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And Their Parasites: Effects of Parasitic Manipulations and Host Responses on Ant Behavioral Ecology Charissa De Bekker, Ian Will, Biplabendu Das & Rachelle M.M

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And Their Parasites: Effects of Parasitic Manipulations and Host Responses on Ant Behavioral Ecology Charissa De Bekker, Ian Will, Biplabendu Das & Rachelle M.M ISSN 1997-3500 Myrmecological News myrmecologicalnews.org Myrmecol. News 28: 1-24 doi: 10.25849/myrmecol.news_028:001 28 August 2018 Review Article The ants (Hymeno ptera: Formicidae) and their parasites: effects of parasitic manipulations and host responses on ant behavioral ecology Charissa de Bekker, Ian Will, Biplabendu Das & Rachelle M.M. Adams Abstract Ants can display modified behaviors that represent the extended phenotypes of genes expressed by parasites that infect them. In such cases, the modifications benefit the parasite. Alternatively, displayed behaviors can represent host responses to infection that benefit colony fitness. Though some enigmatic examples of behavioral manipulation have been reported, parasitism of ants and its effects on ant behavior and ecology are generally poorly understood. Here, we summarize some of the present-day literature on parasite-ant interactions. Our main focus is on interactions that change host behavior so drastically that infected ants play a seemingly different societal and, perhaps, ecological role. We highlight the parallels that can be found across parasite-ant symbioses that result in manipulated behaviors, such as summiting, phototaxis, substrate biting, and wandering. We also point out the many present knowledge gaps that could be filled by efforts ranging from novel parasite discovery, to more detailed behavioral observations and next-generation sequencing to start uncovering mechanisms. Key words: Parasites, ants, behavior, extended phenotype, manipulation, review. Received 17 June 2018; revision received 4 August 2018; accepted 10 August 2018 Subject Editor: Andrew V. Suarez Charissa de Bekker (contact author), Ian Will & Biplabendu Das, University of Central Florida, Department of Biology, Orlando, FL 32816, USA. E-mail: [email protected] Rachelle M.M. Adams, The Ohio State University, Department of Evolution, Ecology and Organismal Biology, Columbus, OH 43212, USA. Introduction Parasites exploit all free-living organisms and comprise drained further by reallocating energy to the display of the majority of species on Earth (Windsor 1998, Schmid- resistance behaviors (Rigby & al. 2002). Furthermore, Hempel 2011). Their biomass in ecosystems is substantial, parasites that modify the behavior of intermediate hosts, and they play important ecological roles in shaping com- to ascertain trophic transmission to ultimate host pred- munities (Kuris & al. 2008). One of the best investigated ators, drastically affect food webs (Lafferty & Morris social insects, Apis mellifera Linnaeus, 1758, has over 70 1996). In fact, parasites can alter the behavior of their host described macro- and micro-parasites (Schmid-Hempel to such an extent that they change its ecological function 1998). While this number is impressive, it is likely an un- as infected animals can react differently to abiotic stim- derestimate and not unique to A. mellifera. Other social in- uli compared to their conspecifics. They can also display sect hosts, with societies equal in complexity and size, have different activity levels, sounds, smells, distribution, and few or no reported parasite species. This may be attributed social roles (Moore 1995). to a lack of commercial interest and limited funding for While parasites are biomass rich, so are ants (Fittkau such investigations, instead of a true lack of parasites & Klinge 1973, Erwin 1989). Ants are among the most (Schmid-Hempel 2011). The high levels of biodiversity abundant animal groups and often comprise more than and biomass of parasites alter energy flux to other trophic 80% of the arthropods in tropical rain forests (Hölldo- levels and change community structure through modified bler & Wilson 1990, Davidson & Patrell-Kim 1996). competitive abilities. Behavior is central to enormous im- This success can be attributed to their complex social pacts on host growth rates as it influences factors such as organization and intriguing behavioral ecology. Ant spe- seed dispersal, prey capture, and soil excavation. Beyond cies display an array of unique behaviors that should be the consumptive effects of parasites, host energy can be studied at the individual, caste, and colony level, then © 2018 The Author(s). Open access, licensed under CC BY 4.0 https://creativecommons.org/licenses/by/4.0 placed in the context of the species’ natural environment In recent years, manipulating parasites and their hosts (Sudd & Franks 1987). Parasites are key components has gained the interest of researchers and the general pub- of that environment as they influence ant behaviors