Seasonal Niche Decoupling and Thermal Alignment of Two Co-occurring Ectoparasites (Diplectanum aequans and Lernanthropus kroyeri) in Cultured European Seabass, Dicentrarchus Labrax

Abstract

Co-occurring ectoparasites represent a challenge in intensive aquaculture; however, quantitative tools to assess how parasite species partition their temporal niches remain limited. The seasonal dynamics of two coexisting gill ectoparasites, Diplectanum aequans and Lernanthropus kroyeri, infecting farmed European seabass (Dicentrarchus labrax) were evaluated using two complementary indices: a Seasonal Niche-Decoupling Index (D) and a standardized Thermal Alignment Score (S). The D index quantified temporal separation in parasite dominance, while S was defined as the Pearson correlation coefficient between seasonal parasite abundance and water temperature. Although both parasites were present year-round, their population dynamics exhibited contrasting seasonal patterns. D. aequans peaked in spring, whereas L. kroyeri predominated in winter, resulting in a pronounced but incomplete temporal separation (D = 0.483). Standardized thermal alignment analysis indicated that D. aequans exhibited a strong negative alignment (S = −0.76), whereas L. kroyeri showed a weak positive alignment (S = +0.19). These findings suggest that temporal niche partitioning may facilitate the coexistence of ectoparasites under continuous infection pressure in intensive aquaculture systems. Under projected warming scenarios, the seasonal window of D. aequans may contract, whereas L. kroyeri may expand its temporal niche. The applied indices provide a practical and transferable framework for evaluating seasonal parasite dynamics and may support improved parasite management strategies in aquaculture.

Keywords

• Dicentrarchus labrax
• ectoparasites
• seasonal niche partitioning
• thermal alignment
• aquaculture

References

1. Abdallah, E. S. H., & Hamouda, A. H. (2023). Morphological and molecular characterization of Lernanthropus kroyeri, a copepod infesting the gills of European seabass (Dicentrarchus labrax). Egyptian Journal of Aquatic Research, 49(1), 41–48. https://doi.org/10.1016/j.ejar.2022.11.003 google scholar
2. Altizer, S., Ostfeld, R. S., Johnson, P. T. J., Kutz, S., & Harvell, C. D. (2006). Climate change and the dynamics of infectious diseases in mammals. Biological Reviews, 81(4), 515–537. https://doi.org/10.1017/S1464793106007040 google scholar
3. Aly, S., El-Gheit, E.-S. A., Osman, H., Tolba, M. M., Essameldin, H. M., & Fathi, M. (2024). Cumulative assessment of Diplectanum spp. occurrence, prevalence, and pathological impact in Dicentrarchus labrax from varied Egyptian fish farms. Veterinary Parasitology, 329, 110215. https://doi.org/10.1016/j.vetpar.2024.110215 google scholar
4. Antonelli, L., Foata, J., Quilichini, Y., & Marchand, B. (2016). Influence of season and site location on European cultured sea bass parasites in Corsican fish farms using indicator species analysis (IndVal). Parasitology Research, 115(4), 1461–1472. https://doi.org/10.1007/s00436-016-4893-7 google scholar
5. Bouloux, C., Langlais, M., & Silan, P. (1998). A marine host–parasite model with direct biological cycle and age structure. Ecological Modelling, 107(1), 73–86. https://doi.org/10.1016/S0304-3800(97)00208-1 google scholar
6. Bush, A. O., Lafferty, K. D., Lotz, J. M., & Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83(4), 575–583. google scholar
7. Byers, J. E. (2021). Marine parasites and disease in the era of global climate change. Annual Review of Marine Science, 13, 1–23. https://doi.org/10.1146/annurev-marine-032320-095828 google scholar
8. Cascarano, M. C., Stavrakidis-Zachou, O., Mladineo, I., Thompson, K. D., Papandroulakis, N., & Katharios, P. (2021). Mediterranean aquaculture in a changing climate: Temperature effects on pathogens and diseases of three farmed fish species. Pathogens, 10(9), 1205. https://doi.org/10.3390/pathogens10091205 google scholar

