Hostname: page-component-848d4c4894-2pzkn Total loading time: 0 Render date: 2024-04-30T21:30:22.193Z Has data issue: false hasContentIssue false
  • English
  • Français

Stable-isotope analysis: a neglected tool for placing parasites in food webs

Published online by Cambridge University Press:  28 February 2018

A.J.M. Sabadel ,
A.D. Stumbo  and
C.D. MacLeod
A.J.M. Sabadel*
Affiliation:
University of Otago, Department of Chemistry, Dunedin, New Zealand
A.D. Stumbo
Affiliation:
Otago Museum, Dunedin, New Zealand
C.D. MacLeod
Affiliation:
University of British Columbia, Department of Zoology, Vancouver, Canada
*
Author for correspondence: A.J.M. Sabadel, E-mail: asabadel@chemistry.otago.ac.nz
Get access Rights & Permissions [Opens in a new window]

Abstract

Parasites are often overlooked in the construction of food webs, despite their ubiquitous presence in almost every type of ecosystem. Researchers who do recognize their importance often struggle to include parasites using classical food-web theory, mainly due to the parasites' multiple hosts and life stages. A novel approach using compound-specific stable-isotope analysis promises to provide considerable insight into the energetic exchanges of parasite and host, which may solve some of the issues inherent in incorporating parasites using a classical approach. Understanding the role of parasites within food webs, and tracing the associated biomass transfers, are crucial to constructing new models that will expand our knowledge of food webs. This mini-review focuses on stable-isotope studies published in the past decade, and introduces compound-specific stable-isotope analysis as a powerful, but underutilized, newly developed tool that may answer many unresolved questions regarding the role of parasites in food webs.

