FIREANTS! First 15 pages

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A Nature Research Journal. Despite the presence of conserved innate immune function, many insects have evolved a variety of mechanical, chemical, and behavioral defensive responses to pathogens. Illness-induced anorexia and dietary changes are two behavioral defensive strategies found in some solitary insects, but little is known regarding the role of such behaviors in social insects, especially in ants. In the present study we examined if such reduced foraging activity exists for a social insect, the invasive fire ant Solenopsis invicta , and its viral pathogen, Solenopsis invicta virus 1 SINV Virus-free fire ant colonies were split into two colony fragments, one of which subsequently was inoculated with SINV Four food resources with different macronutrient ratios were presented to both colony fragments.

SINVinoculated colony fragments consistently displayed reduced foraging performance e.

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These findings provide the first evidence for virus-induced behavioral responses and dietary shifts in shaping the host-pathogen interactions in fire ants. The findings also suggest a possible mechanism for how fire ant colonies respond to viral epidemics. Potential implications of these behavioral differences for current management strategies are discussed.

Social insects have evolved sophisticated defensive systems presumably as adaptive responses to pathogens commonly encountered because of frequent social contact. Both allo-grooming and secretion of antibiotic compounds are two often cited examples reported in social insects 1 , 2 , 3 , 4. Conversely, some pathogens have been reported to alter host behavior to favor their own transmission and enhance their replication and virulence 5.

Studies of non-social insects have reported reduced feeding anorexia and changes in dietary macronutrient preference in pathogen-challenged individuals, both of which are associated with an enhanced ability to cope with pathogen infections likely via starvation of resident pathogens from essential macronutrients or trade-offs in energy allocation 6. Whether similar defensive mechanisms involving illness-induced behavioral changes also occur in social insects, especially ants, remain ambiguous 7 , 8.

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In this study, we tested whether reduced foraging activity or changes in macronutrient preference occur in the highly social fire ant Solenopsis invicta in response to a natural viral pathogen, Solenopsis invicta virus 1 SINV This virus is believed to persist largely as a chronic and asymptomatic infection but may become virulent and result in illness and colony death when ant colonies are stressed More specifically, recent studies demonstrate this virus leads to high larval mortality under certain laboratory rearing conditions and significant weight loss of queens during colony founding Several immune-related genes are up-regulated in SINVinfected fire ants 11 , further suggesting the virus imposes significant fitness costs under certain stressful conditions.

Despite great variations in their dietary preference, S. Since knowledge on interplay among feeding stimulant, foraging patterns and dietary preference plays a critical role in success of bait-based management in fire ants 16 , demonstration that SINV-1 induces reduced foraging activity or changes in macronutrient intake are of critical importance because alterations of feeding rates and dietary preferences may impact the efficacies of poison baits used for fire ant control and population monitoring methods. Results from our behavioral assays revealed significant differences in foraging patterns and macronutrient preferences between the uninfected and SINVinfected colony fragments.

The bizarre physics of fire ants

While the absence of a queen was associated with reduced foraging performance in this study, the impacts of viral infection outweighed the effects associated with queen presence and played a critical role in regulating foraging patterns of S. Numbers of workers foraging on food resources were higher in uninfected fragments compared with SINVinfected fragments.

Both SINV-1 infection and the absence of a queen significantly reduced the total number of forager workers, but the former had a greater impact Fig. A similar pattern was observed for recruitment efficiency. Uninfected fragments reached peak foraging activities significantly faster than SINVinfected fragments. The time required to reach foraging peak significantly differed among the four fragment categories Fig. Foraging activities and peak recruitment time of uninfected round and SINVinfected triangle colony fragments.

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  7. The open and closed symbols denote the presence and absence of a queen in a fragment, respectively. Workers began to forage as soon as Uninfected colony fragments lacking a queen displayed similar patterns in both onset of foraging Queen presence had no significant effect on recruitment efficiency in uninfected fragments Fig. Workers from SINVinfected fragments showed significant differences in foraging intensity compared with uninfected workers. We detected no effect of queen presence on the number of workers or the time of the foraging onset Analyses of numbers of workers on different food resources indicated workers from uninfected fragments prefer high lipid or protein content food i.

    In contrast, workers from SINVinfected fragments significantly preferred diluted honey or potato chip compared with those from uninfected fragments Fig. Moreover, the presence of a queen influenced colony food preferences. All uninfected queenright fragments significantly preferred tuna, a food resource with relatively higher lipid and protein content Fig.

