Our results provide evidence for both reduced foraging activity and a change in macronutrient preferences of virus-challenged fire ants. SINV-1-infected ants invariably displayed reduced foraging activities compared with uninfected ants. SINV-1-infected ants also altered their feeding preferences toward a carbohydrate-rich diet. Similar findings were reported in fire ants infected with another single strand-RNA virus (SINV-3)17,18, suggesting such behavioral alterations might be common in the ant host challenged with a viral infection. Potential adaptive advantages and the illness consequences of these observed virus-induced changes in foraging behavior are discussed below, followed by the potential management implications of our results.

SINV-1 replicates in the gut epithelium of S. invicta and spreads among nestmates largely through trophallaxis10. Reductions in foraging activity of infected workers may lead to decreases in intra-colony food transfer and exchange, which in turn could reduce SINV-1 transmission among nestmates. Reduced social interactions as a result of decreased foraging activity have been documented in honey bees1,19. For example, injection of lipopolysaccharides into honey bees resulted in appetite loss and a reduction in social interactions, and both of these behavioral changes may contribute to reducing potential pathogen transmission. While such behavioral changes are due to direct virus-induced fitness costs or tradeoffs between immune response and energy allocation remains unclear, reduced social interactions and illness-induced anorexia in diseased colonies could be advantageous (e.g., less trophallaxis and brood tending) by reducing potential for spread of infections3,20. We suggest that the fire ant-virus system is an ideal candidate for future empirical testing of how ant hosts cope with viral infection through illness-mediated behavioral responses, which has never been tested before simply because most previous studies have focused on fungal and/or bacterial infections21.

Reduced foraging activities of workers from SINV-1-infected S. invicta colonies also may reduce direct exposure to interspecific competition with co-existing ants, potentially increasing their survival likelihood as a result of avoidance of interference interactions with native ants. SINV-1-infected S. invicta colonies are significantly less competitive than their uninfected counterparts when exposed to interspecific competition with native ants (i.e., lower aggressiveness)22. A recent field study found fire ant workers significantly outnumber workers of other native ant at the baits placed at sites with low SINV-1 prevalence, whereas fire ants account for an extremely low proportion of ants at the baits at sites with high SINV-1 prevalence (Hsu and Yang unpublished data). These field survey results, coupled with our findings, are consistent with predictions of the “resource dominance-parasitoid vulnerability trade-off theory” previously proposed by Feener23. In this case, local coexistence of ant species within communities likely is influenced by highly specialized pathogens, such as SINV-1, that alter interspecific interactions between competing ants via changes in behaviors of dominant species such as S. invicta. From an applied point of view, these results further suggest the biocontrol potential of SINV-1, and increasing field prevalence of SINV-1 (e.g., artificial inoculation18) may practically suppress fire ants both through alterations of the foraging activities and disruption of the competitive dominance of fire ants over native ants.

Reduced foraging activity of SINV-1-infected S. invicta could be among one of several illness consequences associated with this viral infection. Recently, Benaets et al. found that the deformed wing virus (DWV), a ssRNA virus, seemed to be responsible for reduced foraging behaviors of honey bees24. Moreover, most insect-infecting ssRNA viruses (including SINV-1) replicate in the intestinal epithelium10, raising the possibility that increased numbers of viral particles impair digestive capabilities of the epithelium, resulting in loss of appetite and reduced foraging activity19. Our preliminary data are partially in line with this prediction as the number of apoptotic cells in the mid-gut of the 4th instar larvae of S. invicta increases with time after challenge with SINV-1 (Hsu and Yang, unpublished data). Because larval conditions in a colony can act as major drivers of worker foraging activity25, the reduced foraging performance of workers in our study may be indicative of changes in larval health or status (e.g., larval mortality10), or decreased hunger levels associated with widespread SINV-1-induced apoptosis in the intestinal epithelium.

Previous studies have reported illness-induced alterations in macronutrient intake, observed as an increase in carbohydrate intake, as a process of self-medication in multiple invertebrates after being challenged with a parasite or pathogen6,26. Despite the importance of innate immunity in prevention of subsequent infection in insects, increasing numbers of studies suggest that up-regulation of anti-viral immune systems is linked to a higher mortality due to energy costs6. Thus, compensatory feeding may be a less costly strategy as the fitness cost can be alleviated through either enhanced tolerance of microbial infections or recouping of the resources loss as a result of combating infections27,28. Although our data do not allow us to distinguish whether altered feeding preferences towards a carbohydrate-rich diet result from self-medication or compensatory feeding, the latter may be a more plausible case scenario. Previous studies suggest that a therapeutic behavior must meet four essential criteria, one of which predicts a decrease in fitness of an uninfected individual if engaging in a therapeutic behavior28. Carbohydrate supplementation is consistently associated with enhanced fitness at both the individual and colony levels in numerous ant species including fire ants29,30. Also, a recent study reported multiple benefits of a high-carbohydrate diet to immunity function in the ant Ectatomma ruidum31. Thus, increase of carbohydrate intake in pathogen-challenged ants may be much more prevalent than previously thought and may play a role in carbohydrate resource exploitation of ecologically dominant invasive ants.

Our results have implications for current pest management strategies of fire ants and other invasive ants. A prevailing control method of fire ants is the use of poison baits. Our data raise the interesting possibility that conventional baits may be less effective against SINV-1-infected ants as a result of changes in colony feeding patterns. First, the declining foraging activities of infected ants could lead to recruitment of fewer ants to toxic baits. Second, conventional baits may be less attractive to SINV-1-infected fire ants because of a shift in diet preferences towards carbohydrate-rich food sources. This is because current baits are impregnated with soybean oil, which serves as a phagostimulant. One predicted result of the dietary changes towards carbohydrate-rich food sources and away from food sources containing high lipid content (e.g., tuna and peanut butter) is reduced bait efficacy. In support of this prediction, a recent laboratory trial showed that SINV-1-infected S. invicta are significantly less susceptible to two chemicals commonly used in baits (0.73% hydramethylnon and 0.0103% fipronil) compared with non-infected ants32. While the underlying mechanism is unknown as no further tests were conducted, the behavioral and dietary changes associated with SINV-1 infections represent a potential avenue for future study. Alterations in food preferences also may help explain the generally higher prevalence of SINV-1 in many introduced areas where conventional baits have been applied broadly12, given these baits likely are more effective in eliminating uninfected colonies in the field. While our results are suggestive yet consistent with our prediction, additional studies are warranted to determine whether pathogen-induced phenotypic changes do indeed influence the efficacy of fire ant monitoring and management programs.