Abstract Frequent prescribed burns are essential to pine forest restoration and management. Research studies have assessed effects of prescribed fire and burn frequency on plants and vertebrates, but impacts of fire on terrestrial invertebrate communities are still poorly understood. This case study investigated effects of burning frequency on species richness and community composition of social insects (ants, Hymenoptera: Formicidae and termites, Blattodea: Isoptera) in fire-managed Southern longleaf pine flatwoods in central Florida. Community response to different fire frequencies was assessed: burned annually, every 2 yr, or every 3 yr, 30 yr unburned and 75 yr unburned. Richness was similar across all treatments, but ant community composition and species density significantly differed between frequently burned (1, 2, and 3 yr) and long-unburned (30 and 75 yr) treatments. Long-unburned treatments had higher ant abundance, but the species present were less characteristic of open canopy longleaf pine habitat than ants in frequently burned treatments. The annual burn treatment differed from 2-yr burn in species density, but to a lesser degree. Exotic species abundance was highest in frequently burned sites; only native species were detected in the 75-yr unburned plot. The red imported fire ant, Solenopsis invicta Buren (Hymenoptera: Formicidae), was detected in all regularly burned plots but not in long-unburned sites. Frequent burning at this site increased habitat suitability for ant species adapted to the sunny, open canopy, and diverse niches characteristic of longleaf pine forest; however, regular fire disturbance also increased the likelihood of exotic ant species establishment. ants, leaf litter, mesic flatwoods, prescribed fire, social insects Prior to European colonization of North America, the U.S. Southeastern Coastal Plain was dominated by the longleaf pine (Pinus palustris Mill.) (Pinales: Pinaceae) ecosystem, an open, fire-driven forest system of diverse floral and faunal communities that includes many rare plant and animal species (Oswalt et al. 2012). Approximately 3% of the original extent of these forests remains as longleaf pine today, and both federal agencies and private landholders have prioritized conservation and restoration of this ecosystem and its biodiversity (Van Lear et al. 2005, Mitchell et al. 2006, Oswalt et al. 2012). Prescribed burning is a widely used management strategy in southeastern pine forests, where burning every 1–3 yr is essential to maintaining the habitat’s diverse herbaceous and grassy ground cover, as it prevents hardwoods and other fire-intolerant species from invading, crowding, shading out, and significantly reducing ground cover species richness and composition (Kirkman et al. 2004, Van Lear et al. 2005, Oswalt et al. 2012, Ryan et al. 2013). Fire suppression, in addition to inducing vegetative differences, is accompanied by change in soils. The long-term absence of fire transforms longleaf pine into closed canopy forests with a buildup of less-flammable leaf litter, leading to significant increases in the amount of organic matter at the soil surface. This moist humus soil layer, with attendant processes such as fermentation, is not present in frequently burned stands (Switzer et al. 1979, Varner et al. 2005, Ryan et al. 2013). Burning during the growing season is often preferred by restoration professionals because it is favorable for the fruit set of wiregrass (Aristida stricta Michx.) (Poales: Poaceae), a dominant keystone ground cover species in longleaf pine forest (Wade et al. 2000). Not all fire regimes have equal effect, however, and individual species across taxa respond uniquely to different prescribed fire treatments (Lashley et al. 2014). A rich body of research on the effects of fire regimes, comprising parameters such as fire season, frequency, and intensity, highlights the importance of fire in maintaining the diversity of this ecosystem, including studies of flora (Platt et al. 1988, Glitzenstein et al. 1995, Alba et al. 2015), herpetofauna (Litt et al. 2001, Schurbon and Fauth 2003), birds (Tucker et al. 2004, Steen et al. 2013), and mammals (Lashley et al. 2015, Prince et al. 2016). Research on the impacts of fire on the invertebrate community lags behind that on plants and vertebrates (but see Folkerts et al. 1993, Provencher et al. 2002, Hanula and Wade 2003, Izhaki et al. 2003, Sullivan et al. 2003, Knight and Holt 2005, Campbell et al. 2008, Hanula et al. 2009, Hahn and Orrock 2015, Chitwood et al. 2017), despite the importance of invertebrates to essential ecosystem processes, including wood decay, seed dispersal, and soil aeration. Total arthropod species across longleaf pine ecosystems is estimated to be between four and five thousand species, with many restricted to particular habitat types (Folkerts et al. 1993). For example, arthropod