Diversity of nematodes associated with Heterodermia diademata: A case study in the Eco Área of Avellaneda, Buenos Aires, Argentina

José M. Rusconi; Renato García; Augusto Salas; M. Fernanda Achinelly

doi:10.25260/EA.23.33.3.0.2227

Autores/as

José M. Rusconi Centro de Estudios Parasitológicos y de Vectores (CEPAVE)-CCT-La Plata-CONICET-UNLP. La Plata, Buenos Aires, Argentina
Renato García Laboratorio de Biodiversidad y Genética Ambiental (BioGeA), Departamento de Ambiente y Turismo (UNDAV), Universidad Nacional de Avellaneda. Buenos Aires, Argentina
Augusto Salas Instituto Nacional de Tecnología Agropecuaria (INTA), Instituto de Microbiología y Zoología Agrícola. Buenos Aires, Argentina
M. Fernanda Achinelly Centro de Estudios Parasitológicos y de Vectores (CEPAVE)-CCT-La Plata-CONICET-UNLP. La Plata, Buenos Aires, Argentina

DOI:

https://doi.org/10.25260/EA.23.33.3.0.2227

Palabras clave:

Heterodermia diademata, nematodes, líquenes, rol ecosistémico

Resumen

Los líquenes representan una forma de vida compleja caracterizada por una asociación simbiótica entre al menos dos organismos: un hongo y un alga. En esta relación única, el hongo ofrece un hábitat protector para el alga, la que, a su vez, aprovecha la energía de la luz solar, el agua y el aire para proporcionar sustento al hongo. Cumplen roles ecológicos como fuente de alimento para muchos invertebrados y sirven como nivel trófico basal para una variedad de animales; se los considera microecosistemas que pueden albergar una biota rica y diversa. Los nematodos se encuentran entre los metazoos más extendidos y abundantes, habitan ambientes intersticiales húmedos en todos los hábitats y son abundantes en hábitats bentónicos marinos y de agua dulce y en el suelo. También se los encontró en acumulaciones de detritos en las axilas de las hojas, en los ángulos de las ramas de los árboles y en musgos y líquenes. En este estudio de caso se examinó el papel trófico y la diversidad de nematodos de vida libre asociados con líquenes en un área de la provincia de Buenos Aires, Argentina. Se revelaron siete géneros de nematodos vinculados a Heteroderma diademata, que representan todos los niveles tróficos de nematodos de vida libre: bacteriófagos (Plectus y Acrobeles), fungívoros (Aphelenchus), herbívoros (Helicotylenchus), omnívoros (Eudorylaimus y Mesodorylaimus) y un depredador (Prionchulus).

Citas

Anderson, O. R. 2014. Microbial communities associated with tree bark foliose lichens: a perspective on their microecology. Journal of Eukaryotic Microbiology 61(4):364-370. https://doi.org/10.1111/jeu.12116.

Asplund, J., and D. A. Wardle. 2013. The impact of secondary compounds and functional characteristics on lichen palatability and decomposition. Journal of Ecology 101(3):689-700. https://doi.org/10.1111/1365-2745.12075.

Asplund, J., and D. A. Wardle. 2017. How lichens impact on terrestrial community and ecosystem properties. Biological Reviews 92(3):1720-1738. https://doi.org/10.1111/brv.12305.

Asplund, J., S. Bokhorst, P. Kardol, and D. A. Wardle. 2015. Removal of secondary compounds increases invertebrate abundance in lichens. Fungal Ecology 18:18-25. https://doi.org/10.1016/j.funeco.2015.07.009.

Belguidoum, A., R. Haichour, T. Lograda, and M. Ramdani. 2022. Biomonitoring of air pollution by lichen diversity in the urban area of Setif, Algeria. Biodiversitas Journal of Biological Diversity 23(2). https://doi.org/10.13057/biodiv/d230240.

