Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-23T03:18:06.689Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversity and dynamics in larval digenean assemblages parasitizing Heleobia parchappii in a freshwater shallow lake from the Southeastern Pampa plain, Argentina

Published online by Cambridge University Press:  28 October 2021

Florencia Paz Campanini ,
Matías Javier Merlo ,
María Agustina Méndez Casariego  and
Manuela Parietti Open the ORCID record for Manuela Parietti [Opens in a new window]
Florencia Paz Campanini
Affiliation:
Laboratorio de Parasitología, Universidad Nacional de Mar del Plata (UNMDP), Mar del Plata, Bueno Aires, Argentina
Matías Javier Merlo
Affiliation:
Laboratorio de Parasitología, Universidad Nacional de Mar del Plata (UNMDP), Mar del Plata, Bueno Aires, Argentina Instituto de Investigaciones en Producción Sanidad y Ambiente (CONICET-UNMDP), Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
María Agustina Méndez Casariego
Affiliation:
Laboratorio de Parasitología, Universidad Nacional de Mar del Plata (UNMDP), Mar del Plata, Bueno Aires, Argentina Instituto de Investigaciones en Producción Sanidad y Ambiente (CONICET-UNMDP), Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
Manuela Parietti*
Affiliation:
Laboratorio de Parasitología, Universidad Nacional de Mar del Plata (UNMDP), Mar del Plata, Bueno Aires, Argentina Instituto de Investigaciones en Producción Sanidad y Ambiente (CONICET-UNMDP), Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina
*
Author for correspondence: Manuela Parietti, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Digeneans have important roles within ecosystems; however, it is estimated that only 14% of the species have been described. Therefore, before being able to detail their role, digenean species’ identification and the diversity present in the ecosystems must be known. In this study, the diversity and the temporal-spatial dynamics of larval digeneans in the freshwater snail Heleobia parchappii were analysed in a shallow lake. Specimens of H. parchappii were collected seasonally at three points during one year and a total of 2871 molluscs were analysed. A total of 23 species of digenea were registered and both the overall prevalence and the composition of the assemblages presented temporal and spatial variations, responding to the differential environmental conditions characteristics (anthropic effect, presence of native forests, and differential use of the habitat by the definitive hosts) of three sampled sites. The assemblages of larval digenean in their first intermediate host support the idea that this area is of great importance in biodiversity, and could be endemic areas of some species of digenean that use reptiles, amphibians and bats as hosts, groups that are at risk of conservation. Protection of these environments is a fundamental pillar in the policies for the conservation of wild flora and fauna.

Keywords

Bio-indicatorconservation prioritizationdigenean-snail systemparasite diversitytemporal-spatial dynamics
Type
Research Article
Information
Parasitology , Volume 149 , Issue 3 , March 2022 , pp. 347 - 355
Check for updates
Copyright
Copyright © The Author(s), 2021. 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.)

References

Alda, P and Martorelli, SR (2014) Larval trematodes infecting the South-American intertidal mud snail Heleobia australis (Rissooidea: Cochliopidae). Acta Parasitologica 59, 50–67.CrossRefGoogle Scholar
Barquez, RM, Díaz, MM, Montani, ME and Pérez, MJ (2020) Nueva guía de los murciélagos de Argentina. Publicación Especial, 187 pp.Google Scholar