community differences have been noted between sandhill and flatwoods habitats. Most existing studies of arthropods in longleaf pine ecosystems have taken place in longleaf sandhill habitat (Folkerts et al. 1993, Izhaki et al. 2003, Provencher et al. 2003, Knight and Holt 2005, Zanzot et al. 2010, Chitwood et al. 2017) and/or in forest burned during the dormant season (Hanula and Wade 2003, Izhaki et al. 2003, Sullivan et al. 2003, Knight and Holt 2005, Hanula et al. 2009). From studies across fire-driven systems, insect mortality has been positively linked to fire severity, and the mortality of litter-dwelling and surface-foraging insects is higher than subterranean, arboreal, or flying species (Swengel 2001, Wikars and Schimmel 2001). In studies of longleaf pine forests, species richness declines dramatically immediately post-fire (Izhaki et al. 2003, Knight and Holt 2005) (except for fire-favored beetles) (Sullivan et al. 2003), after which recolonization increases with time since burn (Izhaki et al. 2003, Knight and Holt 2005) likely correlated with vegetative regrowth (Swengel 2001, Wikars and Schimmel 2001). For example, ant species richness decreased after winter burning (Izhaki et al. 2003), followed by richness recovery 6 mo post-fire, with varied responses for individual ant genera (Hanula and Wade 2003). Extended fire suppression has been shown to lead to reduced arthropod densities in sandhill habitat, but even in long-unburned areas, prescribed fire during the growing season can lead to subsequent recuperation of the invertebrate community (Provencher et al. 2002). The evidence of recuperation suggests that fire management can help restore arthropod communities in unburned longleaf pine, which is encouraging given that fire severity in longleaf pine is often a consequence of high volumes of leaf litter, which is characteristic of long-unburned stands (Varner et al. 2000, 2005). However, it remains to be demonstrated that community composition at the species level and species-specific community functions can be recovered as well. Most studies of arthropods in longleaf pine have focused at a large taxonomic scale (usually orders or families) without species-level identification (Hanula et al. 2000, 2009; Pitts-Singer et al. 2002; Hanula and Wade 2003; Sells et al. 2015; Chitwood et al. 2017), or on a limited number of species within particular taxonomic groups (Folkerts et al. 1993, Sullivan et al. 2003, Knight and Holt 2005, Campbell et al. 2008, Zanzot et al. 2010, Hahn and Orrock 2015). Because responses to fire vary at the species level, it is important to understand species-specific responses of the arthropod community. In particular, there is a need to better understand how the timing of fire affects ecologically important arthropod groups, such as ants. Ants are important because they interact with every trophic level (Schultz and McGlynn 2000, Holway et al. 2002) as fungivores, scavengers, predators, granivores and, indirectly, as herbivores by tending sapsucking insects; this is also true in longleaf pine ecosystems. Ants are an important food source for many animals, including the endemic, endangered red-cockaded woodpecker (Hanula et al. 2000). They predate other arthropods as well as disperse and predate seeds (Schultz and McGlynn 2000, Stuble et al. 2010). Because of vegetative changes (Platt et al. 1988, Glitzenstein et al. 2012, Alba et al. 2015) and soil characteristics (Switzer et al. 1979, Varner et al. 2000) associated with different burn regimes, we expect species within ant communities to differentially respond both directly to the fire and subsequent fire-induced landscape changes dependent on their species-specific habitat requirements. Many, but not all studies indicate a simple, positive relationship between ant and plant community richness. Studies on dormant season burning found that the highest plant diversity in longleaf pine occurred in frequently burned (every 1–3 yr) mesic longleaf sites (Kirkman et al. 2004), and that plant diversity is improved by increasing fire frequency in flatwood sites (Glitzenstein et al. 2003). It is not clear if fire frequencies that promote high plant diversity also benefit ant species richness in longleaf pine ecosystems. Studies have alternately demonstrated decreases in ant richness as percent herbaceous ground cover increased (Lubertazzi and Tschinkel 2003) and, in contrast, significant increases in arthropod densities as a result of growing season burns (Provencher et al. 2002, 2003); however, these two papers report no significant correlation between plant species richness and arthropod species richness. While the timing of burning clearly influences plant and animal communities, the effects of regular growing season burns on ant communities and the services they provide remain poorly understood. One reason to focus on social insects in