Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T08:27:25.616Z Has data issue: false hasContentIssue false
  • English
  • Français

Allee effect in a manipulative parasite within poikilothermic host under temperature change

Published online by Cambridge University Press:  09 September 2021

Ekaterina Mironova Open the ORCID record for Ekaterina Mironova [Opens in a new window] ,
Mikhail Gopko Open the ORCID record for Mikhail Gopko [Opens in a new window] ,
Anna Pasternak ,
Viktor Mikheev  and
Jouni Taskinen Open the ORCID record for Jouni Taskinen [Opens in a new window]
Ekaterina Mironova*
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskij prosp., 33, 119071 Moscow, Russia
Mikhail Gopko
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskij prosp., 33, 119071 Moscow, Russia
Anna Pasternak
Affiliation:
Shirshov Institute of Oceanology, Russian Academy of Sciences, Nahimovskiy prosp., 36, 117997 Moscow, Russia
Viktor Mikheev
Affiliation:
A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskij prosp., 33, 119071 Moscow, Russia
Jouni Taskinen
Affiliation:
Department of Biological and Environmental Science, University of Jyväskylä, P.O. Box 35, FIN-40014 Jyväskylä, Finland
*
Author for correspondence: Ekaterina Mironova, E-mail: katya_mironova@mail.ru
Get access Rights & Permissions [Opens in a new window]

Abstract

Temperature and intraspecific competition are important factors influencing the growth of all organisms, including parasites. The temperature increase is suggested to stimulate the development of parasites within poikilothermic hosts. However, at high parasite densities, this effect could be diminished, due to stronger intraspecific competition. Our study, for the first time, addressed the joint effects of warming and parasite abundances on parasite growth in poikilothermic hosts. The growth of the common fish parasite larvae (trematode Diplostomum pseudospathaceum) within the rainbow trout at different infection intensities and temperatures (15°C and 18°C) was experimentally investigated. The results showed that temperature was positively correlated with both parasite infection success and growth rates. The growth rates increased much more compared to those in many free-living poikilothermic animals. Atypically for a majority of parasites, D. pseudospathaceum larvae grow faster when abundant (Allee effect). The possible causes for this phenomenon (manipulation cost sharing, etc.) are discussed in this study. Importantly, limited evidence of the interaction between temperature and population density was found. It is likely that temperature did not change the magnitude of the Allee effect but affected its timing. The impact of these effects is supposed to become more pronounced in freshwater ecosystems under current climate changes.

Keywords

Crowding effectDiplostomum pseudospathaceumeye flukeinfection intensitiesmetacercariaeOncorhynchus mykissparasite growthsize variationthermal response
Type
Research Article
Information
Parasitology , Volume 149 , Issue 1 , January 2022 , pp. 35 - 43
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.)

