Skip to main content Accessibility help
×
Home
Hostname: page-component-684bc48f8b-b5g75 Total loading time: 0.42 Render date: 2021-04-11T13:54:13.397Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": false, "newCiteModal": false, "newCitedByModal": true }

Are solo infections of the diphyllobothriidean cestode Schistocephalus solidus more virulent than multiple infections?

Published online by Cambridge University Press:  20 June 2018

David C. Heins
Affiliation:
Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA
Kristine N. Moody
Affiliation:
Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA
Sophia Miller
Affiliation:
Department of Ecology and Evolutionary Biology, Tulane University, New Orleans, LA 70118, USA
Corresponding
E-mail address:

Abstract

We performed a long-term natural experiment investigating the impact of the diphyllobotriidean cestode Schistocephalus solidus on the body condition and clutch size (CS) of threespine stickleback Gasterosteus aculeatus, its second intermediate host, and the growth of larval parasites in host fish. We tested the hypothesis that single S. solidus infections were more virulent than multiple infections. We also asked whether the metrics of mean and total parasite mass (proxies for individual and total volume, respectively) were consistent with predictions of the resource constraints or the life history strategy (LHS) hypothesis for the growth of, hence exploitation by, larval helminths in intermediate hosts. The samples were drawn from Walby Lake, Alaska in eight of 11 years. Host body condition and CS (egg number per spawning bout) decreased significantly with intensity after adjustments for host size and parasite index. Thus, infections have an increasingly negative impact on measures of host fitness with greater intensity, in contrast to the hypothesis that single infections are more harmful than multiple infections. We also found that mean parasite mass decreased with intensity while total parasite mass increased with intensity as predicted by the LHS hypothesis.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below.

Footnotes

*

Present address: Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, TN 37996, USA.