longleaf pine at the species level is to monitor invasive species of ants and termites, which threaten many of Florida’s native ecosystems, including longleaf pine. Ant diversity in Florida comprises at least 221 species, 52 of which are exotic (Deyrup 2017). Exotic ants are more likely to colonize disturbed habitats (Holway et al. 2002) and can disrupt interspecific native ant relationships (Human and Gordon 1996, Holway et al. 2002, Rodriguez-Cabal et al. 2012, Wilder et al. 2013). The red imported fire ant (Solenopsis invicta Buren) (Hymenoptera: Formicidae), e.g., competes with native ants for elaiosomes, lipid-rich seed appendages that attract ant dispersers, and reduces seed dispersal distance in comparison to native seed dispersers in longleaf pine forest (Stuble et al. 2010). Native termite diversity in Florida is lower than that of ants, but no fewer than 21 species of termites have been recorded from Florida (UF/IFAS n.d., Scheffrahn and Su 1994, Scheffrahn 2013). A single species is common in forested habitats of North Central Florida, the native eastern subterranean termite, Reticulitermes flavipes Kollar (Blattodea: Isoptera). This species plays an important role in nutrient cycling in forested ecosystems, and density is affected by the availability of dead wood (Gentry and Whitford 1982). We expect fire frequency to influence the abundance of both ants and termites by affecting habitat quality and resource availability in frequently burned flatwoods, including food availability, soil moisture, presence of symbionts, rate of wood decay, etc. In this study, we tested how differing fire frequencies affect the species richness and community composition of social, litter-dwelling insects—specifically ants and termites—in a longleaf pine flatwoods site. We evaluated the effects of growing season burns (at annual, 2- and 3-yr intervals) in comparison to sites that had long been unburned (30 and 75 yr) in order to provide data relevant to forest management, including conservation of native species and management of invasive species. We conducted this study in an experimental forest that has been consistently managed and documented for decades. We also asked whether burn frequency influenced susceptibility or resistance to exotic insects. Because many exotic species are disturbance specialists and often occur in frequently burned sites (e.g., S. invicta), we specifically tested if fire frequency was positively correlated with the presence of exotic ants. A lack of species-level data on the effects of different fire regimes on invertebrate community composition motivated this research; the goal of this study was to provide a detailed examination of ground-dwelling ants and termites associated with different fire frequencies relevant to long-term management and restoration strategies in the longleaf pine ecosystem. Materials and Methods Sampling Site Sampling was conducted at the Austin Cary Forest (ACF) (29.75, −82.22), a 842 ha (2,080 acre) longleaf and slash pine research and teaching forest maintained by the University of Florida (Gainesville, FL) since 1936 (UF/SFRC n.d.). The Florida Forest Service identifies the major land type at ACF as mesic flatwoods (FNAI and FFS 2015). Flatwoods are one of six recognized types of longleaf pine communities (Oswalt et al. 2012). If maintained with regular burning, mesic flatwoods are ‘characterized by an open canopy of tall pines and a dense, low ground layer of low shrubs, grasses, and forbs’ (FNAI 2010). For approximately a century, large segments of the site had been managed for turpentine production and, more recently, for loblolly pine (Pinus taeda L.) (Pinales: Pinaceae) timber production, a historically dominant tree in the surrounding landscape. In the past several decades, an increasing percentage of the ACF has been designated for longleaf pine forest restoration through silviculture and prescribed fire. Frequent fire intervals of at least every 3 yr are recommended (but not always logistically feasible) to maintain the biodiversity in longleaf pine ecosystems (Glitzenstein et al. 2003). Growing season burns are recommended to promote flowering of the dominant grass A. stricta (Wade et al. 2000), but dormant season burns are also common since winter weather conditions are often more suitable for safe prescribed burning (Hanula and Wade 2003). Treatments Five different fire frequency treatments were examined: 1) burned annually, 2) burned every 2 yr, 3) burned every 3 yr, 4) unburned for 30 yr, and 5) unburned for 75 yr (Fig. 1). The primary soil type within all five plots was Pomona sand. Elevation ranged from 144 to 160 m above mean sea level. Frequently burned plots (1-, 2-, and 3-yr intervals) are burned during the growing season and have been burned consistently on this schedule for at least the previous 15 yr. The study site included a single plot representing