Hostname: page-component-669899f699-8p65j Total loading time: 0 Render date: 2025-04-29T06:38:52.645Z Has data issue: false hasContentIssue false

Behavioural alterations in surface and cave populations of isopod crustacean Asellus aquaticus by Acanthocephalus anguillae

Published online by Cambridge University Press:  10 December 2024

G. Benko
Affiliation:
University of Ljubljana, Biotechnical Faculty, Department of Biology, Slovenia
Ž. Fišer
Affiliation:
University of Ljubljana, Biotechnical Faculty, Department of Biology, Slovenia
R. Kostanjšek*
Affiliation:
University of Ljubljana, Biotechnical Faculty, Department of Biology, Slovenia
*
Corresponding author: R. Kostanjšek; Email: [email protected]

Abstract

Acanthocephalans are obligatory endoparasites that often alter the phenotype of their invertebrate intermediate host to facilitate trophic transmission to their final vertebrate host. Acanthocephalus anguillae, a widespread parasite of European freshwater fishes and isopod Asellus aquaticus, was recently discovered also in Postojna-Planina Cave System (Slovenia) parasitising olms (Proteus anguinus) and cave populations of A. aquaticus. This setting offers a unique opportunity to investigate potential fine-tuning of parasitic manipulations to the specifics of the highly divergent subterranean environment where some common phenotypic alterations lose functionality, but others might gain it. We measured three behavioural traits: movement activity, shelter-seeking, and response to light of infested and uninfested isopods from surface and cave populations. All behaviours were quantified from 1-h video-recordings via video-tracking isopod’s movement in empty or custom modified (half-sheltered/half-illuminated) Petri dishes. Infested isopods of both populations spent significantly less time sheltering and were significantly less photophobic than uninfested ones, whereas the activity of isopods was not altered. However, we observed almost no cave-specific responses upon infestation in the two altered behaviours. It seems phenotypic alterations are not particularly fine-tuned to the subterranean environment and its hosts, and likely still reflect the parasite’s surface origin.

Type
Research Paper
Copyright
© The Author(s), 2024. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Adamo, SA (2012) The strings of the puppet master: how parasites change host behaviour. In Hughes, D and Thomas, F (eds), Parasitic Manipulation. Oxford: Oxford University Press, pp. 3651.CrossRefGoogle Scholar
Aleuy, AO and Kutz, S (2020) Adaptations, life-history traits and ecological mechanisms of parasites to survive extremes and environmental unpredictability in the face of climate change. International Journal for Parasitiology: Parasites and Wildlife 12, 308317.Google ScholarPubMed
Amin, OM, Heckmann, RA, Fišer, Ž, Zakšek, V, Herlyn, H and Kostanjšek, R (2019) Description of Acanthocephalus anguillae balkanicus subsp. n. (Acanthocephala: Echinorhynchidae) from Proteus anguinus Laurenti (Amphibia: Proteidae) and the cave ecomorph of Asellus aquaticus (Crustacea: Asellidae) in Slovenia. Folia Parasitologica 66. https://doi.org/10.14411/fp.2019.015.CrossRefGoogle Scholar
Bakker, TCM, Frommen, JG and Thünken, T (2017) Adaptive parasitic manipulation as exemplified by acanthocephalans. Ethology 123(11), 779784. https://doi.org/10.1111/eth.12660.CrossRefGoogle Scholar
Balázs, G, Biró, A, Fišer, Ž, Fišer, C and Herczeg, G (2021) Parallel morphological evolution and habitat-dependent sexual dimorphism in cave- vs. surface populations of the Asellus aquaticus (Crustacea: Isopoda: Asellidae) species complex. Ecology and Evolution 11(21), 1538915403. https://doi.org/10.1002/ece3.8233.CrossRefGoogle ScholarPubMed
