speleol 41(2):181–188

    Article  Google Scholar 

  • Novak T, Janžekovič F, Lipovšek S (2013) Contribution of non-troglobiotic terrestrial invertebrates to carbon input in hypogean habitats. Acta Carsologica 42(2-3):301–309

    Article  Google Scholar 

  • Pal R, Kumar K (2013) Malpighian tubules of adult flesh fly, Sarcophaga ruficornis fab. (Diptera: Sarcophagidae): an ultrastructural study. Tissue Cell 45(5):312–317

    Article  Google Scholar 

  • Pannabecker T (1995) T. Physiology of the Malpighian tubule. Annu Rev Entomol 40:493–510

    Article  CAS  Google Scholar 

  • Paulus HF (2004) Einiges zur Stammesgeschichte der Spinnentiere (Arthropoda, Chelicerata). In: Thaler K (ed) Diversität und Biologie von Webspinnen, Skorpionen und anderen Spinnentieren. Denisia, vol 12, pp 547–574

    Google Scholar 

  • Santos FH (2007) Ecophysiology. In: Pinto-da-Rocha R, Machado G, Giribet G (eds) Harvestmen. The biology of opiliones. Harvard University Press, Cambridge, pp 473–488

    Google Scholar 

  • Seitz, K.A., 1987. Excretory organs. In: Nentwig, W. (Ed.), Ecophysiology of spiders. Springer. pp. 239–248.

  • Shultz JW (1990) Evolutionary morphology and phylogeny of Arachnida. Cladistics 6:1–38

    Article  Google Scholar 

  • Shultz JW, Pinto-da-Rocha R (2007) Morphology and functional anatomy. In: Pinto-da-Rocha R, Machado G, Giribet G (eds) Harvestmen. The biology of opiliones. Harvard University Press, Cambridge, pp 14–61

    Google Scholar 

  • Wenning A, Greisinger U, Proux JP (1991) Insect-like characteristics of the Malpighian tubules of a non-insect: fluid secretion in the centipede Lithobius forficatus (Myriapoda: Chilopoda). J Exp Biol 158:165–180

    Article  Google Scholar 

  • Yu CH (2003) Ultrastructure of the Malpighian tubule cells in the mosquito larvae, Anopheles sinensis. Korean J Entomol 33:151–159

    Article  Google Scholar 

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Acknowledgements

We sincerely thank Elisabeth Bock und Rudi Schmied (Medical University Graz) for their excellent technical assistance. Michelle Gadpaille valuably improved the English of the manuscript. Helpful suggestions of the Editor and Reviewers are highly appreciated.

Funding

This study was partly supported by the Slovenian Research Agency within the Biodiversity Research Programme (Grant No. P1-0078) and by grant ‘Infrastrukturni program’ University of Maribor (IP-0552).

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Contributions

SL and TN designed the study and wrote the original draft. SL, TN and PK acquired light microscopy images. SL and GL acquired TEM images. All the authors revised and approved the final version.

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Correspondence to Saška Lipovšek.

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The authors declare no competing interests.

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Handling Editor: Handling Editor: Margit Pavelka

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Highlights

• Malpighian tubules (MTs) are described for the first time in Opiliones

• In Amilenus, the MTs consist of the ureter and a pair of long, blind-ended tubules

• The MTs are unitary over the whole length, composed of a single-cell type

• Apart from the exploitation of spherites, the MTs do not change during the diapause

• The one-cell type of MT might offer some advantage in nephron modelling

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Lipovšek, S., Kozel, P., Leitinger, G. et al. Malpighian tubules in harvestmen. Protoplasma 258, 1145–1153 (2021). https://doi.org/10.1007/s00709-021-01634-0

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