Mutualisms - interspecific cooperative interactions in which both partners benefit (Bronstein 2009, Janzen 1975), are essential for the origin and ongoing maintenance of biodiversity (Andresen et al. 2018, Bronstein et al. 2006, Thompson 1999, Tylianakis et al. 2008). A range of essential ecosystem services such as pollination, seed dispersal and cycling of nutrients are the result of mutualistic interactions (Potts et al. 2010, Terborgh et al. 2008, Wilson 2009). However, we have a limited understanding of how mutualist interactions respond to disturbances, either natural or anthropogenic (Teixido et al. 2022, Vasconcelos et al. 2020, Vidal et al. 2021).
Ants are an ecologically dominant faunal group globally that feature in many mutualistic interactions (Bronstein 2015, Rico Gray and Oliveira 2007). Such interactions include the provision of protection services to partners that provide food resources in the form of liquid carbohydrate (Davidson 1997, Hölldobler and Wilson 1990). Chief among these carbohydrate resources is honeydew produced by hemipteran insects (Blüthgen et al. 2000, Del-Claro 2004) and plant secretions from extrafloral nectaries (EFNs) (Blüthgen et al. 2000, Davidson et al. 2003). Both honeydew and extrafloral nectar specifically attract ants (Bentley 1977, Blüthgen et al. 2000), which then repel or kill insect predators and herbivores (Del-Claro et al. 2016, Heil 2015, Zhang et al. 2012), potentially increasing the growth and reproductive success of the hemipteran and plant partners (Nascimento and Del-Claro 2010, Styrsky and Eubanks 2010). Conversely, liquid carbohydrate is a key resource for ants, especially for behaviourally dominant species that require it for fuelling their large colony sizes, high rates of activity and aggressive behaviour (Blüthgen et al. 2000, Davidson et al. 2004, Holway et al. 2002, Lach et al. 2020). Honeydew is an especially valuable resource because it can be produced continuously in large quantities that are predictable in space and time (Blüthgen et al. 2000, Fiala et al. 1990, Rico-Gray and Oliveira 2007). Moreover, it contains a broader spectrum of sugars than does extrafloral nectar (Blüthgen et al. 2004a). Honeydew tends to attract behaviourally dominant dolichoderines and formicines that possess adaptations for processing large quantities of liquid carbohydrate, and such behaviourally dominant species provide the best protection services because of their aggressive behaviour (Blüthgen et al. 2000, Davidson et al. 2004, Holway et al. 2002, Lach et al. 2020). In contrast, EFNs often attract behaviourally subordinate species that tend them opportunistically (Blüthgen et al. 2004b, Blüthgen and Fiedler 2004, Davidson et al. 2003).
Fire is a frequent and widespread disturbance shaping the biota and functioning of many ecosystems around the globe (Andersen et al. 2005, Bond et al. 2005, Bowman et al. 2009, Brando et al. 2019). The impact of fire on ants has been extensively studied (Vasconcelos et al. 2017; Andersen 2019), but little attention has been given to the effects of fire on their mutualistic interactions. The effects of fire on ants, and especially on the abundance of behaviourally dominant species, have important implications for the protection services provided by them in their mutualisms mediated by honeydew and EFNs. For example, a negative effect of severe fire on the outcome of mutualistic interactions mediated by EFN was attributed to changes in ant communities (Vasconcelos et al. 2020). Fire can also affect these mutualisms through stress-induced increases in the quality and quantity of nectar produced by EFNs, thus promoting ant attendance (Alves-Silva and Del-Claro 2013, Silva et al. 2020).
Here we use a long-term fire experiment in an Australian tropical savanna to examine the effects of different fire regimes on ant-honeydew and ant-EFN interactions as an indicator of mutualistic outcomes. Australian savannas are among the world’s most fire-prone biomes. Here, frequent fire promotes ant abundance and diversity because it produces an open habitat that is strongly favoured by the predominantly arid-adapted fauna (Andersen & Vasconcelos 2022). Australian savannas feature two of the world’s most behaviourally dominant ant genera in Iridomyrmex and Oecophylla, which have contrasting responses to fire (Andersen et al. 2007). Iridomyrmex is an arid-adapted ground-nesting genus that prefers open habitats; it suffers little direct mortality during fire because of the protection afforded by its soil nests, and its preferred open habitat is maintained by frequent fire (Parr & Andersen 2008, Andersen et al. 2014). In contrast, Oecophylla is a foliage-nesting, forest-adapted taxon that favours shady habitats; populations can suffer significant mortality during fire, and frequent fire reduces its habitat suitability (Parr & Andersen 2008, Andersen et al. 2014). Fire can therefore be expected to regulate the relative abundance of these dominant taxa as partners in interactions with plant-based liquid carbohydrate.
Our study documents the ant-hemipteran and ant-EFN partners at our site, along with the relative incidence of ant-honeydew vs ant-EFN interactions, and then asks the following key questions. First, to what extent do behaviourally dominant dolichoderines and formicines (highest quality mutualists) visit honeydew over extra-floral nectar? Second, do the incidences of ant-honeydew and ant-EFN interactions, and their relative incidence, vary among different fire regimes? Third, do honeydew or extra-floral nectar preferences of behaviourally dominant dolichoderines and formicines vary among fire regimes, thereby altering the relative incidence of higher quality mutualists? Finally, does frequent fire result in a switching of behaviourally dominant ant partners from forest-adapted Oecophylla to arid-adapted Iridomyrmex?