each fire frequency treatment; as such, multiple transects from each site represent pseudoreplication and treatment may be confounded with site characteristics. Leaf litter volume and height of the understory/midstory were observed to be positively related to time since burn. Frequently burned plots experience low intensity fire due to low accumulation of leaf litter between burns. The annually burned plot is 3.6 ha (9 acres) in size and was last burned in spring 2015. Overall vegetation was sparse and mainly composed of wiregrass (A. stricta) and gallberry (Ilex glabra L.A. Gray) (Aquifoliales: Aquifoliaceae); saw palmetto (Serenoa repens W. Bartram) (Arecales: Arecaceae) was present in a few dispersed clumps. Leaf litter was patchy and mainly comprised of pine needles and pine bark from dead trees. The 2-yr burn plot is 8.5 ha (21 acres) in size and was last burned in spring 2014. Ilex glabra and other shrubs were the dominant ground cover, but A. stricta and S. repens were also present. The leaf litter was less patchy and contained a higher variety of leaves than the annually burned treatment. The 3-yr burn plot is 61 ha (126 acres) in size; it was last burned in spring 2014. Serenoa repens was abundant in this plot; A. stricta and I. glabra were common (see Fig. 1 middle photo). Plants were taller here than in the more frequently burned plots, and a greater depth of leaf litter had accumulated. The 30-yr unburned plot is 10.5 ha (26 acres) in size. This plot had a closed canopy with pines and many oaks and S. repens dominating the midstory at over 1.5 m tall. Ilex glabra was sparse but present; A. stricta was absent. The leaf litter layer in this plot was the deepest (greater than 20 cm) and most moist, compared to that of other plots. The 75-yr unburned plot is 58.3 ha (114 acres) in size. This plot (see Fig. 1 far right photo) shared the characteristics of a closed canopy with pines outnumbered by oaks, a dominant midstory of S. repens, some I. glabra, and the absence of A. stricta, with the 30-yr unburned plot. The leaf litter layer was marginally, but noticeably less deep than in the 30-yr unburned plot. Sampling Design In order to sample ground-dwelling social insect communities, sifted leaf litter samples were collected during III and IV, 2016, before scheduled spring burning in annual and 2-yr fire interval plots. Each plot was sampled three times during the spring 2016 season, with sampling periods 3 wk apart. Leaf litter was collected along 50 m transects in each plot using the ‘mini-Winkler’ method (Fisher 1996). Transect locations were chosen randomly, but roads, water-accumulating depressions, and fire breaks were avoided (see Fig. 1). Each transect was situated at least 25 m from plot borders to avoid edge effects attributable to low burn intensity (Lashley et al. 2014). Each sampling transect consisted of 10 individual collections of 1 m2 of sifted leaf litter, spaced at 5 m intervals. Sampling was conducted to coincide with daytime ant foraging activity (between 10:00 a.m. and 4:00 p.m.). Litter was vigorously sifted through a leaf litter sifter with 1 cm mesh screen to remove coarse debris. Siftate was temporarily placed into labeled cotton bags, shaded from direct sun, and transported in coolers to the University of Florida Entomology and Nematology Department. Litter samples were bagged for 4 h, at most, before being hung in Winkler extractors. Specimens were extracted into 95% EtOH by hanging litter samples in Winkler extractor bags in a greenhouse set to regulate temperature between 25 and 32°C for 48 h. Extracted arthropods were stored in 95% EtOH-filled 50 ml vials. All ants and termites were sorted and identified to species. Pinned voucher specimens are deposited in the Lucky lab at the Entomology and Nematology Department at the University of Florida. Fig. 1. View largeDownload slide From left: 15 sampling transects in ACF, with arrows indicating the burn regime of each plot, outlined in white; 3-yr burn plot with dense, low-diversity understory of shrubs and saw palmetto; 75-yr unburned plot with mixed understory under mixed hardwoods and pine. Fig. 1. View largeDownload slide From left: 15 sampling transects in ACF, with arrows indicating the burn regime of each plot, outlined in white; 3-yr burn plot with dense, low-diversity understory of shrubs and saw palmetto; 75-yr unburned plot with mixed understory under mixed hardwoods and pine. Statistical Analyses Species rarefaction curves were derived to estimate the depth of sampling within each treatment and across treatments for the overall community. To estimate total species richness within treatments, we calculated Chao2 and Jackknife2 richness indices and compared those to observed species richness. These richness estimators were chosen because they allow for greater emphasis on rare species (Agosti et al. 2000). Ninety-five