by lic. New manipulative species interactions are being dis- providing pressures that select for adaptive host behav- covered (Steinkraus & al. 2017). Yet, there are many sig- ioral traits, such as parasite recognition, prevention, and nificant outstanding questions, even in systems that were defense (Lozano 1991, Agnew & al. 2000). In addition described decades ago (Badie & al. 1973, Loos-Frank & to displaying behaviors that protect individuals and the Zimmermann 1976, Romig & al. 1980). Next-generation colony against parasites, infected ants can also be viewed sequencing has made it possible to unveil gene expression as the parasites’ extended phenotype and display behav- and potential mechanisms underlying parasitically altered iors that benefit the parasite’s life cycle and transmission host behaviors (de Bekker & al. 2015, Malagocka & al. (Dawkins 1982). Such manipulated behaviors can be very 2015, Feldmeyer & al. 2016). Such efforts can reveal how apparent, such as the novel, fungus-induced substrate and when parasites influence host activity, especially in biting behavior observed in infected worker ants that are organisms that are as experimentally approachable as thought to be mainly of the foraging caste (Boer 2008, An- ants. We aim to create a broader interest in parasite-ant dersen & al. 2009). Modifications can also be subtler, as interactions by summarizing what is known and high- described for a cestode that reduces activity of infected lighting knowledge gaps waiting to be filled. We hope to individuals of the nursing caste and aggression displayed entice more myrmecologists and behaviorists to integrate by uninfected nestmates, to seemingly facilitate trophic the effect that parasites might have on the behavior and transmission towards the woodpecker host (Plateaux biology of their focal ant species. 1972, Scharf & al. 2012, Beros & al. 2015). The altered Parasites influencing ant behavior behavior of infected individuals, such as reduced or less effective foraging activity, could thus impact the fitness of Phenotypic changes in the host – as a result of parasite the colony as a whole. Parasites could also affect behavior pressures and infection – can be adaptive to that host and at the colony level, for instance, through changes in the aid its survival. Alternatively, parasites can manipulate chemical profiles of infected individuals, as reported for host physiology, morphology, life history, and behavior, certain ectoparasites (e.g., Csata & al. 2017). This makes to directly benefit their own survival (Poulin & Thomas the colony’s gestalt odor (i.e., the uniform odor of a col- 1999, Thomas & al. 2010). Adaptive manipulation of host ony) more heterogeneous and relaxes the margin of error behavior can range from slight changes in existing be- used by uninfected nestmates when assessing chemical haviors to the induction of completely novel ones (Poulin profiles to distinguish kin from non-kin. This could lead to 1994, Thomas & al. 2002). Ants are favorable parasite increased susceptibility to competing conspecifics, social targets because of their dominance in most ecosystems parasites and parasitoids that drain the colony’s resources and ubiquity among habitat types. Furthermore, because and reduce colony fitness. Alternatively, certain behavioral of their social tendencies (e.g., nest living, food sharing, responses to infection might represent mere side-effects brood care), ant societies can spread parasites among without clear functions. Deciphering where parasitic ma- colony members (Cremer & al. 2007, Hughes 2012, Kon- nipulation begins and host response ends is, thus, a com- rad & al. 2012, Beros & al. 2015). As such, parasite-in- plicated endeavor that requires thorough experimentation duced behavioral shifts in ants have been widely reported. to determine which of the interacting organisms, if at all, However, we suspect the records to be far from complete adaptively benefits from the altered behavior. (Schmid-Hempel 1998). We summarize and discuss some Behavioral changes are especially important to con- of the present-day literature on entomopathogenic vi- sider in ants because of their role as ecosystem engineers ruses, prokaryotes, fungi, protozoans, helminths, and (Folgarait 1998, Griffiths & al. 2018). Ants are re- insects, with our main focus on those that manipulate ant sponsible for a substantial part of the nutrient redistri- behavior. This reveals that information on ant-infecting bution performed by animals in the rainforest. Moreo- viruses, prokaryotes, and protozoans is largely lacking. ver, their removal of food resources is not compensated More in-depth research on fungi, helminths and para- by other invertebrates and vertebrates when ants are sitizing insects is actively underway. Moreover, this review removed from a habitat. This makes them key players demonstrates the parallels between observed manipulated in maintaining rainforest ecosystem processes
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