Effects of time-since-fire on ant-plant interactions in southern Brazilian grasslands
Introduction
Natural or anthropogenic disturbances are inherent to ecosystem dynamics, which strongly drive biological communities structure and distribution patterns worldwide (Bond et al., 2005). Open ecosystems, such as grasslands and savannas, are evolutionarily related to burnings and large herbivore grazing (Veldman et al., 2015). Consequently, under disturbance suppression policies (e.g. as in natural reserves and parks) these open ecosystems usually undergo a net loss of its original biodiversity (Abreu et al., 2017). For instance, in southern Brazilian grasslands (Campos Sulinos) the intermittent removal of the aboveground biomass by grazing and/or fire is critical to maintain plant diversity by preventing the dominance of tussock grasses, woody encroachment, and forest expansion (Overbeck et al., 2007, Pillar and Vélez-Martin, 2010). The formation of open gaps in the plant communities stimulates the recruitment of a range of low-competitive small plant species (i.e. geophytes, forbs, sub-shrubs), that otherwise would not be frequent in local communities without disturbances (e.g. Araújo et al., 2013, Fidelis et al., 2014). Animal communities, in turn, rely on ecosystem conditions (i.e. biotic/abiotic environment) and resources (i.e. food availability) that vary with disturbance (Hovick et al., 2017, Andersen, 2018), triggering multithropic ecological interactions and ecosystem services (Van Nuland et al., 2013). Maintaining disturbance regimes in grassland/savanna ecosystem are of great conservation concern, therefore ecosystem assessment and monitoring though the use of indicators of ecological change is highly required.
The major role of ecological indicators is to report on the state (condition of health) of ecosystems, especially in response to environmental change. Historically, ecological indicators were primarily based on parameters such as the presence of target species or simple community metrics (e.g., species richness) (Niemi and McDonald, 2004). In recent decades, ecological indicators have been more broadly applied (i.e., from genes to landscapes), and it is recommended that monitoring programs use a suite of indicators representative of the structure, composition, and specially the function of ecological systems (Dale and Beyeler, 2001). Intrinsic to this approach is the understanding that biodiversity assembly and the maintenance of ecological functions are largely influenced by biotic interactions (Duffy et al., 2007; Valiente-Banuet et al., 2015). Ecological networks are used to represent direct species interactions within the ecosystem, and are considered a powerful tool in applied ecology (e.g., Ferreira et al., 2013, Kaiser-Bunbury and Blüthgen, 2015).
A biotic interaction particularly sensitive to disturbances is the ant-plant interaction mediated by extrafloral nectaries (EFN) (Piovia-Scott, 2011). Extrafloral nectaries are glands that produce nectar, not directly related to pollination (Koptur, 1992), and attract ants that commonly offer protection against insect herbivory (Rico-Gray and Oliveira, 2007, Del-Claro et al., 2016). A diversity of ants and EFN-bearing plants interact in the ecosystems, generating complex mutualistic networks (see Del-Claro et al., 2018), which allow us to evaluate disturbance effects on the proprieties and structure of these interactions (Oliveira and Koptur, 2017). These networks show a nested pattern, with a central core of generalist ant species that comprises most of the interactions, and peripheral ants with few interactions (Guimarães et al., 2006). This core of generalist ants consists mostly of territorial and competitively superior species (i.e., with massive recruitment and/or aggressive behavior) that limit access to the resource by submissive peripheral species, thus strongly influencing the structure and functioning of the whole community (Dáttilo et al., 2014a, Costa et al., 2016). Furthermore, ant-plant interactions are organized by several factors such as habitat features (i.e. abiotic proprieties, Rico-Gray et al., 2012), plant architecture, phenology and ontogeny (e.g. Vilela et al., 2014, Lange et al., 2013), and EFN-productivity (e.g. Fagundes et al., 2017). Events in ecosystems causing variation on these factors may directly affect such mutualistic interactions and their outcomes (protective services) over time.
Recently, ant-plant interaction approaches were used to monitor ecosystem changes after fire in Brazilian savannas demonstrating to be useful bioindicators. Alves-Silva and Del-Claro (2013) found that post-fire resprouted Banisteriopsis campestris (Malpighiaceae) presented enhanced quality of extra-floral nectar, which sustain increased abundance of defensive ants, and reduced levels of herbivory in comparison to unburned plants. Fagundes et al. (2018) detected low fire effects on EFN-visiting ant diversity and their interaction patterns with plant communities, which were considered an indicator of ecosystem resistance. Costa et al. (2018) found immediate negative fire consequences in the frequency and diversity of ant-plant interactions, which reached similar values of unburnt areas about six months after fire, highlighting ecosystem resilience. Despite these early efforts to understand fire effects on plants and ants in savannas, how disturbance-induced habitat changes influences these interactions in other fire-prone ecosystems in Brazil remains completely unexplored.