References

Arme, C and Owen, RW (1967) Infections of the three-spined stickleback, Gasterosteus aculeatus L., with the plerocercoid larvae of Schistocephalus solidus (Muller, 1776), with special reference to pathological effects. Parasitology 57, 301314.CrossRefGoogle Scholar
Bagamian, KH, Heins, DC and Baker, JA (2004) Body condition and reproductive capacity of three-spined stickleback infected with the cestode Schistocephalus solidus. Journal of Fish Biology 64, 15681576.CrossRefGoogle Scholar
Baker, JA and Heins, DC (1994) Effect of drying temperature on weight estimates for oocytes and eggs in the darter Etheostoma lynceum. Copeia 1994, 821823.CrossRefGoogle Scholar
Baker, JA, Foster, SA, Heins, DC, Bell, MA and King, RW (1998) Variation in female life-history traits among Alaskan populations of the threespine stickleback, Gasterosteus aculeatus L. (Pisces: Gasterosteidae). Biological Journal of the Linnean Society 63, 141159.Google Scholar
Bakker, TCM and Mundwiler, B (1994) Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population. Behavioral Ecology 5, 7480.CrossRefGoogle Scholar
Barber, I (2005) Parasites grow larger in faster growing fish hosts. International Journal for Parasitology 35, 137143.CrossRefGoogle ScholarPubMed
Brown-Peterson, NJ and Heins, DC (2009) Interspawning interval of wild female three-pined stickleback Gasterosteus aculeatus in Alaska. Journal of Fish Biology 74, 22992312.CrossRefGoogle ScholarPubMed
Christen, M and Milinski, M (2003) The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host. Parasitology 126, 369378.CrossRefGoogle ScholarPubMed
Clayton, DH and Moore, J (eds.) (1997) Introduction. Host–Parasite Evolution: General Principles and Avian Models. Oxford, UK: Oxford University Press, pp. 16.Google Scholar
Ewald, PW (1994) Evolution of Infectious Disease. Oxford, UK: Oxford University Press.Google Scholar
Fogelman, RM, Kuris, AM and Grutter, AS (2009) Parasitic castration of a vertebrate: effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinal fish, Cheilodipterus quinquelineatus. International Journal for Parasitology 39, 577583.CrossRefGoogle Scholar
Heins, DC (2012) Fecundity compensation in the three-spined stickleback Gasterosteus aculeatus infected by the diphyllobothriidean cestode Schistocephalus solidus. Biological Journal of the Linnean Society 106, 807819.CrossRefGoogle Scholar
Heins, DC and Baker, JA (1993) Clutch production in the darter Etheostoma lynceum and its implications for life history study. Journal of Fish Biology 42, 819829.CrossRefGoogle Scholar
Heins, DC and Baker, JA (2003) Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite. Journal of Parasitology 89, 16.CrossRefGoogle ScholarPubMed
Heins, DC and Baker, JA (2008) The stickleback–Schistocephalus host–parasite system as a model for understanding the effect of a macroparasite on host reproduction. Behaviour 145, 625645.CrossRefGoogle Scholar
Heins, DC and Brown-Peterson, NJ (2010) Influence of the pseudophyllidean cestode Schistocephalus solidus on oocyte development in the threespine stickleback Gasterosteus aculeatus. Parasitology 137, 11511158.CrossRefGoogle ScholarPubMed
Heins, DC, Singer, SS and Baker, JA (1999) Virulence of the cestode Schistocephalus solidus and reproduction in infected threespine stickleback, Gasterosteus aculeatus. Canadian Journal of Zoology 77, 19671974.CrossRefGoogle Scholar
Heins, DC, Baker, JA and Martin, HC (2002) The ‘crowding effect’ in the cestode Schistocephalus solidus: density-dependent effects on plerocercoids size and infectivity. Journal of Parasitology 88, 302307.Google Scholar
Heins, DC, Baker, JA, Toups, MA and Birden, EL (2010 a) Evolutionary significance of fecundity reduction in three-spined stickleback infected by the diphyllobothriidean cestode Schistocephalus solidus. Biological Journal of the Linnean Society 100, 835846.CrossRefGoogle Scholar
Heins, DC, Birden, EL and Baker, JA (2010 b) Host mortality and variability in epizootics of Schistocephalus solidus infecting the threespine stickleback, Gasterosteus aculeatus. Parasitology 137, 16811686.CrossRefGoogle ScholarPubMed
Heins, DC, Baker, JA and Green, DM (2011) Processes influencing the duration and decline of epizootics in Schistocephalus solidus. Journal of Parasitology 97, 371376.CrossRefGoogle ScholarPubMed
Heins, DC, Barry, KA and Petrauskas, LA (2014) Consistency of host responses to parasitic infection in the three-spined stickleback fish infected by the diphyllobothriidean cestode Schistocephalus solidus. Biological Journal of the Linnean Society 113, 958968.CrossRefGoogle Scholar
Heins, DC, Eidam, D and Baker, JA (2016) Timing of Infections in the threespine stickleback (Gasterosteus aculeatus) by Schistocephalus solidus in Alaska. Journal of Parasitology 102, 286289.CrossRefGoogle ScholarPubMed
Hurd, H (2001) Host fecundity reduction: a strategy for damage limitation? Trends in Parasitology 17, 363368.CrossRefGoogle ScholarPubMed
Kalbe, M, Eizaguirre, C, Scharsack, JP and Jakobsen, PJ (2016) Reciprocal cross infection of sticklebacks with the diphyllobothriidean cestode Schistocephalus solidus reveals consistent population differences in parasite growth and host resistance. Parasites & Vectors 9, 130.CrossRefGoogle ScholarPubMed