Footnotes

*

These authors contributed equally to this work

References

Adamo, SA (2012) The strings of the puppet master: how parasites change host behavior. In Hughes, DP, Brodeur, J and Thomas, F (eds), Host Manipulation by Parasites. Oxford, UK: Oxford University Press, pp. 36–53.10.1093/acprof:oso/9780199642236.003.0003CrossRefGoogle Scholar
Angulo, E, Luque, GM, Gregory, SD, Stephen, DG, Wenzel, JW, Bessa-Gomes, C, Berec, L and Courchamp, F (2018) Allee effects in social species. Journal of Animal Ecology 87, 47–58.CrossRefGoogle ScholarPubMed
Auguie, B (2017) gridExtra: Miscellaneous Functions for ‘Grid’ Graphics. R package version 2.3. Available at https://CRAN.R-project.org/package=gridExtra.Google Scholar
Barber, I, Berkhout, BW and Ismail, Z (2016) Thermal change and the dynamics of multi-host parasite life cycles in aquatic ecosystems. Integrative and Comparative Biology 56, 561–572.CrossRefGoogle ScholarPubMed
Bashey, F (2015) Within-host competitive interactions as a mechanism for the maintenance of parasite diversity. Philosophical Transactions of the Royal Society B 370, 20140301.10.1098/rstb.2014.0301CrossRefGoogle ScholarPubMed
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Brown, SP (1999) Cooperation and conflict in host-manipulating parasites. Proceedings of the Royal Society B 266, 1899–1904.CrossRefGoogle Scholar
Brown, SP, De Lorgeril, J, Joly, C and Thomas, F (2003) Field evidence for density-dependent effects in the trematode Microphallus papillorobustus in its manipulated host, Gammarus insensibilis. Journal of Parasitology 89, 668–672.10.1645/GE-3122CrossRefGoogle ScholarPubMed
Bush, AO and Lotz, JM (2000) The ecology of ‘crowding’. Journal of Parasitology 86, 212–213.Google ScholarPubMed
Cable, J, Barber, I, Boag, B, Ellison, AR, Morgan, ER, Murray, K, Pascoe, EL, Sait, SM, Wilson, AJ and Booth, M (2017) Global change, parasite transmission and disease control: lessons from ecology. Philosophical Transactions of the Royal Society B 372, 20160088.10.1098/rstb.2016.0088CrossRefGoogle ScholarPubMed
Chubb, JC (1977) Seasonal occurrence of helminths in freshwater fishes. Part I. Monogenea. Advances in Parasitology 15, 133–199.10.1016/S0065-308X(08)60528-XCrossRefGoogle ScholarPubMed
Chubb, JC (1979) Seasonal occurrence of helminths in freshwater fishes. Part II. Trematoda. Advances in Parasitology 17, 142–313.Google Scholar
Chubb, JC (1980) Seasonal occurrence of helminths in freshwater fishes. Part III. Larval Cestoda and Nematoda. Advances in Parasitology 18, 1–120.CrossRefGoogle ScholarPubMed
Coutant, CC (1977) Compilation of temperature preference data. Journal of the Fisheries Research Board of Canada 34, 739–745.CrossRefGoogle Scholar
Dittmar, J, Janssen, H, Kuske, A, Kurtz, J and Scharsack, JP (2014) Heat and immunity: an experimental heat wave alters immune functions in three-spined sticklebacks (Gasterosteus aculeatus). Journal of Animal Ecology 83, 744–757.CrossRefGoogle ScholarPubMed
Eaton, JG, McCormick, JH, Goodno, BE, O'Brien, DG, Stefan, HG, Hondzo, M and Scheller, RM (1995) A field information-based system for estimating fish temperature tolerances. Fisheries 20, 10–18.10.1577/1548-8446(1995)020<0010:AFISFE>2.0.CO;22.0.CO;2>CrossRefGoogle Scholar
Fong, C, Moron, N and Kuris, A (2017) Two's a crowd? Crowding effect in a parasitic castrator drives differences in reproductive resource allocation in single vs double infections. Parasitology 144, 662–668.10.1017/S003118201600233XCrossRefGoogle Scholar
Franke, F, Armitage, SAO, Kutzer, MAM, Kurtz, J and Scharsack, JP (2017) Environmental temperature variation influences fitness trade-offs and tolerance in a fish-tapeworm association. Parasites & Vectors 10, 252.10.1186/s13071-017-2192-7CrossRefGoogle Scholar
Fredensborg, BL and Poulin, R (2005) Larval helminths in intermediate hosts: does competition early in life determine the fitness of adult parasites? International Journal for Parasitology 35, 1061–1070.CrossRefGoogle ScholarPubMed
