The Early Worm Catches the Bird? Productivity and Patterns of Trichobilharzia szidati Cercarial Emission from Lymnaea stagnalis

. 2016 ; 11 (2) : e0149678. [epub] 20160219

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid26895541

Digenean trematodes are common and abundant in aquatic habitats and their free-living larvae, the cercariae, have recently been recognized as important components of ecosystems in terms of comprising a significant proportion of biomass and in having a potentially strong influence on food web dynamics. One strategy to enhance their transmission success is to produce high numbers of cercariae which are available during the activity peak of the next host. In laboratory experiments with 13 Lymnaea stagnalis snails infected with Trichobilharzia szidati the average daily emergence rate per snail was determined as 2,621 cercariae, with a maximum of 29,560. During a snail's lifetime this summed up to a mass equivalent of or even exceeding the snail's own body mass. Extrapolated for the eutrophic pond where the snails were collected, annual T. szidati biomass may reach 4.65 tons, a value equivalent to a large Asian elephant. Emission peaks were observed after the onset of illumination, indicating emission synchronizing with the high morning activities of the definitive hosts, ducks. However, high cercarial emission is possible throughout the day under favorable lightning conditions. Therefore, although bird schistosomes, such as T. szidati constitute only a fraction of the diverse trematode communities in the studied aquatic ecosystem, their cercariae can still pose a considerable risk for humans of getting cercarial dermatitis (swimmer's itch) due to the high number of cercariae emitted from infected snails.

Zobrazit více v PubMed

Lafferty KD, Dobson AP, Kuris AM. Parasites dominate food web links. P Natl Acad Sci USA. 2006; 103(30): 11211–11216. PubMed PMC

Lafferty KD, Allesina S, Arim M, Briggs CJ, De Leo G, Dobson AP, et al. Parasites in food webs: the ultimate missing links. Ecol Lett. 2008; 11(6): 533–546. 10.1111/j.1461-0248.2008.01174.x PubMed DOI PMC

Kuris AM, Hechinger RF, Shaw JC, Whitney KL, Aguirre-Macedo L, Boch CA, et al. Ecosystem energetic implications of parasite and free-living biomass in free estuaries. Nature. 2008; 454(7203): 515–518. 10.1038/nature06970 PubMed DOI

Amundsen PA, Lafferty KD, Knudsen R, Primicerio R, Klemetsen A, Kuris AM. Food web topology and parasites in the pelagic zone of a subarctic lake. J Anim Ecol. 2009; 78(3): 563–572. 10.1111/j.1365-2656.2008.01518.x PubMed DOI

Preston DL, Orlofske SA, McLaughlin JP, Johnson PTJ. Food web including infectious agents for a California freshwater pond. Ecology. 2012; 93(7): 1760.

Thieltges DW, Jensen KT, Poulin R. The role biotic factors in the transmission of free-living endohelminth stages. Parasitology. 2008; 135(4): 407–426. 10.1017/S0031182007000248 PubMed DOI

Preston DL, Orlofske SA, Lambden JP, Johnson PTJ. Biomass and productivity of trematode parasites in pond ecosystems. J Animal Ecol. 2013; 82(3): 509–517. PubMed

Hechinger RF, Lafferty KD. Host diversity begets parasite diversity: bird final hosts and trematodes in snail intermediate hosts. P R Soc London. 2005; 272(1567): 1059–1066. PubMed PMC

Hechinger RF, Lafferty KD, Huspeni TC, Brooks AJ, Kuris AM. 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. 2007; 151(1): 82–92. PubMed

Pietrock M, Marcogliese DJ. Free-living endohelminth stages: at the mercy of environmental conditions. Trends Parasitol. 2003; 19(7): 293–299. PubMed

Thieltges DW, de Montaudouin X, Fredensborg B, Jensen K, Koprivnikar J, Poulin R. Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Mar Ecol Prog Ser. 2008; 372: 147–155.