Byers, JE, Blakeslee, AMH, Linder, E, Cooper, AB and Maguire, TJ (2008) Control of spatial variation in the prevalence of trematode parasites infecting marine snail. Ecology 89, 439–451.CrossRefGoogle Scholar
Byers, JE, Altman, I, Grosse, AM, Huspeni, TC and Maerz, JC (2010) Using parasitic trematode larvae to quantify an elusive vertebrate host. Conservation Biology 25, 85–93.CrossRefGoogle ScholarPubMed
Carlson, CJ, Hopkins, S, Bell, KC, Doña, J, Godfrey, SS, Kwak, ML, Lafferty, D, Moir, ML, Speer, KA, Strona, G, Torchin, M and Wood, CL (2020 a) A global parasite conservation plan. Biological Conservations 250, 108596.CrossRefGoogle Scholar
Carlson, CJ, Dallas, TA, Alexander, LW, Phelan, AL and Phillips, AJ (2020 b) What would it take to describe the global diversity of parasites? Proceedings of the Royal Society B 287, 20201841.CrossRefGoogle ScholarPubMed
Curtis, LA and Hubbard, KM (1990) Trematode infections in a gasteropod host misrepresented by observing shed cercariae. Journal Experimental Marine Biology Ecology 143, 131–137.CrossRefGoogle Scholar
Deblock, S (1977) De l'abrégement du cycle évolutif chez les Trématodes Digènes Microphallidés. Excerta Parasitologica en memoria del Dr Eduardo Caballero y Caballero. Instituto de Biologia, publicationes especiales 4, 151–160.Google Scholar
Duan, Y, Al-Jubury, A, Kania, PW and Buchmann, K (2021) Trematode diversity reflecting the community structure of Danish freshwater systems: molecular clues. Parasites & Vectors 14, 1–15.CrossRefGoogle ScholarPubMed
Dunne, JA, Lafferty, KD, Dobson, AP, Hechinger, RF, Kuris AM, Martinez ND, McLaughlin JP, Mouritsen KN, Poulin P, Reise K, Stouffer DB, Thieltges DW, Williams RJ and Sieter Zander C. (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biology 11, e1001579.CrossRefGoogle ScholarPubMed
Etchegoin, JA (1997) Sistemas parasitarios presentes en la albufera Mar Chiquita (PhD thesis). Mar del Plata, Argentina: Universidad Nacional de Mar del Plata, 84 pp.Google Scholar
Etchegoin, JA and Martorelli, SR (1998) Nuevas cercarias en Heleobia conexa (Mollusca: Hydrobiidae) de la albufera Mar Chiquita. Neotropica 44, 41–50.Google Scholar
Fernández, MV, Hamann, MI and de Núñez M, O (2013) Larval trematodes of Biomphalaria straminea (Mollusca: Planorbidae) in a ricefield in Corrientes Province. Argentina. Revista Mexicana Biodiversidad 84, 756–764.CrossRefGoogle Scholar
Ferrero, L (2001) Avifauna de Mar Chiquita (Síntesis del trabajo de Mariano M. Martínez). In Iribarne, OO (ed.), Reserva de Biosfera Mar Chiquita: Características físicas, biológicas y ecológicas. Mar del Plata: Editorial Martin, pp. 227–250.Google Scholar
Flores, VR, Semenas, LG and Veleizan, AA (2010) Larval digenean community parasitizing the freshwater snail, Biomphalaria peregrina (Pulmonata: Planorbidae), from a temporary pond in Patagonia, Argentina. Journal of Parasitology 96, 652–656.CrossRefGoogle Scholar
Flores, V, Brant, SV and Loker, ES (2015) Avian schistosomes from the South American endemic gastropod genus Chilina (Pulmonata: Chilinidae), with a brief review of South American schistosome species. Journal of Parasitology 101, 565–576.CrossRefGoogle Scholar
Galaktionov, KV and Dobrovolskij, AA (2003) The biology and evolution of trematodes: an essay on the biology, morphology, life cycles, transmission, and evolution of digenetic trematodes. Dordrecht: Kluwer Academic Pub.CrossRefGoogle Scholar
Gehman, ALM, Satterfield, DA, Keogh, CL, McKay, AF and Budischak, SA (2019) To improve ecological understanding, collect infection data. Ecosphere (Washington, DC) 10, e02770.Google Scholar