Bilgrami A. L. 2008. Biocontrol potentials of predatory nematodes. Pp. 3-28 in A. Ciancio and K. G. Mukerji (eds.). Integrated Management and Biocontrol of Vegetable and Grain Crops Nematodes. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-6063-2_1.

Bokhorst, S., J. Asplund, P. Kardol, and D. A. Wardle 2015. Lichen physiological traits and growth forms affect communities of associated invertebrates. Ecology 96(9):2394-2407. https://doi.org/10.1890/14-1030.1.

Bongers, T. 1990. The maturity index: an ecological measure of environmental disturbance based on nematode species composition. Oecologia 83(1):14-19. https://doi.org/10.1007/BF00324627.

Brodo, I. M., S. D. Sharnoff, and S. Sharnoff. 2001. Lichens of North America. Yale University Press. https://doi.org/10.29173/bluejay5827.

Caldwell, J. R. 1981a. Biomass and respiration of nematode populations in two moss communities at Signy Island maritime Antarctic. Oikos 37:160-166. https://doi.org/10.2307/3544460.

Caldwell, J. R. 1981b. The Signy Island (South Orkney Islands terrestrial reference sites: XIII. Population dynamics of the nematode fauna. British Antarctic Survey Bulletin 54:33-46.

Caveness, F. E., and H. J. Jensen. 1955. Investigations of various therapeutic measures to eliminate root lesion nematodes from Easter lilies. Plant Disease Reporter 39:710-715.

Chapin, F. S. 1980. The mineral nutrition of wild plants. Annual Review of Ecology and Systematics 11:233-260. https://doi.org/10.1146/annurev.es.11.110180.001313.

Chaves, E., M. M. Echeverría, H. M. Álvarez, and A. Salas. 2019. Clave para determinar géneros de nematodos del suelo de la República Argentina. Fundación de Historia Natural Félix de Azara Centro de Ciencias Naturales y Antropológicas, Universidad Maimónides, Buenos Aires, Argentina.

Cid del Prado, V. I. 2012. Two new species of nematodes (Cephalobida: Chambersiellidae) from moss from North and South America. Nematropica 42(1):108-114.

Cornelissen, J. H., S. I. Lang, N. A. Soudzilovskaia, and H. J. During. 2007. Comparative cryptogam ecology: a review of bryophyte and lichen traits that drive biogeochemistry. Annals of Botany 99(5):987-1001. https://doi.org/10.1093/aob/mcm030.

Darby, B. J., D. A. Neher, and J. Belnap. 2007. Soil nematode communities are ecologically more mature beneath late-than early-successional stage biological soil crusts. Applied Soil Ecology 35(1):203-212. https://doi.org/10.1016/j.apsoil.2006.04.006.

De Goede, R. G. M., B. C. Verschoor, and S. S. Georgieva. 1993. Nematode distribution, trophic structure and biomass in a primary succession of blown-out areas in a drift sand landscape. Fundamental and Applied Nematology 16(6):525-538.

De vera, J. P. 2012. Lichens as survivors in space and on Mars. Fungal Ecology 5:472-479. https://doi.org/10.1016/j.funeco.2012.01.008.

Ferris, H., and T. Bongers. 2006. Nematode indicators of organic enrichment. Journal of Nematology 38:3.

Fröberg, L., A. Baur, and B. Baur. 1993. Differential herbivore damage to calcicolous lichens by snails. The Lichenologist 25:83-95. https://doi.org/10.1006/lich.1993.1015.

Gadea, E. 1976. Nematodos liquenícolas de la isla Mayor (Mar Menor). Miscel lània Zoològica 3-5:13-18.

Gauslaa, Y. 2005. Lichen palatability depends on investments in herbivore defense. Oecologia 143(1):94-105. https://doi.org/10.1007/s00442-004-1768-z.

Gerson, U., and M. R. D. Seaward. 1977. Lichen-invertebrate associations. Pp. 69-119 in M. R. D. Seaward (ed.). Lichen Ecology. Academic Press, London.