Combes C, Fournier A, Moné H, Théron A. Behaviours in trematode cercariae that enhance parasite transmission: patterns and processes. Parasitology. 1994; 109: S3–S13. PubMed

Poulin R. Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology. 2006; 132(1): 143–151. PubMed

Morley NJ, Lewis JW. Thermodynamics of cercarial development and emergence in trematodes. Parasitology. 2013; 140(10): 1211–1224. 10.1017/S0031182012001783 PubMed DOI

Soldánová M, Selbach C, Kalbe M, Kostadinova A, Sures B. Swimmer’s itch: etiology, impact and risk factors in Europe. Trends Parasitol. 2013; 29(2): 65–74. 10.1016/j.pt.2012.12.002 PubMed DOI

Brant SV, Loker ES. Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends Parasitol. 2013; 29(9): 449–459. 10.1016/j.pt.2013.06.004 PubMed DOI PMC

Horák P, Mikeš L, Lichtenbergová L, Skála, Soldánová M, Brant SV. Avian schistosomes and outbreaks of cercarial dermatitis. Clin Microbiol Rev. 2015; 28(1): 165–190. 10.1128/CMR.00043-14 PubMed DOI PMC

Horák P, Kolářová L, Adema C. Biology of the Schistosome Genus Trichobilharzia. Adv Parasit. 2002; 52: 155–233. PubMed

Horák P, Kolářová L. Bird schistosomes: do they die in mammalian skin? Trends Parasitol. 2001; 17(2): 66–69. PubMed

Horák P, Kolářová L. Molluscan and vertebrate immune responses to bird schistosomes. Parasite Immunol. 2005; 27(7–8): 247–255. PubMed

Horák P, Kolářová L. Snails, waterfowl and cercarial dermatitis. Freshwater Biol. 2011; 56: 779–790.

Neuhaus W. Biologie und Entwicklung von Trichobilharzia szidati n. sp. (Trematoda, Schistosomatidae), einem Erreger von Dermatitis beim Menschen. Parasitol Res. 1952; 15(3): 203–266. PubMed

Anderson PA, Nowosielski JW, Croll NA. The emergence of cercariae of Trichobilharzia ocellata and its relationship to the activity of its snail host Lymnaea stagnalis. Can J Zool. 1976; 54(9): 1481–1487. PubMed

Sluiters JF, Brussaard-Wüst CM, Meuleman EA. The relationship between miracidial dose, production of cercariae, and reproductive activity of the host in the combination Trichobilharzia ocellata and Lymnaea stagnalis. Z Parasitenkd. 1980; 63(1): 13–26. PubMed

Horák P, Kolářová L, Mikeš L. Schistosomatoidea and diplostomoidea. Adv Exp Med Biol. 2014; 766: 331–364. 10.1007/978-1-4939-0915-5_10 PubMed DOI

Studer A, Poulin R. Differential effects of temperature variability on the transmission of a marine parasite. Mar Biol. 2013; 160(10): 2763–2773.

Żbikowska E, Kobak J, Żbikowski J, Kąklewski J. Infestation of Lymnaea stagnalis by digenean flukes in the Jeziorak Lake. Parasitol Res. 2006; 99(4): 434–439. PubMed

Brassard P, Curtis MA, Rau ME. Seasonality of Diplostomum spathaceum (Trematoda: Strigeidae) transmission to brook trout (Salvelinus fontinalis) in northern Quebec, Canada. Can J Zoolog. 1982; 60(10): 2258–2263.

Taskinen J. Cercarial production of the trematode Rhipidocotyle fennica in clams kept in the field. J Parasitol. 1998; 84(2): 345–349. PubMed

Abràmoff MD, Magalhães PJ, Ram SJ. Image processing with ImageJ. Biophotonics Int. 2004; 11(7): 36–42.

Koehler AV, Brown B, Poulin R, Thieltges DW, Fredensborg BL. Disentangling phylogenetic constraints from selective forces in the evolution of trematode transmission stages. Evol Ecol. 2012; 26(6): 1497–1512.

Glöer P. Die Süßwassergastropoden Nord- und Mitteleuropas—Bestimmungschlüssel, Lebensweise, Verbreitung. Hackenheim: ConchBooks; 2002.

Galaktionov K, Dobrovolskij A. The Biology and Evolution of Trematodes: An Essay on the Biology, Morphology, Life Cycles, Transmissions, and Evolution of Digenetic Trematodes. Dordrecht: Kluwer Academic Publishers; 2003.

Esch GW, Fernández JC. Snail-trematode interactions and parasite community dynamics in aquatic systems: A review. Am Midl Nat. 1994; 131(2): 209–237.

Soldánová M, Kostadinova A. Rapid colonisation of Lymnaea stagnalis by larval trematodes in eutrophic ponds in central Europe. Int J Parasitol. 2011; 41(9): 981–990. 10.1016/j.ijpara.2011.05.005 PubMed DOI

Jurkiewicz-Karnkowska E. Aquatic molluscs communities in riparian sites of different size, hydrological connectivity and succession stage. Pol J Ecol. 2008; 56(1): 99–118.