Type
Review Article
Information
Journal of Helminthology , Volume 93 , Issue 1 , January 2019 , pp. 1 - 7
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. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Altizer, S, Hobson, KA, Davis, AK, De Roode, JC and Wassenaar, LI (2015) Do healthy monarchs migrate farther? Tracking natal origins of parasitized vs. uninfected monarch butterflies overwintering in Mexico. PLoS ONE 10, e0141371.Google Scholar
Boag, B, Neilson, R, Robinson, D, Scrimgeour, CM and Handley, LL (1998) Wild rabbit host and some parasites show trophic-level relationships for δ 13C and δ 15N: a first report. Isotopes in Environmental and Health Studies 34, 81–85.Google Scholar
Boecklen, WJ, Yarnes, CT, Cook, BA and James, AC (2011) On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution, and Systematics 42, 411–440.Google Scholar
Brand, WA and Coplen, TB (2012) Stable isotope deltas: tiny, yet robust signatures in nature. Isotopes in Environmental and Health Studies 48, 393–409.Google Scholar
Britton, JR and Andreou, D (2016) Parasitism as a driver of trophic niche specialisation. Trends in Parasitology 32, 437–445.Google Scholar
Cain, ML, Bowman, WD and Hacker, SD (2008) Ecology. Sunderland, Massachusetts, Sinauer.Google Scholar
Caut, S, Angulo, E and Courchamp, F (2008) Discrimination factors (Δ15N and Δ13C) in an omnivorous consumer: effect of diet isotopic ratio. Functional Ecology 22, 255–263.Google Scholar
Caut, S, Angulo, E and Courchamp, F (2009) Variation in discrimination factors (Δ15N and Δ13C): the effect of diet isotopic values and applications for diet reconstruction. Journal of Applied Ecology 46, 443–453.Google Scholar
Chikaraishi, Y, Steffan, SA, Ogawa, NO, Ishikawa, NF, Sasaki, Y, Tsuchiya, M and Ohkouchi, N (2014) High-resolution food webs based on nitrogen isotopic composition of amino acids. Ecology and Evolution 4, 2423–2449.Google Scholar
Clark, JM and Hawke, DJ (2014) A new epizoic laelapid mite from the New Zealand sand scarab Pericoptus truncatus larvae and its isotopic ecology. New Zealand Journal of Zoology 39, 187–199.Google Scholar
Collinge, S and Ray, C (2006) Disease ecology: community structure and pathogen dynamics. Oxford, UK, Oxford University Press.Google Scholar
Demopoulos, AWJ and Sikkel, PC (2015) Enhanced understanding of ectoparasite–host trophic linkages on coral reefs through stable isotope analysis. International Journal for Parasitology: Parasites and Wildlife 4, 125–134.Google Scholar
DeNiro, MJ and Epstein, S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.Google Scholar
Deudero, S, Pinnegar, JK and Polunin, NVC (2002) Insights into fish host–parasite trophic relationships revealed by stable isotope analysis. Diseases of Aquatic Organisms 52, 77–86.Google Scholar
Dobson, A, Lafferty, KD, Kuris, AM, Hechinger, RF and Jetz, W (2008) Homage to Linnaeus: How many parasites? How many hosts? Proceedings of the National Academy of Sciences, USA 105, 11482–11489.Google Scholar
Dunne, JA, Lafferty, KD, Dobson, AP, et al. (2013) Parasites affect food web structure primarily through increased diversity and complexity. PLoS Biology 11, e1001579.Google Scholar
Fritts, MW, Fritts, AK, Carleton, SA and Bringolf, RB (2013) Shifts in stable-isotope signatures confirm parasitic relationship of freshwater mussel glochidia attached to host fish. Journal of Molluscan Studies 79, 163–167.Google Scholar
Fry, B (2006) Stable isotope ecology, New York, Springer-Verlag.Google Scholar
Gómez-Díaz, E and González-Solís, J (2010) Trophic structure in a seabird host–parasite food web: insights from stable isotope analyses. PLoS One, 5.Google Scholar
Hobson, KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120, 314–326.Google Scholar
Iken, K, Brey, T, Wand, U, Voigt, J and Junghans, P (2001) Food web structure of the benthic community at the Porcupine Abyssal Plain (NE Atlantic): a stable isotope analysis. Progress in Oceanography 50, 383–405.Google Scholar
Knudsen, R, Siwertsson, A, Adams, CE, Newton, J and Amundsen, P-A (2014) Similar patterns of individual niche use are revealed by different time-integrated trophic tracers (stable isotopes and parasites). Ecology of Freshwater Fish 23, 259–268.Google Scholar
Koch, PL (2008) Isotopic study of the biology of modern and fossil vertebrates. Stable isotopes in ecology and environmental science. Oxford, UK, Blackwell Publishing.Google Scholar
Kuris, AM, Hechinger, RF, Shaw, JC, et al. (2008) Ecosystem energetic implications of parasite and free-living biomass in three estuaries. Nature 454, 515–518.Google Scholar