Benesh, DP, Hasu, T, Seppälä, O and Valtonen, ET (2009) Seasonal changes in host phenotype manipulation by an acanthocephalan: time to be transmitted? Parasitology 136(2), 219230.CrossRefGoogle Scholar
Benesh, DP, Valtonen, ET and Seppälä, O (2008) Multidimensionality and intra-individual variation in host manipulation by an acanthocephalan. Parasitology 135(5), 617626. https://doi.org/10.1017/S0031182008004216.CrossRefGoogle Scholar
Benjamini, Y and Hochberg, Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society 57(1), 289300.CrossRefGoogle Scholar
Berisha, H, Horváth, G, Fišer, Ž, Balázs, G, Fišer, C and Herczeg, G (2023) Sex-dependent increase of movement activity in the freshwater isopod Asellus aquaticus following adaptation to a predator-free cave habitat. Current Zoology 69(4), 418425. https://doi.org/10.1093/cz/zoac063.CrossRefGoogle ScholarPubMed
Breder, CM and Rasquin, P (1947) Comparative studies in the light sensitivity of blind characins from a series of Mexican caves. Bulletin of the American Museum of Natural History 89(5), 323351Google Scholar
Bulog, B and Schlegel, P (2000) Functional morphology of the inner ear and underwater audiograms of Proteus anguinus (Amphibia, Urodela). Pflugers Archiv European Journal of Physiology 439(7), R165R167. https://doi.org/10.1007/BF03376559.CrossRefGoogle ScholarPubMed
Cezilly, F and Perrot-Minnot, MJ (2010) Interpreting multidimensionality in parasite-induced phenotypic alterations: panselectionism versus parsimony. Oikos 119(8), 12241229.CrossRefGoogle Scholar
Cezilly, F, Thomas, F, Médoc, V and Perrot-Minnot, MJ (2010) Host-manipulation by parasites with complex life cycles: adaptive or not? Trends in Parasitology 26(6), 311317.CrossRefGoogle ScholarPubMed
Cooper, WE and Frederick, WG (2007) Optimal time to emerge from refuge. Biological Journal of the Linnean Society 91(3), 375382. https://doi.org/10.1111/j.1095-8312.2007.00802.x.CrossRefGoogle Scholar
Cribari-Neto, F and Zeileis, A (2010) “Beta Regression in R.” Journal of Statistical Software, 34(2), 124. https://doi.org/10.18637/jss.v034.i02.CrossRefGoogle Scholar
Culver, DC and Pipan, T (2019) The biology of caves and other subterranean habitats. Oxford University Press.CrossRefGoogle Scholar
Dawkins, R (1982) The extended phenotype (Vol. 8). Oxford: Oxford University Press.Google Scholar
Dumas, P and Chris, B (1998) The olfaction in Proteus anguinus: a behavioural and cytological study. Behavioural Processes 43(2), 107113. https://doi.org/10.1016/S0376-6357(98)00002-3.CrossRefGoogle ScholarPubMed
Emmer, KM, Russart, GKL, Walker, WH, Nelson, RJ and Courtney DeVries, A (2018) Effects of light at night on laboratory animals and research outcomes. Behavioral Neuroscience 132(4), 302314. https://doi.org/10.1037/bne0000252.CrossRefGoogle ScholarPubMed
Fayard, M, Dechaume-Moncharmont, FX, Wattier, R and Perrot-Minnot, MJ (2020) Magnitude and direction of parasite-induced phenotypic alterations: a meta-analysis in acanthocephalans. Biological Reviews 95(5), 12331251. https://doi.org/10.1111/brv.12606.CrossRefGoogle ScholarPubMed
Fišer, Ž (2017) Evolucija reproduktivne izolacije ob prilagajanju na podzemeljsko okolje - doktorsko delo. Oddelek Za Biologijo.Google Scholar
Fišer, Ž, Novak, L, Luštrik, R and Fišer, C (2016) Light triggers habitat choice of eyeless subterranean but not of eyed surface amphipods. Science of Nature 103(1). https://doi.org/10.1007/s00114-015-1329-9.CrossRefGoogle Scholar