Here, we propose to study EFN-bearing plants and their visiting ants across a post-fire successional gradient, i.e. sites from a few months to more than two years since the last fire, in natural ungrazed grasslands in South Brazil. For this, we selected an EFN-bearing sub-shrub from the study region (Chamaecrista repens Vogel H. S. Irwin & Barneby; Fabaceae-Caesalpinioideae) as a study model. We explored time-since-fire effects on a suite of indicators in this system: (i) habitat structure: vegetation height, bare soil, and grass cover; (ii) C. repens populations: density of individuals, size, number of reproductive structures, and EFNs; (iii) EFN-visiting ant communities: abundance and richness; and (iv) individual-based ant-plant networks: d’– interaction specialization index, which measures how each ant species interacts with plant individuals (Blüthgen et al., 2006), and number and composition of ants from the network central core. We specifically have the following predictions:
- (i)
Vegetation of old-burnt grasslands will be taller, and with increased cover of caespitose tussock grasses in comparison with freshly-burnt grasslands, which will present increased habitat openness (bare soil) (Overbeck et al., 2005, Podgaiski et al., 2014).
- (ii)
Populations of C. repens will be reduced in old-burnt grasslands, and their individuals would be less vigorous (decreased in size, and number of reproductive structures) and with diminished densities of EFNs in comparison with freshly-burnt grasslands. We have these expectations because low-competitive small plant species usually suffer a strong fitness reduction in disturbance-suppressed grasslands, or in grasslands with alleviation of disturbance regimes, due to competition for light/space with tall vegetation, especially tussock grasses (Overbeck et al., 2005, Fidelis et al., 2012). On the other hand, we expect the transitory habitat openness of recently burned grasslands to benefit C. repens populations that could resprout from underground organs or re-establish by seed germination, and thus invest in vegetative growth, reproduction and EFNs to attract protective ants.
- (iii)
EFN-visiting ant communities will be more abundant and species-rich in plants from freshly-burnt grasslands. Ants should respond positively to C. repens size, resource availability (EFNs density), and habitat openness. We expect an increase in ant species richness with C. repens size due to species-area relationships (i.e., C. repens as resource islands; MacArthur and Wilson, 1967), so that more ant species could coexist in larger plants through spatial segregation in EFNs use (Dáttilo et al., 2014b). We postulate a relationship between ant densities and EFN densities according to the resource concentration hypothesis (Root, 1973), so that ants would be more abundant in plants offering more resources (Blüthgen et al., 2000, Lange et al., 2017, Costa et al., 2018). Finally, we expect more EFN-visiting ant abundance and richness in plants established in open grasslands, because habitat simplification promotes ant activity, i.e. allowing for a greater foraging distance, speed, and efficiency (e.g., Parr et al., 2007, Gibb and Parr, 2010).
- (iv)
Based on the fire-induced habitat changes, ant-plant ecological networks in freshly-burnt grasslands will present ant species interacting with more plant individuals (lower individual interaction specialization) than old-burnt grasslands. Moreover, as the core of generalist ant species is known to be stable in networks across geographical distances (Dáttilo et al., 2013), plant phenology (Lange et al. 2013), and even after drastic disturbances such as hurricanes (Sánchez-Galván et al., 2012), we expect them to be consistent across the post-fire successional gradient.
Section snippets
Study area and plant model
We conducted the study in natural grassland patches at the Parque Natural Municipal Sain’t Hilaire (PNMSH) (30°5′ S, 51°5′ W, 82 m a.s.l.), Viamão municipality, Rio Grande do Sul state, Brazil (Fig. 1A). The ecosystem from the study region belongs to the Pampa biome (Campos Sulinos; Overbeck et al., 2007). The climate regime is humid subtropical (Cfa) according to Köppen’s classification, with mean temperature around 22° C and mean annual rainfall of 1.400 mm (Alvares et al., 2013).
The PNMSH
Grassland habitat structure
Grassland vegetation height was different among all the time-since-fire categories (Table 1), ranging from an average of 10 cm in freshly-burnt to 30 cm in old-burn patches. In the old-burnt patches we found an increased cover of grasses along with a low proportion of bare soil in comparison to freshly-burn patches. The intermediated-burnt patches did not differ from the freshly or old in relation to grass cover and bare soil (Table 1).
Chamaecrista repens populations
We found different C. repens population densities among the
Discussion
By using a suite of structural and functional indicators (i.e., habitat structure, plant populations, ant communities, and ecological networks), we explored ecosystem changes across a post-fire successional gradient in grasslands of South Brazil. We first show a marked variation in habitat structure and in EFN-bearing plant populations (C. repens) caused by the time since the last fire. As expected, freshly-burnt grasslands favored the fast recruitment, development and reproduction of C. repens
CRediT authorship contribution statement
Carolina Veronese Corrêa da Silva: Conceptualization, Methodology, Formal analysis, Investigation, Data curation, Writing - original draft, Visualization. Camila da Silva Goldas: Conceptualization, Methodology, Investigation. Wesley Dáttilo: Methodology, Writing - review & editing. William Dröse: Investigation, Writing - review & editing. Milton de Souza Mendonça: Resources. Luciana Regina Podgaiski: Conceptualization, Methodology, Validation, Formal analysis, Writing - review & editing,
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
We thank the staff of the Natural Municipal Park Saint’Hilaire for the fieldwork assistance. C.S. Goldas received PhD scholarship from CAPES, Brazil. W. Dröse received PhD scholarship from CNPq, Brazil. M.S.M. Jr. received Research Productivity grants from CNPq, Brazil (309616/2015-8). L.R. Podgaiski received Post-Doc grants from CAPES (PNPD), Brazil.