Haene, E (2006) Caracterización y conservación del talar bonaerense. In Merida, E and Athor, J (eds), Talares bonaerenses y su conservación. Buenos Aires: Universidad Maimónides, pp. 46–70.Google Scholar
Hall, JE (1958) Studies on the biology of the trematode family Lecithodendriidae odhner (PhD thesis), Indiana, EE.UU.: Purdue University, 80 pp.Google Scholar
Hechinger, RF, Lafferty, KD, Huspeni, TC, Brooks, AJ and Kuris, AM (2007) Can parasites be indicators of free-living diversity? Relationships between species richness and the abundance of larval trematodes and of local benthos and fishes. Oecologia 151, 82–92.CrossRefGoogle ScholarPubMed
Huspeni, TC, Hechinger, RF and Lafferty, KD (2005) Trematode parasites as estuarine indicators. In Bortone, SA (ed.), Estuarine Indicators. Boca Ratón: CRC Press, pp. 297–314.Google Scholar
Isla, FI and Gaido, ES (2001) Evolución geológica de la laguna Mar Chiquita. In Iribarne, OO (ed.), Reserva de Biosfera Mar Chiquita: características físicas, biológicas y ecológicas. Mar del Plata: Editorial Martín, pp. 19–30.Google Scholar
Josens, ML, Pretelli, MG and Escalante, AH (2009) Censos de aves acuáticas en sus colonias reproductivas en lagunas del sudeste de la Provincia de Buenos Aires. Hornero 24, 7–12.Google Scholar
Kuris, AM and Lafferty, KD (1994) Community structure: larval trematodes in snail host. Annual Review of Ecology and Systematics 25, 189–217.CrossRefGoogle Scholar
Labriola, J and Suriano, D (2001) Community structure of parasitic helminths of birds of the genus Larus from Mar del Plata, Argentina. Vie et Milieu/Life & Environment 67–76.Google Scholar
Lafferty, KD (1997) Environmental parasitology: what can parasites tell us about human impacts on the environment? Parasitology Today 13, 251–255.CrossRefGoogle ScholarPubMed
Lafferty, KD, Allesina, S, Arim, M, Briggs, CJ, De Leo G, Dobson AP, Dunne JA, Johnson PTJ, Kuris AM, Marcogliese DJ, Martinez ND, Memmott J,Marquet PA, McLaughlin JP, Mordecai EA, Pascual M, Poulin R and Thieltges DW (2008) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.CrossRefGoogle ScholarPubMed
Lindenmeyer, D, Barton, P and Pierson, J (2015) Indicators and Surrogates of Biodiversity and Environmental Change. Australia: CRC Press, 216 pp.CrossRefGoogle Scholar
Lunaschi, L (2002) Tremátodos Lecithodendriidae y Anenterotrematidae de Argentina, México y Brasil. Anales del Instituto de Biología. Serie Zoología 73, 1–10.Google Scholar
Magurran, AE (1988) Ecological Diversity and Its Measurement. Princeton: Princeton University Press, pp. 180.CrossRefGoogle Scholar
Martorelli, SR (1986 a) Estudio sistemático y biológico de un digeneo perteneciente a la familia Microphallidae Travassos, 1920. I: Microphallus szidati sp. nov. parásito intestinal de Rallus sanguinolentus sanguinolentus (Aves: Rallidae) e Himantopus melanurus (Aves: Recurvirostridae). Revista Iberica de Parasitologia 46, 373–378.Google Scholar
Martorelli, SR (1986 b) Estudio sistemático y biológico de un digeneo perteneciente a la familia Microphallidae Travassos, 1920. II: Desarrollo del ciclo biológico de Microphallus szidati en dos ambientes de condiciones ecológicas diferentes. Revista Iberica de Parasitologia 46, 379–385.Google Scholar
Martorelli, SR (1986 c) Estudios parasitológicos en biotopos Iénticos de la República Argentina 1: el ciclo biológico de Echinochasmus talaensis sp. nov. (Digenea) parásita de Pirangurus bolivianus (Aves: Tyrannidae). Neotrópica 31, 187–200.Google Scholar
Martorelli, SR (1988) El ciclo biológico de Levinseniella cruzi Travassos, 1920 (Digenea, Microphallidae) Parásito de los ciegos cólicos de Rollandia rolland chilensis (Aves, Podicipedidae) e Himantopus melanurus (Aves, Recurvirostridae). Iheringia 68, 49–62.Google Scholar