Fišer, Ž, Prevorčnik, S, Lozej, N and Trontelj, P (2019) No need to hide in caves: shelter-seeking behavior of surface and cave ecomorphs of Asellus aquaticus (Isopoda: Crustacea). Zoology 134, 5865. https://doi.org/10.1016/j.zool.2019.03.001.CrossRefGoogle ScholarPubMed
Franceschi, N, Cornet, S, Bollache, L, Dechaume-Moncharmont, FX, Bauer, A, Motreuil, S and Rigaud, T (2010) Variation between populations and local adaptation in acanthocephalan-induced parasite manipulation. Evolution 64(8), 24172430. https://doi.org/10.1111/j.1558-5646.2010.01006.x.Google ScholarPubMed
Friard, O and Gamba, M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods in Ecology and Evolution 7(11), 13251330. https://doi.org/10.1111/2041-210X.12584.CrossRefGoogle Scholar
Herczeg, G, Hafenscher, VP, Balázs, G, Fišer, Ž, Kralj-Fišer, S and Horváth, G (2020) Is foraging innovation lost following colonization of a less variable environment? A case study in surface- vs. cave-dwelling Asellus aquaticus. Ecology and Evolution 10(12), 53235331. https://doi.org/10.1002/ece3.6276.CrossRefGoogle ScholarPubMed
Herczeg, G, Nyitrai, V, Balázs, G and Horváth, G (2022) Food preference and food type innovation of surface- vs. cave-dwelling waterlouse (Asellus aquaticus) after 60 000 years of isolation. Behavioral Ecology and Sociobiology 76(1), 011. https://doi.org/10.1007/s00265-021-03109-x.CrossRefGoogle Scholar
Hervant, F, Mathieu, J, Barré, H, Simon, K and Pinon, C (1997) Comparative study on the behavioral, ventilatory, and respiratory responses of hypogean and epigean crustaceans to long-term starvation and subsequent feeding. Comparative Biochemistry and Physiology - A Physiology 118(4), 12771283. https://doi.org/10.1016/S0300-9629(97)00047-9.CrossRefGoogle Scholar
Horváth, G, Kerekes, K, Nyitrai, V, Balázs, G, Berisha, H and Herczeg, G (2023) Exploratory behaviour divergence between surface populations, cave colonists and a cave population in the water louse, Asellus aquaticus. Behavioral Ecology and Sociobiology 77(1). https://doi.org/10.1007/s00265-022-03288-1.CrossRefGoogle Scholar
Horváth, G, Sztruhala, SS, Balázs, G and Herczeg, G (2021) Population divergence in aggregation and sheltering behaviour in surface- versus cave-adapted Asellus aquaticus (Crustacea: Isopoda). Biological Journal of the Linnean Society 134(3), 667678. https://doi.org/10.1093/biolinnean/blab093.CrossRefGoogle Scholar
Hughes, DP, Andersen, SB, Hywel-Jones, NL, Himaman, W, Billen, J and Boomsma, JJ (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC Ecology 11:13.CrossRefGoogle ScholarPubMed
Klein, SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26: 247264.CrossRefGoogle ScholarPubMed
Konec, M, Prevorčnik, S, Sarbu, SM, Verovnik, R and Trontelj, P (2015) Parallels between two geographically and ecologically disparate cave invasions by the same species, Asellus aquaticus (Isopoda, Crustacea). Journal of Evolutionary Biology 28(4), 864875. https://doi.org/10.1111/jeb.12610.CrossRefGoogle ScholarPubMed
Kostanjšek, R, Zakšek, V, Bizjak-Mali, L and Trontelj, P (2023) The olm (Proteus anguinus), a flagship groundwater species. In Malard, F, Griebler, C and Rétaux, S (eds.), Groundwater Ecology and Evolution. Academic Press, pp. 305327.CrossRefGoogle Scholar
Lefevre, T, Roche, B, Poulin, R, Hurd, H, Renaud, F and Thomas, F (2008) Exploiting host compensatory responses: the ‘must’of manipulation? Trends in Parasitology 24(10), 435439.CrossRefGoogle ScholarPubMed
Lenth, R (2023). _emmeans: Estimated Marginal Means, aka Least-Squares Means_. R package version 1.8.9, <https://CRAN.R-project.org/package=emmeans>..>Google Scholar