    Food preference expressed as the number of workers at each food resource across time. Note quantitative scales for the y-axis differ among the graphs due to differences in number of foragers between uninfected and infected fragments. Our results provide evidence for both reduced foraging activity and a change in macronutrient preferences of virus-challenged fire ants.

    SINVinfected ants invariably displayed reduced foraging activities compared with uninfected ants. SINVinfected 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.

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    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 bees 1 , 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. SINVinfected S. 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.

    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. Recently, Benaets et al. Moreover, most insect-infecting ssRNA viruses including SINV-1 replicate in the intestinal epithelium 10 , raising the possibility that increased numbers of viral particles impair digestive capabilities of the epithelium, resulting in loss of appetite and reduced foraging activity Our preliminary data are partially in line with this prediction as the number of apoptotic cells in the mid-gut of the 4 th instar larvae of S.

    Because larval conditions in a colony can act as major drivers of worker foraging activity 25 , the reduced foraging performance of workers in our study may be indicative of changes in larval health or status e. 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 pathogen 6 , 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 costs 6.

    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 infections 27 , 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 behavior Carbohydrate supplementation is consistently associated with enhanced fitness at both the individual and colony levels in numerous ant species including fire ants 29 , Also, a recent study reported multiple benefits of a high-carbohydrate diet to immunity function in the ant Ectatomma ruidum 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 SINVinfected 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 SINVinfected 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. 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 broadly 12 , 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.

    Fire ant colonies were collected from northern Taiwan. The social form and infection status of colonies with respect to three S. Note that polygyne colonies were not included in this study due to scarcity of virus-free colonies of this given social form in the field 12 , Fragments were maintained on a diet of frozen crickets, sucrose solution and water.

    Behavioral assays were conducted 30 days post inoculation. To quantify the foraging intensity, we recorded total numbers of foragers at all four food resources using an automatic recording system camera Olympus TG-3, Olympus Corp. These pictures were analyzed to estimate the total number of foraging workers at each time point using a naked-eye-counting strategy. Time required for the first five workers to arrive at one of the four food resources was measured onset of foraging.

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    We also measured recruitment efficiency, defined as the time elapsed until peak in foraging was reached during a hour observation period. Food preference was determined by assessing the number of workers at each food resource in both uninfected and infected fragments. The effects of viral infection on fire ant foraging behavior were analyzed by comparing foraging patterns and food preferences between uninfected and SINV1-infected fragments.

    For the statistical analysis of foraging intensity, defined as total number of forager workers observed on all four food resources, the effects of infection and the presence of queen were modeled by using generalized linear mixed models GLMMs with Poisson errors and negative-binomial errors. Despite nearly identical results, we only showed the results estimated with negative-binomial errors because of lower Akaike information criterion AIC values and overdispersion Chi-square test. The numbers of ants at each time point are considered as response variables, infection status and presence of queen as fixed effects, and colony identity and each time point as random factors.

    Significances of the fixed effects were tested using the likelihood ratio test by comparing the full model and models sequentially removing each effect term. The significances among the four fragment categories were first analyzed by a one-way ANOVA or Kruskal-Wallis test, and then post hoc by pairwise T test or pairwise Kruskal-Wallis test with the Bonferroni correction. For changes in food preference, the full mixed model was built using negative-binomial errors with the total ant numbers at each time point considered as response variables, and colony identity and each time point as random factors.

    The likelihood ratio test was used to determine significance level of each fixed effect by reducing the full model. The relationship between food preference and fragment categories was analyzed using a local regression locally weighted scatterplot smoothing curve, LOWESS curve. Simone-Finstrom, M. Social immunity and the superorganism: behavioral defenses protecting honey bee colonies from pathogens and parasites.

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    Bee World 94 , 21—29 Tragust, S. Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Ugelvig, L. Social prophylaxis: group interaction promotes collective immunity in ant colonies. Zeng, Y. Multiple antibacterial activities of proteinaceous compounds in crude extract from the eastern subterranean termite, Reticulitermes flavipes Kollar Blattodea: Isoptera: Rhinotermitidae.

    Hafer, N. Conflicts over host manipulation between different parasites and pathogens: investigating the ecological and medical consequences. Bioessays 38 , — Mason, A. Reduced consumption of protein-rich foods follows immune challenge in a polyphagous caterpillar.

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    Adamo, S. Illness-induced anorexia may reduce trade-offs between digestion and immune function. Singer, M.

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