Gopko, M, Mikheev, VN and Taskinen, J (2015) Changes in host behaviour caused by immature larvae of the eye fluke: evidence supporting the predation suppression hypothesis. Behavioral Ecology and Sociobiology 69, 1723–1730.CrossRefGoogle Scholar
Gopko, M, Mikheev, VN and Taskinen, J (2017 a) Positive density-dependent growth supports costs sharing hypothesis and population density sensing in a manipulative parasite. Parasitology 144, 1511–1518.CrossRefGoogle Scholar
Gopko, M, Mikheev, VN and Taskinen, J (2017 b) Deterioration of basic components of the anti-predator behavior in fish harboring eye fluke larvae. Behavioral Ecology and Sociobiology 71, 68.CrossRefGoogle Scholar
Gopko, M, Mironova, E, Pasternak, A, Mikheev, V and Taskinen, J (2020) Parasite transmission in aquatic ecosystems under temperature change: effects of host activity and elimination of parasite larvae by filter-feeders. Oikos 129, 1531–1540.10.1111/oik.07414CrossRefGoogle Scholar
Hafer-Hahmann, N (2019) Experimental evolution of parasitic host manipulation. Proceedings of the Royal Society B 286, 20182413.CrossRefGoogle ScholarPubMed
Hakalahti, T, Karvonen, A and Valtonen, ET (2006) Climate warming and disease risks in temperate regions – Argulus coregoni and Diplostomum spathaceum as case studies. Journal of Helminthology 80, 93–98.CrossRefGoogle ScholarPubMed
Harvell, CD, Mitchell, C, Ward, J, Altizer, S, Dobson, A, Ostfeld, R and Samuel, M (2002) Climate warming and disease risks for terrestrial and marine biota. Science (New York, N.Y.) 296, 2158–2162.CrossRefGoogle ScholarPubMed
Heins, DC, Baker, JA and Martin, HC (2002) The ‘crowding effect’ in the cestode Schistocephalus solidus: density-dependent effects on plerocercoid size and infectivity. Journal of Parasitology 88, 302–307.Google ScholarPubMed
Höglund, J and Thuvander, A (1990) Indications of nonspecific protective mechanisms in rainbow trout Oncorhynchus mykiss with diplostomosis. Diseases of Aquatic Organisms 8, 91–97.10.3354/dao008091CrossRefGoogle Scholar
Holmes, JC (1961) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). I. General effects and comparison with crowding. Journal of Parasitology 47, 209–216.10.2307/3275291CrossRefGoogle ScholarPubMed
Holmes, JC (1962) Effects of concurrent infections on Hymenolepis diminuta (Cestoda) and Moniliformis dubius (Acanthocephala). II. Effects on growth. Journal of Parasitology 48, 87–96.10.2307/3275418CrossRefGoogle ScholarPubMed
Jones, AW and Tan, BD (1971) Effect of crowding upon growth and fecundity in the mouse bile duct tapeworm, Hymenolepis microstoma. Journal of Parasitology 57, 88–93.10.2307/3277757CrossRefGoogle Scholar
Karvonen, A, Seppälä, O and Valtonen, ET (2004) Eye fluke-induced cataract formation in fish: quantitative analysis using an ophthalmological microscope. Parasitology 129, 473–478.CrossRefGoogle ScholarPubMed
Kuha, J, Arvola, L, Hanson, P, Huotari, J, Huttula, T, Juntunen, J, Järvinen, M, Kallio, K, Ketola, M, Kuoppamäki, K, Lepistö, A, Lohila, A, Paavola, R, Vuorenmaa, J, Winslow, L and Karjalainen, J (2016) Response of boreal lakes to episodic weather-induced events. Inland Waters 6, 523–534.10.1080/IW-6.4.886CrossRefGoogle Scholar
Kuris, AM (2003) Evolutionary ecology of trophically transmitted parasites. Journal of Parasitology 89, 96–100.Google Scholar
Kuznetsova, A, Brockhoff, PB and Christensen, RHB (2017) lmerTest package: tests in linear mixed effects models. Journal of Statistical Software 82, 1–26.CrossRefGoogle Scholar
Lafferty, KD and Morris, AK (1996) Altered behavior of parasitized killifish increases susceptibility to predation by bird final hosts. Ecology 77, 1390–1397.CrossRefGoogle Scholar
Lv, S, Zhou, X, Zhang, Y, Liu, H, Zhu, D, Yin, W, Steinmann, P, Wang, X and Jia, T (2006) The effect of temperature on the development of Angiostrongylus cantonensis (Chen 1935) in Pomacea canaliculata (Lamarck 1822). Parasitology Research 99, 583–587.10.1007/s00436-006-0198-8CrossRefGoogle ScholarPubMed
Lyholt, H and Buchmann, K (1996) Diplostomum spathaceum: effects of temperature and light on cercarial shedding and infection of rainbow trout. Diseases of Aquatic Organisms 25, 169–173.CrossRefGoogle Scholar