Martorelli, SR (1989) Estudios parasitológicos en biotopos lénticos de la República Argentina y desarrollo del ciclo biológico monoxeno de la metacercaria progenética de Genarchella travassos, 1928 (Digenea, Hemiuridae) parásita Littoridina parchappei (Mollusca, Hidrobiidae). Revista Museo Plata 14, 109–117.Google Scholar
Martorelli, SR and Etchegoin, JA (1996) Cercarias de la superfamilia Opistorchioidea en Heleobia conexa (Mollusca: Hydrobiidae) de la albufera de Mar Chiquita. Neotrópica 42, 61–67.Google Scholar
Merlo, MJ (2014) Ecología de las comunidades de digeneos larvales en hospedadores moluscos del género Heleobia Stimpson, 1865 (Gastropoda: Rissooidea) (PhD thesis). Mar del Plata, Argentina: Universidad Nacional de Mar del Plata, 173 pp.Google Scholar
Merlo, MJ and Etchegoin, JA (2011) Testing temporal stability of the larval digenean community in Heleobia conexa (Mollusca: Cochliopidae) and its possible use as an indicator of environmental fluctuations. Parasitology 138, 249–256.CrossRefGoogle ScholarPubMed
Merlo, MJ, Parietti, M and Etchegoin, JA (2014) Digeneos larvales de Heleobia parchappii y de Heleobia australis en ambientes dulceacuícolas y estuariales de la provincia de Buenos Aires (Argentina). Revista Argentina de Parasitología 2, 14–21.Google Scholar
Merlo, MJ, Parietti, M and Etchegoin, JA (2016) Long-term study of the life cycle of the freshwater snail Heleobia parchappii (Mollusca: Cochliopidae) in a lentic environment in Argentina. Limnetica 35, 49–60.Google Scholar
Merlo, MJ, Parietti, M and Etchegoin, JA (2019) Temporal variations of larval digenean assemblages parasitizing Heleobia parchappii (Mollusca: Cochliopidae) in two shallow lakes from the Buenos Aires province. Argentina. Iheringia. Série Zoologia 109, 1–7.Google Scholar
Milano, AMF (2016) Helmintofauna de murciélagos (Chrioptera) del noreste Argentino (PhD thesis), La Plata, Argentina: Universidad Nacional de La Plata, 168 pp.Google Scholar
Moore, CS, Gittman, RK, Puckett, BJ, Wellman, EH and Blakeslee, AMH (2020) If you build it, they will come: restoration positively influences free-living and parasite diversity in a restored tidal marsh. Food Webs 25, e00167.CrossRefGoogle Scholar
Oksanen, J, Blanchet, FG, Friendly, M, et al. (2016) Vegan: Community Ecology Package. R package version 2.4-3. Vienna: R Foundation for Statistical Computing.Google Scholar
Ostrowski de Nuñez, M (1992) Life history studies of heterophyid trematodes in the Neotropical region: Ascocotyle (Leighia) hadra sp. n. Memorias do Instituto Oswaldo Cruz 87, 539–543.CrossRefGoogle ScholarPubMed
Ostrowski de Nuñez, M (1995) Life history of Pygidiopsis crassus n. sp. (Trematoda, Digenea, Heterophyidae) in the neotropical region. Memórias do Instituto Oswaldo Cruz 90, 13–19.CrossRefGoogle Scholar
Ostrowsky de Nuñez, M, Arredondo, NJ and de Pertierra, AG (2017) Adult trematodes (Platyhelminthes) of freshwater fishes from Argentina: a checklist. Revue suisse de Zoologie 124, 91–113.Google Scholar
Parietti, M, Merlo, MJ and Etchegoin, JA (2013) Can the studies at a spatial scale of 100 s meters detect the spatiotemporal fluctuations of a parasite assemblage? Acta Parasitologia 58, 577–584.Google Scholar
Parietti, M, Merlo, MJ and Etchegoin, JA (2014) Population dynamic of two digenean species parasitizing the grass shrimp Palaemonetes argentinus Nobili 1901 (Decapoda: Palaemonidae) in a lentic environment from Argentina. Acta Parasitologica 60, 124–129.CrossRefGoogle Scholar
Parietti, M, Merlo, MJ and Etchegoin, JA (2020) Spatio-temporal variations in larval digenean assemblages of Heleobia parchappii (Mollusca: Cochliopidae) inhabiting four human-impacted streams. Journal of Helminthology 94, 1–8. doi: 10.1017/S0022149X2000019XCrossRefGoogle ScholarPubMed
Parietti, M, Merlo, MJ and Etchegoin, JA (2021) Effects of droughts on the larval digenean assemblage that parasitizes the snail Biomphalaria peregrina (Planorbidae): a 4-year study in a temporary pond from Argentina. Parasitology Research 120, 1909–1914.CrossRefGoogle Scholar
Poulin, R (2007) Evolutionary Ecology of Parasites. New Jersey: Princeton University, 360 pp.CrossRefGoogle Scholar
Prado, WS, Waller, T, Albareda, DA, Cabrera, MR, Etchepare, EG, Giraudo, AR, González Carman, V, Prosdocimi, L and Richard, D (2012) Categorización del estado de conservación de las tortugas de la República Argentina. Cuadernos de Herpetología 26, 375–388.Google Scholar
Rauque, C, Viozzi, G, Flores, V, Vega, R, Waicheim, A and Salgado-Maldonado, G (2018) Helminth parasites of alien freshwater fishes in Patagonia (Argentina). International Journal for Parasitology: Parasites and Wildlife 7, 369–379.Google Scholar
R Development Core Team (2018) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. Available at https://www.gbif.org/es/tool/81287/r-a-language-and-environment-for-statistical-computing.Google Scholar
Sato, T, Watanabe, K, Kanaiwa, M, Niizuma, Y, Harada Y and Lafferty KD (2011) Nematomorph parasites drive energy flow through a riparian ecosystem. Ecology 92, 201–207.CrossRefGoogle ScholarPubMed
Sosnovsky, A and Quirós, R (2006) El estado trófico de pequeñas lagunas pampeanas, su relación con la hidrología y el uso de la tierra. Ecología Austral 16, 115–124.Google Scholar
Sousa, WP and Grosholz, ED (1991) The influence of habitat structure on the transmission of parasites. Population Community Biological Series , 8, 300–324. doi: 10.1007/978-94-011-3076-9_15Google Scholar
Stellatelli, OA, Block, C, Vega, LE and Cruz, FB (2015) Nonnative vegetation induces changes in predation pressure and escape behavior of two sand lizards (Liolaemidae: Liolaemus). Herpetologica 71, 136–142.CrossRefGoogle Scholar
Szidat, L (1957) Über den Entwicklungszyklus von Psilochasmus oxyurus (Creplin 1825, Lühe 1910) (Trematoda, Psilostomidae) in Argentinien. Zeitschrift für Parasitenkunde 18, 24–35.CrossRefGoogle Scholar
Taglioretti, V, Rossin, MA and Timi, JT (2018) Fish-trematode systems as indicators of anthropogenic disturbance: effects of urbanization on a small stream. Ecological Indicators 93, 759–770.CrossRefGoogle Scholar
Thieltges, DW, Fredensborg, BL and Poulin, R (2009) Geographical variation in metacercarial infection levels in marine invertebrate hosts: parasite species character versus local factors. Marine Biology 156, 983–990.CrossRefGoogle Scholar
Tietze, E and De Francesco, CG (2010) Environmental significance of freshwater mollusks in the Southern Pampas, Argentina: to what detail can local environments be inferred from mollusk composition? Hydrobiologia 641, 133–143.CrossRefGoogle Scholar
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S, 4th Edn. New York: Springer. ISBN 0-387-95457-0.CrossRefGoogle Scholar
Voigt, CC and Kingston, T (2016) Bats in the Anthropocene: Conservation of Bats in a Changing World. London: Springer Nature, 601 pp.CrossRefGoogle Scholar
Yamaguti, S (1975) A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates: With Special Reference to the Morphology of Their Larval Forms. Tokyo: Keigaku Publishing Co, pp. 219.Google Scholar
Zuur, A, Ieno, EN, Walker, N, Saveliev, AA and Smith, GM (2009) Mixed Effects Models and Extensions in Ecology with R. New York, NY, USA: Springer Science & Business Media.CrossRefGoogle Scholar