Hazir, S., H. K. Kaya, M. Touray, H. Cimen, and D. Shapiro-Ilan. 2022. Basic laboratory and field manual for conducting research with entomopathogenic nematodes Steinernema and Heterorhabditis, and their bacterial symbionts. Turkish Journal of Zoology 46:305-350. https://doi:10.55730/1300-0179.3085.

Hawksworth, D. L., and M. Grube. 2020. Lichens redefined as complex ecosystems. The New Phytologist 227(5):1281-1283. https://doi.org/10.1111/nph.16630.

Heidemann, K., A. Hennies, J. Schakowske, L. Blumenberg, L. Ruess, S. Scheu, and M. Maraun. 2014. Free‐living nematodes as prey for higher trophic levels of forest soil food webs. Oikos 123(10):1199-1211. https://doi.org/10.1111/j.1600-0706.2013.00872.x.

Huiskes, A. H. L, N. J. M. Gremmen, and J. W. Francke. 1997. The delicate stability of lichen symbiosis: comparative studies on the photosynthesis of the lichen Mastodia tesselata and its free-living phycobiont, the alga Prasiola crispa. Pp. 234-240 in B. Battaglia, J. Valencia and D. W. H. Walton (eds.). Antarctic Communities. Species, Structures and Survival. University Press: Cambridge.

Jairajpuri, M. S., and W. U. Khan. 1982. Predatory nematodes (Mononchida). New Delhi, Associated Publishing Company.

Kaasalainen, U., A. R. Schmidt, and J. Rikkinen. 2017. Diversity and ecological adaptations in Palaeogene lichens. Nature Plants 3(5):1-8. https://doi.org/10.1038/nplants.2017.49.

Kumpula, J., S. C. Lefrere, and M. Nieminen. 2004. The use of woodland lichen pasture by reindeer in winter with easy snow conditions. Arctic 57:273-278. https://doi.org/10.14430/arctic504.

Leinaas, H. P., and A. Fjellberg. 1985. Habitat structure and life-history strategies of 2 partly sympatric and closely related, lichen feeding Collembolan species. Oikos 44:448-458. https://doi.org/10.2307/3565786.

Liu, Y., X. Li, R. Jia, L. Huang, Y. Zhou, and Y. Gao. 2011. Effects of biological soil crusts on soil nematode communities following dune stabilization in the Tengger Desert, Northern China. Applied Soil Ecology 49:118-124. https://doi.org/10.1016/j.apsoil.2011.06.007.

Nash, T. 2008. Introduction. Pp. 1-8 in T. Nash III (ed.). Lichen Biology. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511790478.002.

Neher, D. A. 2001. Role of nematodes in soil health and their use as indicators. Journal of Nematology 33(4):161.

Neher, D. A., and B. J. Darby. 2009. Nematodes as environmental indicators, Pp. 107-123. In M. J. Wilson and T. Kakouli-Duarte. (eds.). General community indices that can be used for analysis of nematode assemblages. CABI, UK. https://doi.org/10.1079/9781845933852.0107.

Manzanilla-López, R. H., and N. Marbán-Mendoza. 2012. Practical plant nematology. Guadalajara, Jalisco, México, Biblioteca Básica de Agricultura, Colegio de Postgraduados and Mundi-Prensa.

McSorley, R. 2012. Ecology of the dorylaimid omnivore genera Aporcelaimellus, Eudorylaimus and Mesodorylaimus. Nematology 14(6):645-663. https://doi.org/10.1163/156854112X651168.

Pöykkö, H., M. Hyvärinen, and M. Bačkor. 2005. Removal of lichen secondary metabolites affects food choice and survival of lichenivorous moth larvae. Ecology 86(10):2623-2632. https://doi.org/10.1890/04-1632.