Macnab, V and Barber, I (2012) Some (worms) like it hot: fish parasites grow faster in warmer water, and alter host thermal preferences. Global Change Biology 18, 1540–1548.CrossRefGoogle Scholar
Marcogliese, DJ (2001) Implications of climate change for parasitism of animals in the aquatic environment. Canadian Journal of Zoology 79, 1331–1352.CrossRefGoogle Scholar
Marcogliese, DJ (2016) The distribution and abundance of parasites in aquatic ecosystems in a changing climate: more than just temperature. Integrative Comparative Biology 56, 611–619.CrossRefGoogle Scholar
Mikheev, VN, Pasternak, AF, Taskinen, J and Valtonen, ET (2010) Parasite-induced aggression and impaired contest ability in a fish host. Parasites & Vectors 3, 17.CrossRefGoogle Scholar
Morley, NJ (2012) Thermodynamics of miracidial survival and metabolism. Parasitology 139, 1640–1651.CrossRefGoogle ScholarPubMed
Morley, NJ and Lewis, JW (2013) Thermodynamics of cercarial development and emergence in trematodes. Parasitology 140, 1211–1224.10.1017/S0031182012001783CrossRefGoogle ScholarPubMed
Niewiadomska, K (1986) Verification of the life-cycles of Diplostomum spathaceum (Rudolphi, 1819) and D. pseudospathaceum Niewiadomska, 1984 (Trematoda, Diplostomidae). Systematic Parasitology 8, 23–31.CrossRefGoogle Scholar
Parker, GA, Ball, MA and Chubb, JC (2015) Evolution of complex life cycles in trophically transmitted helminths. II. How do life-history stages adapt to their hosts? Journal of Evolutionary Biology 28, 292–304.CrossRefGoogle ScholarPubMed
Paull, SH, Raffel, TR, LaFonte, BE and Johnson, PTJ (2015) How temperature shifts affect parasite production: testing the roles of thermal stress and acclimation. Functional Ecology 29, 941–950.CrossRefGoogle Scholar
Poulin, R (1994) The evolution of parasite manipulation of host behavior – a theoretical analysis. Parasitology 109, 109–118.CrossRefGoogle ScholarPubMed
Poulin, R (2006) Global warming and temperature-mediated increases in cercarial emergence in trematode parasites. Parasitology 132, 143–151.CrossRefGoogle ScholarPubMed
Poulin, R, Giari, L, Simoni, E and Dezfuli, B (2003) Effects of conspecifics and heterospecifics on individual worm mass in four helminth species parasitic in fish. Parasitology Research 90, 143–147.10.1007/s00436-002-0778-1CrossRefGoogle ScholarPubMed
R Core Team (2019) R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/.Google Scholar
Read, CP (1951) The crowding effect in tapeworm populations. Journal of Parasitology 37, 174–178.CrossRefGoogle Scholar
Rellstab, C, Louhi, KR, Karvonen, A and Jokela, J (2011) Analysis of trematode parasite communities in fish eye lenses by pyrosequencing of naturally pooled DNA. Infection, Genetics and Evolution 11, 1276–1286.CrossRefGoogle ScholarPubMed
Saldanha, I, Leung, T and Poulin, R (2009) Causes of intraspecific variation in body size among trematode metacercariae. Journal of Helminthology 83, 289–293.CrossRefGoogle ScholarPubMed
Sandland, G and Goater, C (2000) Development and intensity dependence of Ornithodiplostomum ptychocheilus metacercariae in fathead minnows (Pimephales promelas). The Journal of Parasitology 86, 1056–1060.10.1645/0022-3395(2000)086[1056:DAIDOO]2.0.CO;2CrossRefGoogle ScholarPubMed
Schmidt-Nielsen, K (1997) Animal Physiology: Adaptation and Environment. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Seppälä, O, Karvonen, A and Valtonen, ET (2004) Parasite-induced change in host behaviour and susceptibility to predation in an eye fluke–fish interaction. Animal Behavior 68, 257–263.10.1016/j.anbehav.2003.10.021CrossRefGoogle Scholar
Seppälä, O, Karvonen, A and Valtonen, ET (2005) Manipulation of fish host by eye flukes in relation to cataract formation and parasite infectivity. Animal Behavior 70, 889–894.CrossRefGoogle Scholar
Seppälä, O, Karvonen, A and Valtonen, ET (2012) Behavioural mechanisms underlying ‘specific’ host manipulation by a trophically transmitted parasite. Evolutionary Ecology Research 14, 73–81.Google Scholar