Kuris, AM (2003) Evolutionary ecology of trophically transmitted parasites. Journal of Parasitology 89, S96S100.Google Scholar
Lafferty, KD and Kuris, AM (2002) Trophic strategies, animal diversity and body size. Trends in Ecology and Evolution 17, 507513.CrossRefGoogle Scholar
Legendre, P (2008) Studying beta diversity: ecological variation partitioning by multiple regression and canonical analysis. Journal of Plant Ecology 1, 38.CrossRefGoogle Scholar
LoBue, CP and Bell, MA (1993) Phenotypic manipulation by the cestode parasite Schistocephalus solidus of its intermediate host, Gasterosteus aculeatus, the three-spined stickleback. American Naturalist 142, 725735.CrossRefGoogle Scholar
Michaud, M, Milinski, M, Parker, GAChubb, JC (2006) Competitive growth strategies in intermediate hosts: experimental tests of a parasite life-history model using the cestode, Schistocephalus solidus. Evolutionary Ecology 20, 3957.CrossRefGoogle Scholar
Nordeide, JT and Matos, F (2016) Solo Schistocephalus solidus tapeworms are nasty. Parasitology 143, 13011309.CrossRefGoogle ScholarPubMed
Oksanen, J, Blanchet, FG, Kindt, R, Legendre, P, Minchin, PR, O'Hara, RB, Simpson, GL, Solymos, P, Stevens, MHH and Wagner, H (2016) vegan: Community ecology package. R package version 2.4-1. Available at https://CRAN.R-project.org/package=vegan.Google Scholar
Parker, GA, Chubb, JC, Roberts, GN, Michaud, M and Milinski, M (2003) Optimal growth strategies of larval helminths in their intermediate hosts. Journal of Evolutionary Biology 16, 4754.CrossRefGoogle ScholarPubMed
Pennycuick, L (1971) Seasonal variation in the parasite infections in a population of three-spined sticklebacks, Gasterosteus aculeatus L. Parasitology 63, 373388.CrossRefGoogle Scholar
Peres-Neto, PR and Legendre, P (2010) Estimating and controlling for spatial structure in the study of ecological communities. Global Ecology and Biogeography 19, 174184.CrossRefGoogle Scholar
Rao, CR (1964) The use and interpretation of principal component analysis in applied research. Sankhya A 26, 329358.Google Scholar
Scharsack, JP, Koch, K and Hammerschmidt, K (2007) Who is in control of the stickleback immune system: interactions between Schistocephalus solidus and its specific vertebrate host. Proceedings of the Royal Society of London B: Biological Sciences 274, 31513158.CrossRefGoogle ScholarPubMed
Schultz, ET, Topper, M and Heins, DC (2006) Decreased reproductive investment of female threespine stickleback Gasterosteus aculeatus infected with the cestode Schistocephalus solidus: parasite adaptation, host adaptation, or side effect? Oikos 114, 303310.CrossRefGoogle Scholar
Smyth, JD (1962) Introduction to Animal Parasitology. Springfield, IL: C. C. Thomas.Google Scholar
Sokal, RR and Rohlf, FJ (1995) Biometry, 3rd Edn. New York, USA: W.H. Freeman and Co.Google Scholar
Threlfall, W (1968) A mass die-off of three-spined sticklebacks (Gasterosteus aculeatus L.) caused by parasites. Canadian Journal of Zoology 46, 105106.CrossRefGoogle ScholarPubMed
Tierney, JF and Crompton, DW (1992) Infectivity of plerocercoids of Schistocephalus solidus (Cestoda: Ligulidae) and fecundity of the adults in an experimental definitive host, Gallus gallus. Journal of Parasitology 78, 10491054.CrossRefGoogle Scholar
Tierney, JF, Huntingford, FA and Crompton, DWT (1996) Body condition and reproductive status in sticklebacks exposed to a single wave of Schistocephalus solidus infection. Journal of Fish Biology 49, 483493.Google Scholar
Walkey, M and Meakins, RH (1970) An attempt to balance the energy budget of a host–parasite system. Journal of Fish Biology 2, 361372.CrossRefGoogle Scholar
Wedekind, C, Strahm, D and Schärer, L (1998) Evidence for strategic egg production in a hermaphroditic cestode. Parasitology 117, 373382.CrossRefGoogle Scholar
Woods, PF (1985) Limnology of Nine Small Lakes, Matanuska–Susitna Borough, Alaska, and the Survival and Growth Rates of Rainbow Trout. US Geological Survey Water-Research Investigation Report 85-4292. Anchorage, AK, USA: US Department of the Interior.Google Scholar
Wootton, RJ (1976) The Biology of the Sticklebacks. London, UK: Academic Press.Google Scholar

Altmetric attention score

Full text views

Full text views reflects PDF downloads, PDFs sent to Google Drive, Dropbox and Kindle and HTML full text views.

Total number of HTML views: 16
Total number of PDF views: 106 *
View data table for this chart

* Views captured on Cambridge Core between 20th June 2018 - 11th April 2021. This data will be updated every 24 hours.

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Are solo infections of the diphyllobothriidean cestode Schistocephalus solidus more virulent than multiple infections?
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Are solo infections of the diphyllobothriidean cestode Schistocephalus solidus more virulent than multiple infections?
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Are solo infections of the diphyllobothriidean cestode Schistocephalus solidus more virulent than multiple infections?
Available formats
×
×

Reply to: Submit a response


Your details


Conflicting interests

Do you have any conflicting interests? *