Raggio, J., A. Pintado, C. Ascaso, R. De la torre, A. De Los Ríos, J. Wierzchos, G. Horneck, and L. G. Sancho. 2011. Whole lichen thallus survive exposure to space conditions: results of lithopanspermia experiment with Aspicilia fruticulosa. Astrobiology 11(4):281-292. https://doi.org/10.1089/ast.2010.0588.

Ranković, B., and M. Kosanić. 2019. Lichens as a potential source of bioactive secondary metabolites. Pp. 1-29 in Lichen secondary metabolites. Springer, Cham. https://doi.org/10.1007/978-3-030-16814-8_1.

Roy, P., and A. Borah. 2020. Role of Predeceous nematodes in plant disease management. Pharma Innovation Journal 9:463-467.

Ryss, A., S. Bostrom, and B. Sohlenius. 2005. Tylenchid nematodes found on the Nunatak basen, East Antarctica. Annales Zoologici 55(3):315-324.

Salas, A. 2019. Estudio de la diversidad de nematodos asociados al sustrato como indicadores de la calidad del suelo en agroecosistemas. Tesis de Doctorado en Ciencias Naturales. Facultad de Ciencias Naturales y Museo. Universidad Nacional de La Plata, Buenos Aires, La Plata, Argentina. https://doi.org/10.35537/10915/74184.

Salas, A., and M. F. Achinelly. 2020. Community structure of soil nematodes associated with the rhizosphere of Solanum lycopersicum in a major production area in Argentina: a case study among agroecosystem types. Journal of Soil Science and Plant Nutrition 20(1):43-54. https://doi.org/10.1007/s42729-019-00099-8.

Siddiqi, M., and D. Hawksworth. 1982. Nematodes associated with galls on Cladonia glauca, including two new Species. The Lichenologist 14(2):175-184. https://doi.org/10.1017/S0024282982000310.

Sieriebriennikov, B., H. Ferris, and R. G. de Goede. 2014. NINJA: An automated calculation system for nematode-based biological monitoring. European Journal of Soil Biology 61:90-93. https://doi.org/10.1016/j.ejsobi.2014.02.004.

Talavera, M., T. C. Thoden, M. D Vela‐Delgado, S. Verdejo‐Lucas, and S. Sánchez‐Moreno. 2021. The impact of fluazaindolizine on free‐living nematodes and the nematode community structure in a root‐knot nematode infested vegetable production system. Pest Management Science 77(11):5220-5227. https://doi.org/10.1002/ps.6563.

Vera-Morales, M., R. F. Castañeda-Ruiz, D. Sosa, A. Quevedo, J. Naranjo-Morán, L. Serrano, and M. F. Ratti. 2022. Mecanismos de captura, colonización y alimentación empleados por parásitos y predadores de nematodos. Ecosistemas 31(3):2390-2390. https://doi.org/10.7818/ECOS.2390.

Yeates, G. W., T. Bongers, R. G. De Goede, D. W. Freckman, and S. Georgieva. 1993. Feeding habits in soil nematode families and genera - an outline for soil ecologists. Journal of Nematology 25(3):315.

Weldon, J., and U. Grandin. 2021. Weak recovery of epiphytic lichen communities in Sweden over 20 years of rapid air pollution decline. The Lichenologist 53(2):203-213. https://doi.org/10.1017/S0024282921000037.

Young, E. H., and A. Unc. 2023. A review of nematodes as biological indicators of sustainable functioning for northern soils undergoing land-use conversion. Applied Soil Ecology 183:104762. https://doi.org/10.1016/j.apsoil.2022.104762.

Zheng, J., F. Dini-Andreote, L. Luan, S. Geisen, J. Xue, H. Li, B. Sun, and Y. Jiang. 2022. Nematode predation and competitive interactions affect microbe-mediated phosphorus dynamics. Mbio 13(3):e03293-21. https://doi.org/10.1128/mbio.03293-21.