Lope, G, Bonacchi, N, Frazão, J, Neto, JP, Atallah, BV, Soares, S, Moreira, L, Matias, S, Itskov, PM, Correia, PA, Medina, RE, Calcaterra, L, Dreosti, E, Paton, JJ and Kampff, AR (2015) Bonsai: an event-based framework for processing and controlling data streams. Frontiers in Neuroinformatics 9(APR), 114. https://doi.org/10.3389/fninf.2015.00007.Google Scholar
Lyndon, AR (1996) The role of acanthocephalan parasites in the predation of freshwater isopods by fish. In Greenstreet, SPR and Tasker, ML (eds), Aquatic Predators and their Prey. Oxford, UK: Fishing News Books, 2632.Google Scholar
Manenti, R, Vinci, L, Barzaghi, B, Lombardi, B, Teodoro, C, Baglioni, L, Melotto, A and Ficetola, GF (2024) Sit-and-wait foraging is not enough in food-deprived environments: evidence from groundwater and salamanders. Animal Behaviour 207, 191200. https://doi.org/10.1016/j.anbehav.2023.11.005.CrossRefGoogle Scholar
Nickol, BB and Whittaker, FB (1978) Neoechinorhynchus cylindratus (Acanthocephala) from the troglodytic fish, Amblyopsis spelaea, in Kentucky. Proc Helminthol Soc Wash 45, 136137.Google Scholar
Park, T and Sparkes, TC (2017) Multidimensionality of modification in an isopod-acanthocephalan system. Frontiers in Ecology and Evolution 5(SEP), 113. https://doi.org/10.3389/fevo.2017.00103.CrossRefGoogle Scholar
Perrot-Minnot, MJ, Cozzarolo, CS, Amin, O, Barčák, D, Bauer, A, Filipović Marijić, V, García-Varela, M, Servando Hernández-Orts, J, Yen Le, TT, Nachev, M, Orosová, M, Rigaud, T, Šariri, S, Wattier, R, Reyda, F and Sures, B (2023) Hooking the scientific community on thorny-headed worms: interesting and exciting facts, knowledge gaps and perspectives for research directions on Acanthocephala. Parasite 30. https://doi.org/10.1051/parasite/2023026.CrossRefGoogle ScholarPubMed
Perrot-Minnot, MJ, Sanchez-Thirion, K and Cézilly, F (2014) Multidimensionality in host manipulation mimicked by serotonin injection. Proceedings of the Royal Society B: Biological Sciences 281(1796). https://doi.org/10.1098/rspb.2014.1915.Google ScholarPubMed
Peuß, R, Box, AC, Chen, S, Wang, Y, Tsuchiya, D, Persons, JL, Kenzior, A, Maldonado, E, Krishnan, J, Scharsack, JP, Slaughter, BD and Rohner, N (2020) Adaptation to low parasite abundance affects immune investment and immunopathological responses of cavefish. Nature Ecology and Evolution 4(10), 14161430. https://doi.org/10.1038/s41559-020-1234-2.CrossRefGoogle ScholarPubMed
Pilecka-Rapacz, M (1986) On the development of acanthocephalans of the genus Acanthocephalus Koebreuther, 1771, with special attention to their influence on intermediate host, Asellus aquaticus L. Acta Parasitol. Pol. 30, 233248.Google Scholar
Poulin, R (1995). “Adaptive” changes in the behaviour of parasitized animals: a critical review. International Journal for Parasitology 25(12), 13711383.CrossRefGoogle ScholarPubMed
Poulin, R (2010) Parasite manipulation of host behavior: an update and frequently asked questions. In Advances in the Study of Behavior (Vol. 41, pp. 151186). Academic Press.Google Scholar
Prevorčnik, S, Blejec, A and Sket, B (2004) Racial differentiation in Asellus aquaticus (L.) (Crustacea: Isopoda: Asellidae). Archiv Fur Hydrobiologie 160(2), 193214. https://doi.org/10.1127/0003-9136/2004/0160-0193.CrossRefGoogle Scholar
Protas, M and Jeffery, WR (2012) Evolution and development in cave animals: from fish to crustaceans. Wiley Interdisciplinary Reviews: Developmental Biology 1(6), 823845. https://doi.org/10.1002/wdev.61.CrossRefGoogle Scholar
Protas, M, Trontelj, P, Prevorčnik, S and Fišer, Ž (2023) The Asellus aquaticus species complex: an invertebrate model in subterranean evolution. In Malard, F, Griebler, C, Rétaux, S (eds.), Groundwater Ecology and Evolution. Academic Press, pp. 329350.CrossRefGoogle Scholar
