Coping with uncertainty: Nutrient deficiencies motivate insect migration at a cost to immunity

Authors: Srygley, Robert; LORCH, PATRICK - Kent State University

Submitted to: Integrative & Comparative Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/10/2013
Publication Date: 12/1/2013
Publication URL: http://handle.nal.usda.gov/10113/58168
Citation: Srygley, R.B., Lorch, P.D. 2013. Coping with uncertainty: Nutrient deficiencies motivate insect migration at a cost to immunity. Integrative & Comparative Biology. 53(6):1002-1013.

Interpretive Summary: Mormon crickets in search of nutrients form migratory bands in rangeland of the western U.S. Because the Mormon crickets are nutrient-deprived and expending energy in migration, we predicted that their immune systems might also be compromised. We have found that migrants deficient in proteins have less phenoloxidase activity, which might compromise their ability to defend themselves against pathogenic fungi. We have also found that migrants deficient in carbohydrates have less anti-bacterial activity. We hypothesize a direct compromise between migratory and anti-bacterial activity mediated by a protein that functions in lipid transport on the one hand and immune activity on the other. Here we report that the bands from Nevada lacked carbohydrates in their diet, confirming previous findings that resource limitation spurs migration. Mormon crickets fed carbohydrates did not migrate as far as those fed proteins, and those fed carbohydrates increased their anti-bacterial activity, supporting the hypothesis of a direct compromise between movement and immunity. The anti-bacterial activity of captive insects was not affected by the diet treatments, which also supports the hypothesis that movement and immunity are in conflict. Movement is rarely incorporated into studies of immune function, and so results of pathogenic studies obtained in confinement may not reflect efficacy in the field. We also extend these results to suggest that environmental unpredictability in protein and carbohydrate resources will make many insect populations fluctuate between a protein-deficient state that might be more susceptible to pathogenic fungi to a carbohydrate-deficient state that is more susceptible to bacteria.

Technical Abstract: Migration is often associated with movement away from areas with depleted nutrients or other resources, and yet migration itself is energetically demanding. Migrating Mormon crickets Anabrus simplex (Orthoptera: Tettigoniidae) lack nutrients, and supplementation of deficient nutrients slows migratory movements and enhances specific aspects of their immune systems. Migrants deficient in proteins have less spontaneous phenoloxidase (PO) activity, whereas those deficient in carbohydrates have less anti-bacterial titers with a proposed compromise between migratory and anti-bacterial activities. To investigate the relationship between diet, movement, and immunity further, we removed Mormon crickets from a migratory band and offered each cricket one of five diet treatments: high protein, high carbohydrate, equal weight proteins and carbohydrates (P+C), vitamins only, or water only for one hour. We then attached a radio, returned each to the migratory band, and recaptured them 18-24 h later. Mormon crickets fed protein moved the furthest, those without diet or only vitamins moved less, and those fed carbohydrates or P+C moved the least. Standard intake trials also indicated that the Mormon crickets were deficient in carbohydrates. Consistent with a previous study, anti-bacterial activity was greatest in those fed carbohydrates, and there was no difference between those fed water, protein, or P+C. Crickets were removed from the same migratory band and fed one of four diet treatments: high P, high C, P+C, or vitamins only, for 1 h. Then the crickets were held in captivity with water only for 4 or 24 h before blood was drawn. Immunity measures did not differ between draw times. Diet treatments had no effect on anti-bacterial activity of captive Mormon crickets, whereas total PO was greater in those fed protein. These results support the hypothesis of a direct compromise between migratory and anti-bacterial activities, whereas PO is compromised by poor protein nutrition independent of migratory activities. We discuss the potential effects of climate on nutritional deficits and susceptibility to different pathogens.