Sharma, S, Gray, DK, Read, JS, O'Reilly, CM, Schneider, P, Qudrat, A, Gries, C, Stefanoff, S, Hampton, SE, Hook, S, Lenters, JD, Livingstone, DM, McIntyre, PB, Adrian, R, Allan, MG, Anneville, O, Arvola, L, Austin, J, Bailey, J and Woo, KH (2015) A global database of lake surface temperatures collected by in situ and satellite methods from 1985–2009. Scientific Data 2, 150008.CrossRefGoogle ScholarPubMed
Shigin, A (1986) Trematody Fauny SSSR. Rod Diplostomum. Metacercarii. Moskva: Nauka (in Russian).Google Scholar
Sinha, D and Hopkins, C (1967) Studies on Schistocephalus solidus: 4. The effect of temperature on growth and maturation in vitro. Parasitology 57, 555–566.10.1017/S0031182000072437CrossRefGoogle ScholarPubMed
Stephens, PA and Sutherland, WJ (1999) Consequences of the Allee effect for behaviour, ecology and conservation. Trends in Ecology & Evolution 14, 401–405.CrossRefGoogle ScholarPubMed
Stephens, PA, Sutherland, WJ and Freckleton, RP (1999) What is the Allee effect? Oikos 87, 185–190.CrossRefGoogle Scholar
Studer, A, Thieltges, DW and Poulin, R (2010) Parasites and global warming: net effects of temperature on an intertidal host-parasite system. Marine Ecology Progress Series 415, 11–22.10.3354/meps08742CrossRefGoogle Scholar
Stumbo, AD and Poulin, R (2016) Possible mechanism of host manipulation resulting from a diel behaviour pattern of eye-dwelling parasites? Parasitology 143, 1261–1267.10.1017/S0031182016000810CrossRefGoogle ScholarPubMed
Sweeting, RA (1974) Investigations into natural and experimental infections of freshwater fish by the common eye-fluke Diplostomum spathaceum Rud. Parasitology 69, 291–300.10.1017/S0031182000062995CrossRefGoogle ScholarPubMed
Tokeson, J and Holmes, JC (1982) The effects of temperature and oxygen on the development of Polymorphus marilis (Acanthocephala) in Gammarus lacustris (Amphipoda). Journal of Parasitology 68, 112.CrossRefGoogle Scholar
Valtonen, ET and Gibson, DI (1997) Aspects of the biology of diplostomid metacercarial (Digenea) populations occurring in fishes in different localities of northern Finland. Annales Zoologici Fennici 34, 47–59.Google Scholar
Valtonen, ET, Holmes, JC and Koskivaara, M (1997) Eutrophication, pollution, and fragmentation: effects on the parasite communities in roach (Rutilus rutilus) and perch (Perca fluviatilis) in four lakes in central Finland. Canadian Journal of Fisheries and Aquatic Sciences 54, 572–585.10.1139/f96-306CrossRefGoogle Scholar
Vernberg, WB (1968) Platyhelminthes: respiratory metabolism. In Florkin, M and Scheer, BT (eds), Chemical Zoology: Porifera, Coelenterata, and Platyhelminthes. New York, USA and London: Academic Press, pp. 359–394.10.1016/B978-0-12-395535-7.50022-XCrossRefGoogle Scholar
Voutilainen, A, Taskinen, J and Huuskonen, H (2010) Temperature-dependent effect of the trematode eye flukes Diplostomum spp. on the growth of Arctic charr Salvelinus alpinus (L.). Bulletin of the European Association of Fish Pathologists 30, 106–113.Google Scholar
Walther, G, Post, E, Convey, P, Menzel, A, Parmesan, C, Beebee, T, Fromentin, J, Hoegh-Guldberg, O and Bairlein, F (2002) Ecological responses to recent climate change. Nature 416, 389–395.CrossRefGoogle ScholarPubMed
Wegner, KM, Kalbe, M and Reusch, TBH (2007) Innate versus adaptive immunity in sticklebacks: evidence for trade-offs from a selection experiment. Evolutionary Ecology 21, 473–483.CrossRefGoogle Scholar
Weinersmith, K, Warinner, C, Tan, V, Harris, D, Mora, A, Kuris, A, Lafferty, K and Hechinger, R (2014) A lack of crowding? Body size does not decrease with density for two behavior-manipulating parasites. Integrative and Comparative Biology 54, 184–192.CrossRefGoogle Scholar
Wickham, H (2016) ggplot2: Elegant Graphics for Data Analysis. New York, USA: Springer-Verlag.CrossRefGoogle Scholar
Wikgren, B-JP (1966) The effect of temperature on the cell division cycle in diphyllobothrid plerocercoids. Acta Zoologica Fennica 114, 1–27.Google Scholar
Yao, G, Huffman, JE and Fried, B (1991) The effects of crowding on adults of Echinostoma caproni in experimentally infected golden hamsters. Journal of Helminthology 65, 248–254.CrossRefGoogle ScholarPubMed