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ARS Home » Northeast Area » Beltsville, Maryland (BARC) » Beltsville Agricultural Research Center » Animal Parasitic Diseases Laboratory » Research » Publications at this Location » Publication #302216

Research Project: MOLECULAR AND IMMUNOLOGICAL APPROACHES TO CONTROLLING GI NEMATODE INFECTIONS OF RUMINANTS

Location: Animal Parasitic Diseases Laboratory

Title: Resource limitation alters the consequences of co-infection for both hosts and parasites

Author
item BUDISCHAK, S - University Of Georgia
item SAKAMOTO, K - University Of Georgia
item MEGOW, L - University Of Georgia
item CUMMINGS, K - University Of Georgia
item Urban, Joseph
item EZENWA, V - University Of Georgia

Submitted to: International Journal for Parasitology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/1/2015
Publication Date: 3/24/2015
Publication URL: http://doi:10.1016/j.ijpara.2015.02.005
Citation: Budischak, S.A., Sakamoto, K., Megow, L.C., Cummings, K.R., Urban Jr, J.F., Ezenwa, V. 2015. Resource limitation alters the consequences of co-infection for both hosts and parasites. International Journal for Parasitology. 45(7):455-463.

Interpretive Summary: Most animals are infected with multiple parasite species simultaneously in the natural world, and these co-infections can affect host susceptibility and parasite infectivity. Community ecology theory can provide a mechanistic framework for understanding the network of direct and indirect interactions among hosts and parasites and for making predictions for the outcomes of co-infection. For instance, a classic trophic framework applied to host parasite communities sees “attacks” by the host’s immune system as analogous to top-down predation pressure, while host resources represented in the diet may exert bottom-up effects on the parasite community by limiting critical nutrients. It is unclear, however, how alterations in resource availability affect within-host parasite interactions. Resource limitation can influence the hosts’ ability to mount an adequate immune response that could alter the strength of immune-meditated interactions among coinfecting parasites. Alternatively, parasite competition or trade-offs between different immune responses may be more critical in resource-limited hosts. To test the concurrent interactions among resource availability, immune function, and micro- and macro-parasites, laboratory mice were given a standard or low quality diet and then infected with two parasitic worm species alone and in combination, and also challenged with the bacterial micro-parasite Mycobacterium bovis. Diet strongly influenced host immune function and condition, and parasite survival and reproduction. Interactions between the two worm parasite species were stronger among mice fed a standard protein diet, but the interactions between worms and the mycobacteria were stronger among mice fed a low protein diet. The immune-mediated effects of worm co-infection and diet were stronger than bottom-up, resource-mediated effects on worm reproductive capacity. Protein malnutrition may affect the strength of some parasitic worm and pathogenic bacterial interactions, and also influence the transmission of worm infections in natural populations. These findings highlight the importance of investigating parasite communities and not single parasite infections to understand the responses of both host and parasite populations to additional pathogens and changing resource availability.

Technical Abstract: Most animals are concurrently infected with multiple parasites and live in environments with fluctuating resource availability. Compelling evidence from humans, laboratory model systems, and wildlife suggests that interactions among co-infecting parasites can influence disease dynamics, individual health, and host fitness. However, it is unclear how alterations in resource availability affect within-host parasite interactions. Resource limitation often influences hosts’ ability to mount adequate immune responses, and, consequently, could alter the strength of immune-meditated interactions among co-infecting parasites. Alternatively, parasite competition or trade-offs between different immune responses may be elevated in resource-limited hosts. To test concurrent interactions among resource availability, immune function, and micro- and macro-parasites, we conducted a factorial experiment using laboratory mice (BALB/c). Specifically, mice were given a standard or low quality diet, dosed with two species of helminths (alone and in combination), and then challenged with the microparasite Mycobacterium bovis. Diet strongly influenced host immune function and condition, and parasite survival and reproduction. The magnitude and direction of responses depended on diet quality and the combination of co-infecting parasites. Interactions between the two helminth species were stronger among mice fed a standard protein diet, but the interactions between helminths and M. bovis were stronger among mice fed a low protein diet. For both helminth species, immune-mediated effects of co-infection and diet were stronger than bottomup, resource-mediated effects on parasite reproduction. Overall, our data reinforce the impetus to investigate parasite communities, not simply single parasites, and demonstrate the need to understand how both hosts and parasites responses will respond to changing resource availability.