percent CIs for species richness estimates were compared to evaluate whether burn frequency had a significant effect on estimated species richness (Chao and Chiu 2016). To elucidate differences in habitat occupancy (a proxy measure of the density of ant colonies at the landscape scale), species density was calculated as the sum of different species present within each 1 m2 sample per treatment. Between-treatment differences in overall species density and exotic species density were evaluated with one-way analysis of variance (ANOVA) tests. The untransformed data did not meet all ANOVA assumptions (normality, homogeneity of variance); therefore, to achieve normality and homogeneity of variance, the overall species density data were log-transformed and exotic species density was raised to the sixth power. The effect of fire frequency on community composition was tested using nonparametric multivariate analysis of variance (npMANOVA) (Anderson 2001) with treatment and sampling period as predictor variables. The test was applied to two different hypotheses: 1) fire frequency will have no influence on species composition, measured by the presence of individual species along each transect; and 2) fire frequency will have no effect on individual species abundance, defined as the number of samples in which a species was detected along each transect. Dissimilarities in community composition were determined using the Jaccard distance measure (Jaccard 1912). Relative abundances needed to be standardized in order to compare across treatments; abundance data were Wisconsin double standardized prior to analysis. Tests for homogeneity of multivariate dispersions determined that the species presence and abundance data sets met npMANOVA assumptions that variability from the mean be homogeneous across treatments. Ant community dissimilarities as influenced by fire frequency were visualized graphically using nonmetric multidimensional scaling (NMDS) (Anderson 2001). Since these data sets lacked the power to discern pairwise differences between individual fire frequency treatments, an additional npMANOVA analysis was conducted in which the frequently burned and long-unburned treatments were grouped together to detect whether a significant change in presence of individual species could be established on this broader level. Histograms were constructed to visualize the 10 most abundant ant species per treatment. All statistical analyses were performed in R 3.3.0 (R Core Team 2016) with use of the vegan package (Oksanen et al. 2016) and SpadeR package (Chao et al. 2016). Results A total of 39 ant and one termite species, R. flavipes, were collected across all treatment plots (Table 1). Ants and termites were present in all treatments during all sampling periods, with the exception of the annually burned plot during the first sampling period, where no ants or termites were collected. Termite presence was not affected by fire frequency. Overall ant richness leveled off near 39 species, the total number of ant species detected across all treatments, suggesting that the ant community was well sampled over the course of this study and that few species remain undetected (Fig. 2). Six species were detected in all treatment plots: the five ant species Temnothorax pergandei (Emery), Pheidole dentata Mayr, Pheidole dentigula Smith, Brachymyrmex depilis Emery, and Solenopsis molesta (Say)-group spp. (Hymenoptera: Formicidae), as well as one termite species, R. flavipes. Table 1. Ant and termite species occurrence in forest plots managed with different burn regimes, out of 30 collections per treatment Darkness of shading is correlated with decreasing fire frequency treatment. Uncolored cells indicate the species was not detected in the given treatment. A = ant, T = termite, N = native, E = exotic. View Large Table 1. Ant and termite species occurrence in forest plots managed with different burn regimes, out of 30 collections per treatment Darkness of shading is correlated with decreasing fire frequency treatment. Uncolored cells indicate the species was not detected in the given treatment. A = ant, T = termite, N = native, E = exotic. View Large Fig. 2. View largeDownload slide Expected number of ant species across all treatments, based on sample-based rarefaction. Shaded area around the curve represents two times the SE. Estimates calculated with ‘exact’ method in ‘specaccum’ function in R vegan package. Fig. 2. View largeDownload slide Expected number of ant species across all treatments, based on sample-based rarefaction. Shaded area around the curve represents two times the SE. Estimates calculated with ‘exact’ method in ‘specaccum’ function in R vegan package. Burn Frequency Effect on Species Richness Each of the five burn treatments supported a similar species richness of ants (18–23 species), and all harbored a single species of termite (R. flavipes). Ant