References (86)
- et al.
Litter-twig dwelling ant species richness and predation potential within a forest fragment and neighboring coffee plantations of contrasting habitat quality in Mexico
Agriculture, Ecosystems & Environment
(2003) - et al.
Resilience to fire and climate seasonality drive the temporal dynamics of ant-plant interactions in a fire-prone ecosystem
Ecol. Indic.
(2018) - et al.
Challenges in the development and use of ecological indicators
Ecol. Indic.
(2001) - et al.
Secretory activity of extrafloral nectaries shaping multitrophic ant-plant-herbivore interactions in an arid environment
J. Arid Environ.
(2015) - et al.
Limited effects of fire disturbances on the species diversity and structure of ant-plant interaction networks in Brazilian Cerrado
Acta Oecol.
(2018) - et al.
What do we know about the effects of landscape changes on plant–pollinator interaction networks?
Ecol. Indic.
(2013) - et al.
Does disturbance affect bud bank size and belowground structures diversity in Brazilian subtropical grasslands?
Flora
(2014) - et al.
Food source quality and ant dominance hierarchy influence the outcomes of ant-plant interactions in an arid environment
Acta Oecol.
(2018) - et al.
Brazil’s neglected biome: The South Brazilian Campos
Perspect. Plant Ecol. Evol. Syst.
(2007) - et al.
Adaptive strategies in burned subtropical grassland in Southern Brazil
Flora
(2007)
The South Brazilian grasslands - a South American Tallgrass Prairie? Parallels and implications of fire dependency
Perspect. Ecol. Conserv.
Conditional outcomes in ant-plant- herbivore interactions influenced by sequential flowering
Flora
The biodiversity cost of carbon sequestration in tropical savanna
Sci. Adv.
The ALL Protocol
Patterns of leaf development and herbivory in a tropical understory community
Ecology
Köppen's climate classification map for Brazil
Meteorol. Zeitschrift.
Post fire resprouting of Banisteriopsis malifolia (Malpighiaceae) and the role of extrafloral nectars on the associated ant fauna in a Brazilian Savanna
Sociobiol.
Effect of post-fire resprouting on leaf fluctuating asymmetry, extrafloral nectar quality, and ant-plant-herbivore interactions
Naturwissenschaften
Responses of ant communities to disturbance: five principles for understanding the disturbance dynamics of a globally dominant faunal group
J. Anim. Ecol.
Temporal turnover of species maintains ant diversity but transforms species assemblage recovering from fire disturbance
Sociobiol.
Fire drives the reproductive responses of herbaceous plants in a Neotropical swamp
Plant Ecol.
Guia para os gêneros de formigas do Brasil, ed
INPA, Manaus.
Fitting linear mixed-effect models using lme4
J. Stat. Softw.
How plants shape the ant community in the Amazonian rainforest canopy: the key role of extrafloral nectaries and homopteran honeydew
Oecologia
Measuring specialization in species interaction networks
BMC Ecol.
The global distribution of ecosystems in a world without fire
New Phytol.
Unidades de conservação e os campos do Rio Grande do Sul
Revista Brasileira de Biociências
Nectar- and pollen-gathering Cephalotes ants provide no protection against herbivory: a new manipulative experiment to test ant protective capabilities
Acta Ethol.
O gênero Chamaecrista Moench (Leguminosae Caesalpinioideae) no Rio Grande do Sul. Iheringia
Ser. Bot.
Cobertura vegetal atual do Rio Grande do Sul
Few ant species play a central role linking different plant resources in a network in rupestrian grasslands
PLoS One
Spatial structure of ant–plant mutualistic networks
Oikos
Ant dominance hierarchy determines the nested pattern in ant-plant networks
Biol. J. Linnean Soc.
Individual-based ant-plant networks: diurnal-nocturnal structure and species-area relationship
PLoS ONE
Loss and gains in ant–plant interactions mediated by extrafloral nectar: fidelity, cheats, and lies
Insect Sociaux
The complex relationships between ants and plants into tropical ecological networks
Ant species identity has a greater effect than fire on the outcome of an ant protection system in Brazilian Cerrado
Biotropica
The functional role of biodiversity in ecosystems: incorporating trophic complexity
Ecol. Lett.
The need for a consistent fire policy for Cerrado conservation
J. Appl. Ecol.
Availability of food and nesting-sites as regulatory mechanisms for the recovery of ant diversity after fire disturbance
Sociobiol.
Differences between ant species in plant protection are influenced by the production of extrafloral nectar and related to the degree of leaf herbivory
Biol. J. Linnean Soc.
Temporary grazing exclusion promotes rapid recovery of species richness and productivity in a long-term overgrazed Campos grassland
Restor. Ecol.
Fire intensity and severity in Brazilian Campos grasslands
Interciência
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