Team, R Core. (2022). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/Google Scholar
Schlegel, P and Bulog, B (1997) Population-specific behavioral electrosensitivity of the European blind cave salamander, Proteus anguinus. Journal of Physiology Paris 91(2), 7579. https://doi.org/10.1016/S0928-4257(97)88941-3.CrossRefGoogle ScholarPubMed
Schlegel, PA, Steinfartz, S and Bulog, B (2009) Non-visual sensory physiology and magnetic orientation in the Blind Cave Salamander, Proteus anguinus (and some other cave-dwelling urodele species). Review and new results on light-sensitivity and non-visual orientation in subterranean urodeles (Amphibia). Animal Biology 59(3), 351384. https://doi.org/10.1163/157075609X454971.CrossRefGoogle Scholar
Seppälä, O, Valtonen, ET and Benesh, DP (2008) Host manipulation by parasites in the world of dead-end predators: adaptation to enhance transmission? Proceedings of the Royal Society B: Biological Sciences 275(1643), 16111615. https://doi.org/10.1098/rspb.2008.0152.CrossRefGoogle ScholarPubMed
Sket, B (1994) Distribution of Asellus aquaticus (Crustacea: Isopoda: Asellidae) and its hypogean populations at different geographic scales, with a note on Proasellus istrianus. Hydrobiologia 287(1), 3947. https://doi.org/10.1007/BF00006895.CrossRefGoogle Scholar
Tesarova, M, Mancini, L, Mauri, E, Aljančič, G, Nǎpǎruş-Aljančič, M, Kostanjšek, R, Bizjak Mali, L, Zikmund, T, Kaucká, M, Papi, F, Goyens, J, Bouchnita, A, Hellander, A, Adameyko, I and Kaiser, J (2022) Living in darkness: exploring adaptation of Proteus anguinus in 3 dimensions by X-ray imaging. GigaScience 11, 18. https://doi.org/10.1093/gigascience/giac030.CrossRefGoogle ScholarPubMed
Thomas, F, Brodeur, J, Maure, F, Franceschi, N, Blanchet, S and Rigaud, T (2011) Intraspecific variability in host manipulation by parasites. Infection, Genetics and Evolution 11(2), 262269. https://doi.org/10.1016/j.meegid.2010.12.013.CrossRefGoogle ScholarPubMed
Thomas, F, Poulin, R and Brodeur, J (2010) Host manipulation by parasites: a multidimensional phenomenon. Oikos 119(8), 12171223. https://doi.org/10.1111/j.1600-0706.2009.18077.x.CrossRefGoogle Scholar
Turk, S, Sket, B and Sarbu, Ş (1996) Comparison between some epigean and hypogean populations of Asellus aquaticus (Crustacea: Isopoda: Asellidae). Hydrobiologia 337(1–3), 161170. https://doi.org/10.1007/BF00028517.CrossRefGoogle Scholar
Uiblein, F, Durand, JP, Juberthie, C and Parzefall, J (1992) Predation in caves : the effects of prey immobility and darkness on the foraging behaviour of two salamanders, Euproctus asper and Proteus anguinus. Behavioual Processes 28(1–2), 3340.CrossRefGoogle ScholarPubMed
Uiblein, F and Parzefall, J (1993) Does the cave salamander Proteus anguinus detect mobile prey by mechanical cues? Memoires se Biospeleologie 20, 261264.Google Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York.CrossRefGoogle Scholar
Zahavi, A (1979) Parasitism and nest predation in parasitic cuckoos. The American Naturalist 113(1), 157159.CrossRefGoogle Scholar
Zeileis, A and Hothorn, T (2002) Diagnostic checking in regression relationships. R News 2/3, 7-10.Google Scholar
Zuk, M and McKean, KA (1996) Sex differences in parasite infections: patterns and processes. International Journal for Parasitology 26(10), 10091024. https://doi.org/10.1016/S0020-7519(96)00086-0.CrossRefGoogle ScholarPubMed
Supplementary material: File

Benko et al. supplementary material

Benko et al. supplementary material
Download Benko et al. supplementary material(File)
File 290.6 KB