Soldánová M, Faltýnková A, Scholz T, Kostadinova A. Parasites in a man-made landscape: contrasting patterns of trematode flow in a fishpond area in central Europe. Parasitology. 2011; 138(6): 789–807. 10.1017/S0031182011000291 PubMed DOI

Żbikowska E, Franckiewicz-Grygon B, Wójcik AR. Przypadek dermatitis u czlowieka wywolany przez cerkarie ptasich schistosom. [The case of dermatitis in the human as a result of the influence of the cercaria of the bird schistosome.] Wiad Parasitol. 2001; 47(3): 427–431. PubMed

Rudolfová J, Hampl V, Bayssade-Dufour C, Lockyer AE, Littlewood DT, Horák P. Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol Res. 2005; 95(2): 79–89. PubMed

Théron A. Dynamics of larval populations of Schistosoma mansoni in Biomphalaria glabrata. I. Rhythmic production of cercariae in monomiracidial infections. Ann Trop Med Parasit. 1981; 75(1): 71–77. PubMed

Théron A. Dynamics of larval populations of Schistosoma mansoni in Biomphalaria glabrata. II. Chronobiology of the intramolluscan larval development during the shedding period. Ann Trop Med Parasit. 1981; 75: 547–554. PubMed

Toledo R, Munoz-Antoli C, Esteban JG. Production and chronobiology of emergence of the cercariae of Euparyphium albuferensis (Trematoda: Echinostomatidae). J Parasitol. 1999; 85(2): 263–267. PubMed

Selbach C, Soldánová M, Sures B. Estimating the risk of swimmer’s itch in surface waters–a case study from Lake Baldeney, the Ruhr River. Int J Hyg Environ Health. 2015; In press. PubMed

Soldánová M, Kuris AM, Scholz T, Lafferty KD. The role of spatial and temporal heterogeneity and competition in structuring trematode communities in the great pond snail, Lymnaea stagnalis (L.). J Parasitol. 2012; 98(3): 460–471. 10.1645/GE-2964.1 PubMed DOI

Poulin R, George-Nascimento M. The scaling of total parasite biomass with host body mass. Int J Parasitol. 2007; 37(3–4): 359–364. PubMed

Hechinger RF. A metabolic and body-size scaling framework for parasite within-host abundance, biomass, and energy flux. Am Nat. 2013; 182(2): 234–248. 10.1086/670820 PubMed DOI

Hechinger RF, Lafferty KD, Mancini FT, Warner RR, Kuris AM. How large is the hand in the puppet? Ecological and evolutionary factors affecting body mass of 15 trematode parasitic castrators in their snail host. Evol Ecol. 2009; 23(5): 651–667.

Hudson PJ. Parasites, diversity and the ecosystem In: Thomas F, Reanud TF, Guegan JF, editors. Parasitism & Ecosystems. Oxford: Oxford University Press; 2005. pp 1–12.

Finch CE, Roth GS. Biochemistry of Aging In: Siegel GJ, Agranoff BW, Albers RW, Fisher SK, Uhler MD, editors. Basic Neurochemistry—Molecular, Cellular and Medical Aspects. Philadelphia: Lippincott-Raven; 1999. pp. 613–636.

Loy C, Haas W. Prevalence of cercariae from Lymnaea stagnalis snails in a pond system in Southern Germany. Parasitol Res. 2001; 87(10): 878–882. PubMed

Soldánová M. Selbach C. Sures B, Kostadinova A, Pérez-del-Olmo A. Larval trematode communities in Radix auricularia and Lymnaea stagnalis in a reservoir system of the Ruhr River. Parasite Vectors. 2010; 3(1): 56. PubMed PMC

Lyholt HCK, Buchmann K. Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Dis Aquat Organ. 1996; 25: 169–173.

Karvonen A, Kirsi S, Hudson PJ, Valtonen ET. Patterns of cercarial production from Diplostomum spathaceum: terminal investment or bet hedging? Parasitology. 2004; 129(1): 87–92. PubMed

Haas W. Parasitic worms: strategies of host finding, recognition and invasion. Zoology (Jena). 2003; 106(4): 349–364. PubMed

Brown R, Soldánová M, Barrett J, Kostadinova A. Small-scale to large scale and back: larval trematodes in Lymnaea stagnalis and Planorbarius corneus in Central Europe. Parasitol Res. 2011; 108(1):137–150. 10.1007/s00436-010-2047-z PubMed DOI

Zikmundová J, Georgieva S, Faltýnková A, Soldánová M, Kostadinova A. Species diversity of Plagiorchis Lűhe, 1899 (Digena: Plagiorchiidae) in lymnaeid snails from freshwater ecosystems in central Europe revealed by molecules and morphology. Syst Parasitol. 2014; 88(1): 37–54. 10.1007/s11230-014-9481-8 PubMed DOI

Johnson PTJ, Dobson A, Lafferty KD, Marcogliese DJ, Memmott J, Orlofske SA, et al. When parasites become prey: ecological and epidemiological significance of eating parasites. Trends Ecol Evol. 2010; 25(6): 362–371. 10.1016/j.tree.2010.01.005 PubMed DOI

Morley NJ. Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia. 2012; 691(1):7–19.

