Fungal infection alters collective nutritional intake of ant colonies.

In animals, parasitic infections impose significant fitness costs.1,2,3,4,5,6 Infected animals can alter their feeding behavior to resist infection,7,8,9,10,11,12 but parasites can manipulate animal foraging behavior to their own benefits.13,14,15,16 How nutrition influences host-parasite interactions is not well understood, as studies have mainly focused on the host and less on the parasite.9,12,17,18,19,20,21,22,23 We used the nutritional geometry framework24 to investigate the role of amino acids (AA) and carbohydrates (C) in a host-parasite system: the Argentine ant, Linepithema humile, and the entomopathogenic fungus, Metarhizium brunneum. First, using 18 diets varying in AA:C composition, we established that the fungus performed best on the high-amino-acid diet 1:4. Second, we found that the fungus reached this optimal diet when given various diet pairings, revealing its ability to cope with nutritional challenges. Third, we showed that the optimal fungal diet reduced the lifespan of healthy ants when compared with a high-carbohydrate diet but had no effect on infected ants. Fourth, we revealed that infected ant colonies, given a choice between the optimal fungal diet and a high-carbohydrate diet, chose the optimal fungal diet, whereas healthy colonies avoided it. Lastly, by disentangling fungal infection from host immune response, we demonstrated that infected ants foraged on the optimal fungal diet in response to immune activation and not as a result of parasite manipulation. Therefore, we revealed that infected ant colonies chose a diet that is costly for survival in the long term but beneficial in the short term-a form of collective self-medication.

Infection with a non-lethal fungal parasite is associated with increased immune investment in the ant Myrmica scabrinodis.

Social insects, such as ants, are preferred host organisms of pathogens and parasites because colonies are densely populated, and the number of potential hosts is high in the same place and time. Within a colony, individuals are exposed differentially to risks according to their function and age. Thus, older individuals forage and are therefore the most exposed to infection, predation, or physical stress, while young workers mostly stay inside the sheltered nest being less exposed. Immune investment is considered to be dependent on an individual's age and pathogen pressure. Long-term exposure to a parasite could affect the immune activity of individuals in an intriguing way that interferes with the age-dependent decline in immunocompetence. However, there are only few cases in which such interferences can be studied. The myrmecopathogenic fungus Rickia wasmannii, which infects entire colonies without killing the workers, is a suitable candidate for such studies. We investigated the general immunocompetence of Myrmica scabrinodis ant workers associated with non-lethal fungal infection by measuring the levels of active phenoloxidase (PO) and total PO (PPO) (reflecting the amount of both active and inactive forms of the enzyme) in two age classes. The level of PO proved to be higher in infected workers than in uninfected ones, while the level of PPO increased with age but was not affected by infection. Overall, these results indicate that a long-term infection could go hand in hand with increased immune activity of ant workers, conferring them higher level of protection.

Non-lethal fungal infection could reduce aggression towards strangers in ants.

Many parasites interfere with the behaviour of their hosts. In social animals, such as ants, parasitic interference can cause changes on the level of the individual and also on the level of the society. The ant-parasitic fungus Rickia wasmannii influences the behaviour of Myrmica ants by expanding the host's nestmate recognition template, thereby increasing the chance of the colony accepting infected non-nestmates. Infected ants consistently show an increase of the alkane tricosane (n-C23) in their cuticular hydrocarbon profiles. Although experimental application of single compounds often elicits aggression towards manipulated ants, we hypothesized that the increase of n-C23 might underlie the facilitated acceptance of infected non-nestmates. To test this, we mimicked fungal infection in M. scabrinodis by applying synthetic n-C23 to fresh ant corpses and observed the reaction of infected and uninfected workers to control and manipulated corpses. Infected ants appeared to be more peaceful towards infected but not uninfected non-nestmates. Adding n-C23 to uninfected corpses resulted in reduced aggression in uninfected ants. This supports the hypothesis that n-C23 acts as a 'pacifying' signal. Our study indicates that parasitic interference with the nestmate discrimination of host ants might eventually change colony structure by increasing genetic heterogeneity in infected colonies.

Ant Foragers Compensate for the Nutritional Deficiencies in the Colony.

Achieving nutritional homeostasis is crucial for the fitness of all living organisms [1]. Using "collective wisdom," ants have been shown to excel at making rapid and appropriate decisions under various contexts [2, 3], including foraging [4-7]. Ants often use pheromone trails to share information about food resources [8-10], a process allowing them to focus their foraging activity on the best food source available [7, 11-14]. However, what constitutes the best food source depends on the nutritional context of the colony in relation to its food environment [15]. In this study, we exposed ant colonies to various nutrient deficiencies and observed their compensatory nutritional responses. Ants were deprived of carbohydrate, sterol, protein, a subset of amino acids, or a single amino acid. We found that ants were rapidly able to match their foraging decisions to their nutritional needs, even if the deficiency concerned a single amino acid. An individual-based model demonstrates that these impressive feats of nutritional compensation can emerge from the iterative process of trail-laying behavior, which relies on a simple individual decision: to eat or not to eat. Our results show that, by adjusting their feeding behavior at the individual level, ants sustain homeostasis at the colony level.

Morphometric characteristics and COI haplotype diversity of Arctodiaptomus spinosus (Copedoda) populations in soda pans in Hungary.

Arctodiaptomus spinosus (Daday, 1891) is a characteristic species of the soda pan zooplankton in the Great Hungarian Plain. The biogeographical distribution of the species is interesting, since its range expands from the Pannonian Biogeographic region to the other side of the Carpathians, occurring in saline lakes in Eastern Anatolia, Armenia, Iran and in temporary waters in Ukraine. Our investigations focused on the morphometric characteristics and the COI haplotype diversity of four Hungarian populations in the Kiskunság area. We detected substantial morphological differences between the Böddi-szék population and the rest of the sampling sites, however considerable differences were not observable in the COI haplotypes in the populations. The 20 animals investigated for COI haplotypes belonged to the same haplotype network. Tajima's D indicated departures from the neutral Wright - Fisher population model and suggested population expansion. The genetic composition of Arctodiaptomus spinosus populations in the Kiskunság area is rather uniform.

Lock-picks: fungal infection facilitates the intrusion of strangers into ant colonies.

Studies investigating host-parasite systems rarely deal with multispecies interactions, and mostly explore impacts on hosts as individuals. Much less is known about the effects at colony level, when parasitism involves host organisms that form societies. We surveyed the effect of an ectoparasitic fungus, Rickia wasmannii, on kin-discrimination abilities of its host ant, Myrmica scabrinodis, identifying potential consequences at social level and subsequent changes in colony infiltration success of other organisms. Analyses of cuticular hydrocarbons (CHCs), known to be involved in insects' discrimination processes, revealed variations in chemical profiles correlated with the infection status of the ants, that could not be explained by genetic variation tested by microsatellites. In behavioural assays, fungus-infected workers were less aggressive towards both non-nestmates and unrelated queens, enhancing the probability of polygyny. Likewise, parasitic larvae of Maculinea butterflies had a higher chance of adoption by infected colonies. Our study indicates that pathogens can modify host recognition abilities, making the society more prone to accept both conspecific and allospecific organisms.

The effects of fungal infection and physiological condition on the locomotory behaviour of the ant Myrmica scabrinodis.

Parasite infection often results in alterations in host behaviour. These changes vary greatly in their magnitude, from slight shifts in the time spent by the host performing a given activity to the appearance of novel behaviours. The effects of parasites can differ with the age and the physiological condition of the host. Rickia wasmannii is an ectoparasitic fungal symbiont in Myrmica ants that covers the whole body surface of the host and reduces its lifespan. The fungus is present in both young and old individuals, making it an optimal subject for the study of age-related parasitic effects. We tested the effect of fungal infection on the locomotory activity of the Myrmica scabrinodis ant in different age categories. The fat content of workers was measured as a proxy for their physiological status. Based on our findings, old workers bore more thalli and were leaner than young individuals, while they tended to move at higher speeds and with a lower degree of meandering. Young individuals covered smaller distances, at slower speeds and with a higher degree of meandering. Contrary to our expectations, the infection intensity of R. wasmannii affected neither the fat content nor the locomotory activity of ant workers. However, the two age classes seem to have different strategies with regards to the relationship between fat content and distance covered. Our results suggest that characteristics of locomotory activity differ between the age classes in many respects, and are also influenced by their physiological status, but parasitism by R. wasmannii does not seem to have a straightforward effect on any of the variables studied.

Distribution of the myrmecoparasitic fungus Rickia wasmannii (Ascomycota: Laboulbeniales) across colonies, individuals, and body parts of Myrmica scabrinodis.

The ant species Myrmica scabrinodis plays a markedly important ecological role through much of the humid grasslands of Eurasia. It hosts a species-rich community of pathogens and parasites, including Rickia wasmannii, an enigmatic member of entomoparasitic laboulbenialean fungi. This study provides a descriptive ecology of R. wasmannii by characterizing its prevalence and distribution across several hierarchical levels: colonies, individuals, and anatomic body parts. Infections were restricted to a single ant species, M. scabrinodis, and infected colonies occurred predominantly in wet habitats. Infections tended to be highly prevalent within infected colonies, often reaching 100% sample prevalence among workers. Individual infections exhibited an aggregated distribution typical to host-parasite systems. Workers from the aboveground part of nests (presumably older ones acting as foragers) were more infected than those from the belowground part. Fungal thalli could be found all over the body of the hosts, the head and the abdomen being the most infected parts of the body. The fungi's distribution among host body parts statistically differed between low versus high-intensity infections: the initial dominance of the head decreased with advancing infection. These findings may provide baseline data for future comparative or monitoring studies.

Rickia wasmannii increases the need for water in Myrmica scabrinodis (Ascomycota: Laboulbeniales; Hymenoptera: Formicidae).

The order Laboulbeniales (Fungi, Ascomycota) is a little-studied group of microscopic ectoparasites of invertebrates, mostly insects. The effects of Laboulbeniales species on their hosts are mostly unknown. Rickia wasmannii Cavara, 1899 is a common Laboulbeniales fungus occurring in Europe and is currently known to be a parasite of at least eight Myrmica ant species. R.wasmannii serves as a good model organism for Laboulbeniales-host interactions, as this species covers the host in a very high density, and infected host individuals can be easily collected in high numbers. The effect of R. wasmannii on the survival rate of its most common host species, Myrmica scabrinodis Nylander 1846, was therefore investigated in a laboratory experiment on an individual level. To enhance the results, environmental stresses were simulated by depriving infected and uninfected workers of water and food. The survival of individuals was recorded hourly until the death of the last individual. Infected specimens were significantly more sensitive to the withdrawal of food and water than uninfected specimens. When we tested for water consumption, we found that infected ants spent more time consuming water than uninfected ants. Therefore, it is possible that infected ants must replace the loss of water. Based on these results, R. wasmannii substantially decreases the chances and time of survival of infected individuals, at least in resource-limited environments, which suggest that R. wasmannii has a negative effect on its host.