Lafferty, KD, Allesina, S, Arim, M, et al. (2008) Parasites in food webs: the ultimate missing links. Ecology Letters 11, 533–546.Google Scholar
Lagrue, C and Poulin, R (2007) Life cycle abbreviation in the trematode Coitocaecum parvum: can parasites adjust to variable conditions? Journal of Evolutionary Biology 20, 1189–1195.Google Scholar
Lee-Thorp, JA (2008) On isotopes and old bones*. Archaeometry 50, 925–950.Google Scholar
Marcogliese, DJ and Cone, DK (1997) Food webs: a plea for parasites. Trends in Ecology & Evolution 12, 320–325.Google Scholar
McCann, KS (2000) The diversity-stability debate. Nature 405, 228–233.Google Scholar
McClelland, JW and Montoya, JP (2002) Trophic relationships and the nitrogen isotopic composition of amino acids in plankton. Ecology 83, 2173–2180.Google Scholar
McLeod, RJ, Hyndes, GA, Hurd, CL and Frew, RD (2013) Unexpected shifts in fatty acid composition in response to diet by a common littoral amphipod. Marine Ecology Progress Series 479, 1–12.Google Scholar
McMahon, KW and McCarthy, MD (2016) Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology. Ecosphere 7, 1–26.Google Scholar
Meier-Augenstein, W (2002) Stable isotope analysis of fatty acids by gas chromatography–isotope ratio mass spectrometry. Analytica Chimica Acta 465, 63–79.Google Scholar
Minagawa, M and Wada, E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ 15N and animal age. Geochimica et Cosmochimica Acta 48, 1135–1140.Google Scholar
Morley, NJ (2012) Cercariae (Platyhelminthes: Trematoda) as neglected components of zooplankton communities in freshwater habitats. Hydrobiologia 691, 7–19.Google Scholar
Nachev, M, Jochmann, MA, Walter, F, Wolbert, JB, Schulte, SM, Schmidt, TC and Sures, B (2017) Understanding trophic interactions in host–parasite associations using stable isotopes of carbon and nitrogen. Parasites & Vectors 10, 90.Google Scholar
Neilson, R, Boag, B and Hartley, G (2005) Temporal host–parasite relationships of the wild rabbit, Oryctolagus cuniculus (L.) as revealed by stable isotope analyses. Parasitology 131, 279–285.Google Scholar
O'Grady, SP and Dearing, MD (2006) Isotopic insight into host–endosymbiont relationships in Liolaemid lizards. Oecologia 150, 355–361.Google Scholar
Ohkouchi, N, Chikaraishi, Y, Close, HG, et al. (2017) Advances in the application of amino acid nitrogen isotopic analysis in ecological and biogeochemical studies. Organic Geochemistry 113, 150–174.Google Scholar
Pascual, M and Dunne, JA (2006) From small to large ecological networks in a dynamic world. New York, Oxford University Press.Google Scholar
Peterson, BJ and Fry, B (1987) Stable isotopes in ecosystem studies. Annual Review of Ecology and Systematics 18, 293–320.Google Scholar
Pinnegar, JK, Campbell, N and Polunin, NVC (2001) Unusual stable isotope fractionation patterns observed for fish host–parasite trophic relationships. Journal of Fish Biology 59, 494–503.Google Scholar
Post, DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.Google Scholar
Poulin, R and Morand, S (2004) Parasite biodiversity. Washington, DC, Smithsonian Institution Books.Google Scholar
Pulkkinen, K, Aalto, SL and Nykänen, H (2016) Parasite infection alters host stable-isotope composition under controlled feeding. Freshwater Biology 61, 1981–1990.Google Scholar
Sabadel, AJM, Woodward, EMS, Van Hale, R and Frew, RD (2016) Compound-specific isotope analysis of amino acids: a tool to unravel complex symbiotic trophic relationships. Food Webs 6, 9–18.Google Scholar
Sánchez, MI, Varo, N, Matesanz, C, Ramo, C, Amat, JA and Green, AJ (2013) Cestodes change the isotopic signature of brine shrimp, Artemia, hosts: implications for aquatic food webs. International Journal for Parasitology 43, 73–80.Google Scholar
Sukhdeo, MV (2012) Where are the parasites in food webs? Parasites & Vectors 5, 239.Google Scholar
Thieltges, DW, De Montaudouin, X, Fredensborg, B, Jensen, KT, Koprivnikar, J and Poulin, R (2008) Production of marine trematode cercariae: a potentially overlooked path of energy flow in benthic systems. Marine Ecology Progress Series 372, 147–155.Google Scholar
Thompson, RM, Brose, U, Dunne, JA, et al. (2012) Food webs: reconciling the structure and function of biodiversity. Trends in Ecology & Evolution 27, 689–697.Google Scholar
Vander Zanden, JM and Rasmussen, JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnology and Oceanography 46, 2061–2066.Google Scholar
Wing, SR, Mcleod, RJ, Leichter, JJ, Frew, RD and Lamare, MD (2012) Sea ice microbial production supports Ross Sea benthic communities: influence of a small but stable subsidy. Ecology 93, 314–323.Google Scholar