Thieltges DW, Amundsen PA, Hechinger RF, Johnson PTJ, Lafferty KD, Mouritsen KN, et al. Parasites as prey in aquatic food webs: Implications for predator infection and parasite transmission. Oikos. 2013; 122(10): 1473–1482.

Welsh JE, van der Meer J, Brussaard CPD, Thieltges DW. Inventory of organisms interfering with transmission of a marine trematode. J Mar Biol Assoc U.K. 2014; 94(4): 697–702.

Kuris AM. Guild structure of larval trematodes in molluscan hosts: prevalence, dominance and significance of competition In: Esch GW, Bush AO, Aho JM, editors. Parasite communities: Patterns and Processes. London: Chapman & Hall; 1990. pp. 69–100.

Sauter A, Korner P, Fiedler W, Jenni L. Individual behavioural variability of an ecological generalist: activity patterns and local movements of Mallards Anas platyrhynchos in winter. J Ornithol. 2011; 153(3): 713–726.

Théron A, Mouahid G, Moné H. Schistosoma mansoni: Cercarial shedding patterns from a mixed infection of Biomphalaria glabrata with two (early and late) chronobiological variants. Parasitol Res. 1997; 83(4): 356–358. PubMed

Pagess JR, Théron A. Analysis and comparison of cercarial emergence rhythms of Schistosoma haematobium, S. intercalatum and S. bovis and their hybrid progeny. Int J Parasitol. 1990; 20(2): 193–197. PubMed

N‘goran E, Bremond P, Sellin E, Sellin B, Théron A. Intraspecific diversity of Schistosoma haematobium in West Africa: chronobiology of cercarial emergence. Acta Trop. 1997; 66(1): 35–44. PubMed

Verbrugge LM, Rainey JJ, Reimink RL, Blankespoor HD. Prospective study of swimmer’s itch incidence and severity. J Parasitol. 2004; 90(4): 697–704. PubMed

Lindblade KA. The epidemiology of cercarial dermatitis and its association with limnological characteristics of a northern Michigan lake. J Parasitol. 1998; 84(1): 19–23. PubMed

Horsák M, Juřičková L, Picka J. Měkkýši České a Slovenské Republiky Molluscs of the Czech and Slovak Republics. Zlín: Kabourek; 2013.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Other Schistosomatoidea and Diplostomoidea

. 2024 ; 1454 () : 107-155.

Cercariae of a Bird Schistosome Follow a Similar Emergence Pattern under Different Subarctic Conditions: First Experimental Study

. 2022 Jun 03 ; 11 (6) : . [epub] 20220603

Somatic Dimorphism in Cercariae of a Bird Schistosome

. 2022 Feb 24 ; 11 (3) : . [epub] 20220224

Temperature does not influence functional response of amphipods consuming different trematode prey

. 2020 Dec ; 119 (12) : 4271-4276. [epub] 20200826

Confirmation of the presence of zoonotic Trichobilharzia franki following a human cercarial dermatitis outbreak in recreational water in Slovakia

. 2020 Aug ; 119 (8) : 2531-2537. [epub] 20200620

The chemotactic swimming behavior of bird schistosome miracidia in the presence of compatible and incompatible snail hosts

. 2020 ; 8 () : e9487. [epub] 20200716

Hidden parasite diversity in a European freshwater system

. 2020 Feb 14 ; 10 (1) : 2694. [epub] 20200214

Cercarial dermatitis: a systematic follow-up study of human cases with implications for diagnostics

. 2018 Dec ; 117 (12) : 3881-3895. [epub] 20181009

Impact of trematode infections on periphyton grazing rates of freshwater snails

. 2018 Nov ; 117 (11) : 3547-3555. [epub] 20180901

Potamopyrgus antipodarum as a potential defender against swimmer's itch in European recreational water bodies-experimental study

. 2018 ; 6 () : e5045. [epub] 20180625

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace