Summiting Behaviour

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A diverse set of pathogens have evolved the ability to manipulate the behavior of their insect hosts to maximise their own reproductive success. These pathogens cause the infected hosts to climb vegetation and clamp their mandibles in a stereotypical ‘death-grip’ bite. They either die in this position, or wait for extended periods.

This behaviour has been termed Wipfelkrankheit, tree-top disease, topping behaviour or summit disease (Marikovsky 1962, Schmid-Hempel 1998; Salwiczek & Wolfgang, 2009), and summit behaviour.

In fungal infections (involving several species of the fungal family Entomophthoraceae (Zygomycota, Entomophthorales)), the fungus kills the ant once it is in position, sprouts a stalk and releases infective spores into wind currents where they can be effectively disseminated.

If the infection is caused by a trematode, the ant waits at the tips of the vegetation until it is eaten by a passing vertebrate, the primary host of the trematode. This behaviour will be repeated every night until the ant is eaten by a vertebrate host in which the parasite can fully mature and complete its life cycle.

  • Pandora formicae infection stages in Formica polyctena host.
    (A) Dead ant before outgrowth of fungal conidiophores, with visible rhizoids (arrow).
    (B) Sporulating ant cadaver with visible white, dense rings of conidiophores (arrow).
    (C) Approximate timeline of infection progress in one host. Fungal structures are shown in black. Ants get infected (1) after conidia have attached to and penetrated the cuticle. The fungus later proliferates within host hemocoel (2), until nutrients are depleted and the infected ant is close to death. At that time the behavior of the host is altered so the ant seeks an elevated position on vegetation (3), on which it will die shortly thereafter, with its mandibles now locked on the plant surface, and with fungal rhizoids outgrowing and assisting fixation to vegetation (4). Fungal conidiophores will soon after (depending on humidity and temperature) grow out through soft parts of ant exoskeleton to produce and actively discharge conidia (5). (From Małagocka et al., 2015, Fig. 1)

Botnevik et al. (2016) note that when searching for infected ants they sampled between 1400 and 1700 hr. This time period may not be optimal in terms of achieving the greatest number of ants, which are more common in the morning and evening hours (Spindler et al., 1986). However, it was selected to avoid collecting ants infected by the entomopathogenic fungus Pandora formicae, which induces the same summiting behavior as D. dendriticum (Malagocka, 2016). Ants infected with P. formicae are almost exclusively found in tetany in the evening after which the fungus rapidly kills the ant, produces conidiophores, and spreads its conidia spores during the night and early morning hours (Malagocka, 2016).

Trinh et al. (2021) conducted field and transcriptome studies and found that the host circadian clock, olfaction and communication may be disrupted in fungus-infected ants, which suggests that the fungus is affecting ant foraging activity and effectivity. In Camponotus floridanus, foraging behaviour was notably affected during early stage Ophiocordyceps infection. Specifically, they found that Ophiocordyceps-infected ants became arrhythmic in their activity patterns, were less likely to participate in effective foraging efforts and seemed less able to communicate with their nestmates compared to healthy ants. They hypothesized that these changes in behaviours are adaptive to Ophiocordyceps transmission since they reduce the chance of aggressive interference by nestmates.

Salwiczek & Wolfgang (2009) took an ethological perspective of “summit-disease” and found that it unfolds as being the initial common element (climbing up) of different behaviours such as sleeping and standing lookout. To differentiate between those behaviours, one has to pay close attention to additional behaviour components like activity-rhythm, mandible movements (e.g. fastening to the substrate or eating respectively), or conspecifics’ responses in the above cases. It does not come as a surprise, then, if phylogenetically distant parasites such as a fungus and a fluke evoke the same dormant sleeping behaviour in an infected ant, but two different flukes might elicit two different ant behaviours that share a common first component. Of course, an early death of the infected animal (as in the fungus-infected ant) may prevent the full behaviour performance required for analysis.

de Bekker et al. (2018) note that ants killed by the fungus Pandora have been found biting grasses and twigs in the proximity of foraging trails and nests (Loos-Frank & Zimmermann 1976, Boer 2008, Malagocka & al. 2017). Malagocka and colleagues speculate that infected Formica polyctena workers die near the nest where humidity levels are optimal for Pandora formicae sporulation rather than inside the nest where humidity would be too low (Coenen-Stass & al. 1980, Steinkraus 2006). Similar to Ophiocordyceps-infected host species, F. polyctena foragers appear more susceptible to Pandora than their nestmates that fulfill tasks inside the nest (Malagocka & al. 2017). Fixation at elevated positions likely facilitates ideal spore dispersal while at the same time protecting the cadavers from nestmates that would normally dispose or remove dead ants from the nesting area (Loos-Frank & Zimmermann 1976, Boer 2008).