9. Cecchini, S., Saroglia, M., Berni, P., & Cognetti-Varriale, A. M. (1998). Influence of temperature on the life cycle of Diplectanum aequans (Monogenea, Diplectanidae), parasitic on sea bass, Dicentrarchus labrax. Journal of Fish Diseases, 21(1), 73–75. https://doi.org/10.1046/j.1365-2761.1998.00068.x google scholar
10. Čolak, S., Lorencin, V., Končar, D., Šarić, T., Petani, B., & Mustać, B. (2021). Seasonal dynamics of parasite Lernanthropus kroyeri (van Beneden, 1851) on cultured sea bass Dicentrarchus labrax (Linnaeus, 1758) from the Adriatic Sea. Aquaculture, 531, 735851. https://doi.org/10.1016/j.aquaculture.2020.735851 google scholar
11. Czekanowski, J. (1909). Zur differentialdiagnose der Neandertalgruppe. Korrespondenz-Blatt der Deutschen Gesellschaft für Anthropologie, Ethnologie und Urgeschichte, 40, 44-47. google scholar
12. Fioravanti, M. L., Mladineo, I., Palenzuela, O., Beraldo, P., Gustinelli, A., & Sitjà-Bobadilla, A. (2020). Fish farmer’s guide to combating parasitic infections in European sea bass and gilthead sea bream aquaculture (Guide No. 4). ParaFishControl. google scholar
13. Gehman, A.-L. M., Hall, R. J., & Byers, J. E. (2018). Host and parasite thermal ecology jointly determine the effect of climate warming on epidemic dynamics. Proceedings of the National Academy of Sciences of the United States of America, 115(4), 744–749. https://doi.org/10.1073/pnas.1705067115 google scholar
14. González-Lanza, C., Alvarez-Pellitero, P., & Sitjà-Bobadilla, A. (1991). Diplectanidae (Monogenea) infestations of sea bass, Dicentrarchus labrax, from the Spanish Mediterranean area. Parasitology Research, 77, 307–314. https://doi.org/10.1007/BF00930906 google scholar
15. Hinkle, D. E., Wiersma, W., & Jurs, S. G. (2003). Applied statistics for the behavioral sciences (5th ed.). Houghton Mifflin. google scholar
16. Marcogliese, D. J. (2008). The impact of climate change on the parasites and infectious diseases of aquatic animals. Reviews in Fish Biology and Fisheries, 18(2), 133–156. https://doi.org/10.1007/s11160-007-9051-0 google scholar
17. Masala-Antonelli, L., Godeaux, Q., Poiron-Guidoni, N., & Quilichini, Y. (2021). A long-term monitoring survey of Diplectanum aequans parasite of European cultured seabass Dicentrarchus labrax from Corsican fish farms. Pathogens, 10(7), 896. https://doi.org/10.3390/pathogens10070896 google scholar
18. Mladineo, I. (2004). Monogenean parasites in Adriatic cage-reared fish. Acta Adriatica, 45(1), 61–67. google scholar
19. Mladineo, I. (2005). Parasite communities of cage-reared sea bass (Dicentrarchus labrax) in the Adriatic Sea. Diseases of Aquatic Organisms, 64(1), 77–83. https://doi.org/10.3354/dao064077 google scholar
20. Mladineo, I., Petrić, M., Šegvić, T., & Dobričić, N. (2010). Scarcity of parasite assemblages in the Adriatic-reared European sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata). Veterinary Parasitology, 174(3–4), 307–314. https://doi.org/10.1016/j.vetpar.2010.08.009 google scholar
21. Özer, A., Okkay, S., Öztürk, T., Baki, B., Acar, G., Güven, A., & Öztürk, D. K. (2019). Comparative Diplectanum aequans infestations in cultured European seabass (Dicentrarchus labrax) in the Black Sea and the Aegean Sea. Ege Journal of Fisheries and Aquatic Sciences, 36(2), 163–169. https://doi.org/10.12714/egejfas.2019.36.2.08 google scholar
22. Paull, S. H., & Johnson, P. T. J. (2014). Experimental warming drives a seasonal shift in the timing of host–parasite dynamics with consequences for disease risk. Ecology Letters, 17(4), 445–453. https://doi.org/10.1111/ele.12244 google scholar
23. Pianka, E. R. (1973). The structure of lizard communities. Annual Review of Ecology and Systematics, 4, 53-74. google scholar
24. Rohde, K. (1994). Niche theory and the ecology of parasites. International Journal for Parasitology, 24(1), 31–40. https://doi.org/10.1016/0020-7519(94)90056-6 google scholar
25. Schoener, T. W. (1970). Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology, 51(3), 408–418. https://doi.org/10.2307/1935376 google scholar
26. Shocket, M. S., Vergara, D., Sickbert, A. J., Walsman, J. M., Strauss, A. T., Hite, J. L., Duffy, M. A., Cáceres, C. E., & Hall, S. R. (2018). Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics. Ecology, 99(9), 1971–1983. https://doi.org/10.1002/ecy.2430 google scholar
27. Silan, P., Langlais, M., & Maillard, C. (1996). Marine host–parasite systems: A new discrete model. Journal of Biological Systems, 4(2), 241–254. https://doi.org/10.1142/S0218339096000203 google scholar
28. Yıldız, H. Y., & Korkmaz, A. Ş. (2021). Parasitic copepod (Lernanthropus kroyeri) on caged sea bass (Dicentrarchus labrax): An estimation of abundance and internal infestation pressure. Journal of Fish Diseases, 44(12), 1901–1909. https://doi.org/10.1111/jfd.13504 google scholar
29. Zoli, M., Rossi, L., Bibbiani, C., & Bacenetti, J. (2023). Life cycle assessment of seabass and seabream production in the Mediterranean area: A critical review. Aquaculture, 573, 739580. https://doi.org/10.1016/j.aquaculture.2023.739580 google scholar