Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2017 Apr;183(4):1031-1040.
doi: 10.1007/s00442-017-3822-7. Epub 2017 Jan 30.

Host resistance and tolerance of parasitic gut worms depend on resource availability

Sarah A Knutie  1 , Christina L Wilkinson  2 , Qiu Chang Wu  3 , C Nicole Ortega  2 , Jason R Rohr  2
Affiliations

Host resistance and tolerance of parasitic gut worms depend on resource availability

Sarah A Knutie et al. Oecologia. 2017 Apr.

Abstract

Resource availability can significantly alter host-parasite dynamics. Abundant food can provide more resources for hosts to resist infections, but also increase host tolerance of infections by reducing competition between hosts and parasites for food. Whether abundant food favors host resistance or tolerance (or both) might depend on the type of resource that the parasite exploits (e.g., host tissue vs. food), which can vary based on the stage of infection. In our study, we evaluated how low and high resource diets affect Cuban tree frog (Osteopilus septentrionalis) resistance and tolerance of a skin-penetrating, gut nematode Aplectana sp. at each stage of the infection. Compared to a low resource diet, a high resource diet enhanced frog resistance to worm penetration and tolerance while worms traveled to the gut. In contrast, a low resource diet increased resistance to establishment of the infection. After the infection established and worms could access food resources in the gut, a high resource diet enhanced host tolerance of parasites. On a high resource diet, parasitized frogs consumed significantly more food than non-parasitized frogs; when food was then restricted, mass of non-parasitized frogs did not change, whereas mass of parasitized frogs decreased significantly. Thus, a high resource diet increased frog tolerance of established worms because frogs could fully compensate for energy lost to the parasites. Our study shows that host-parasite dynamics are influenced by the effect of resource availability on host resistance and tolerance, which depends on when parasites have access to food and the stage of infection.

Keywords: Amphibians; Disease dynamics; Ecoimmunology; Helminths; Host defense; Nematodes.

PubMed Disclaimer

Figures

Fig. 1
Fig. 1
Predictions for the effect of resource availability on the relationship between host health and parasite abundance. a) When only hosts have access to food resources, hosts with high resources (solid line) will have fewer parasites than hosts with low resources (dotted line). b) Once the infection has established, hosts with high resources will be more tolerant of effects of parasites compared to hosts with low resources (Figure modified from Råberg et al. 2007).
Fig. 2
Fig. 2
Effect of resources on host resistance against initial worm penetration and establishment in the gut. a) Low resource diet frogs were penetrated by proportionally more worms compared to high resource diet frogs (n = 15 for each treatment); b) Proportional change in mass was negatively related to the proportion of worms that penetrated the frogs; c) high resource diet frogs had proportionally more worms establish in frog guts (out of the number that penetrated) compared to low resource diet frogs; d) total number of worms that established in the gut did not differ significantly between treatments. Each panel displays means (± 1 SE).
Fig. 3
Fig. 3
Relationship between antibody-mediated immune response and parasitism across diet treatments. a) Parasite abundance was positively related to antibody levels for low (dotted line) and high (solid line) resource diet; b) high resource diet frogs had lower antibody levels (optical density (OD) values) compared to low resource diet frogs (low resource diet: n = 14 frogs, high resource diet: n = 15 frogs). Means are displayed with ± 1 SE.
Fig. 4
Fig. 4
Effect of resources on host tolerance of parasitism after infection had established. a) Parasitized frogs defecated significantly more often (n = 11) than non-parasitized frogs (n = 13); b) Mean (± SE) number of crickets eaten by non-parasitized (n = 13) and parasitized (n = 11) frogs after two days and across two trials; c) Mean (± SE) proportional change in frog mass between weeks during high access to food or from high to low access to food (parasitized, trial 1: n = 11 frogs, trial 2: n = 9; non-parasitized, trial 1: n = 13, trial 2: n = 12). A value of zero indicates no change in mass, while a positive value indicates an increase and a negative value indicates a decrease in mass. Non-parasitized and parasitized frogs that were provided an high resource diet gained mass; when on a low resource diet, parasitized frogs loss mass; d) Tolerance of frogs to Aplectana worms on high and low resource diets. While on a high resource diet (black points and line), mass did not significantly vary with parasite abundance. In contrast, mass decreased with increasing parasite abundance on a low resource diet (grey points and line) in the same frogs.
See this image and copyright information in PMC

References

    1. Adelman JS, Kirkpatrick L, Grodio JL, Hawley DM. House finch populations differ in early inflammatory signaling and pathogen tolerance at the peak of Mycoplasma gallisepticum infection. Am Nat. 2013;181:674–689. doi: 10.1086/670024. - DOI - PubMed
    1. Anholt BR, Werner EE. Interaction between food availability and predation mortality mediated by adaptive behavior. Ecology. 1995;76:2230–2234. doi: 10.2307/1941696. - DOI
    1. Becker DJ, Streicker DG, Altizer S. Linking anthropogenic resources to wildlife-pathogen dynamics: a review and meta-analysis. Ecol Lett. 2015;18:483–495. doi: 10.1111/ele.12428. - DOI - PMC - PubMed
    1. Beldomenico PM, Begon M. Disease spread, susceptibility and infection intensity: vicious circles? Trends Ecol Evol. 2010:21–27. doi: 10.1016/j.tree.2009.06.015. - DOI - PubMed
    1. Bown MD, Poppi DP, Sykes AR. The effect of post-ruminal infusion of protein or energy on the pathophysiology of Trichostrongylus colubriformis infection and body composition in lambs. Aust J Agric Res. 1991;42:253–267. doi: 10.1071/AR9910253. - DOI

Publication types

LinkOut - more resources