species accumulation curves within individual treatments did not completely plateau, but rate of new species discovery leveled off for all treatments (Fig. 3A). Estimated local ant diversity in individual plots ranged from 21 to 42 species, based on Chao2 and second-order Jackknife estimates, and in general neither Chao2 nor second-order Jackknife estimates were significantly different between treatments (Fig. 3B). Some undetected species may be present but the probability of large numbers of undiscovered species is low in most plots, as suggested by the narrow 95% CIs for these estimates. The one exception to this pattern was the large SE for the 75-yr unburned plot when using the Chao2 estimator, which heavily weights the number of singletons. Nearly half of the species detected in the 75-yr unburned plot were found only once in that treatment, suggesting that more species remain undetected here than in other treatment plots. Fig. 3. View largeDownload slide (A) Expected number of ant species according to treatment. Sample-based rarefaction curves were calculated with the ‘exact’ method and ‘specaccum’ function in R vegan package. Error bars are not displayed. (B) Observed species richness, Chao2, and second-order Jackknife species richness estimates for all treatments. Bars are 95% CIs. All bars overlap: no significant differences are suggested. Fig. 3. View largeDownload slide (A) Expected number of ant species according to treatment. Sample-based rarefaction curves were calculated with the ‘exact’ method and ‘specaccum’ function in R vegan package. Error bars are not displayed. (B) Observed species richness, Chao2, and second-order Jackknife species richness estimates for all treatments. Bars are 95% CIs. All bars overlap: no significant differences are suggested. Ant species density was considerably higher in long-unburned plots than in frequently burned plots (F = 14.4; df = 4, 143; P < 0.001; Fig. 4; Table 2). Species density differences were also detected between the annual and 2-yr burn treatment (P = 0.026), but the magnitude of the difference (M = 1.77 and M = 2.43, respectively) was smaller than the differences between frequently burned and long-unburned plots (Table 2). Exotic species density was higher in burned than unburned plots, but this relationship was not significant (F = 0.8; df = 4, 143; P = 0.53; Fig. 4). Fig. 4. View largeDownload slide Influence of fire frequency on species density. Mean species density was calculated from species richness per 1 m2 sample. ‘Overall’ includes all ant species; ‘exotic’ is limited to non-native ant species. Fire frequency has a significant impact on overall mean ant density (one-way ANOVA, P < 0.0001) but not on mean exotic ant density (one-way ANOVA, P = 0.53). Error bars represent 95% CIs: shared letters indicate no significant difference between groups. Fig. 4. View largeDownload slide Influence of fire frequency on species density. Mean species density was calculated from species richness per 1 m2 sample. ‘Overall’ includes all ant species; ‘exotic’ is limited to non-native ant species. Fire frequency has a significant impact on overall mean ant density (one-way ANOVA, P < 0.0001) but not on mean exotic ant density (one-way ANOVA, P = 0.53). Error bars represent 95% CIs: shared letters indicate no significant difference between groups. Table 2. Pairwise comparisons of ant species density across fire frequency treatments Pairwise comparisons Difference P.adjusted Annual vs 2 yr 0.378 0.026* Annual vs 3 yr 0.234 0.344 2 yr vs 3 yr 0.144 0.785 Annual vs unburned 30 0.746 <0.001* Annual vs unburned 75 0.794 <0.001* 2 yr vs unburned 30 0.368 0.033* 2 yr vs unburned 75 0.416 0.011* 3 yr vs unburned 30 0.512 <0.001* 3 yr vs unburned 75 0.559 <0.001* Unburned 30 vs unburned 75 0.048 0.996 Pairwise comparisons Difference P.adjusted Annual vs 2 yr 0.378 0.026* Annual vs 3 yr 0.234 0.344 2 yr vs 3 yr 0.144 0.785 Annual vs unburned 30 0.746 <0.001* Annual vs unburned 75 0.794 <0.001* 2 yr vs unburned 30 0.368 0.033* 2 yr vs unburned 75 0.416 0.011* 3 yr vs unburned 30 0.512 <0.001* 3 yr vs unburned 75 0.559 <0.001* Unburned 30 vs unburned 75 0.048 0.996 Tukey’s HSD pairwise comparisons were used to determine significant differences in ant species density between burn regime treatments (N = 2 for annual and N = 3 each other treatment). P-values were adjusted for multiple comparisons using the Bonferroni method. P-values of significant comparisons are in bold. *P < 0.05. View Large Table 2. Pairwise comparisons of ant species density across fire frequency treatments Pairwise comparisons Difference P.adjusted Annual vs 2 yr 0.378 0.026* Annual vs 3 yr 0.234 0.344 2 yr vs 3 yr 0.144 0.785 Annual vs unburned 30 0.746 <0.001* Annual vs unburned 75 0.794 <0.001* 2 yr vs unburned 30 0.368 0.033* 2 yr vs unburned 75 0.416 0.011* 3 yr vs unburned 30 0.512 <0.001* 3 yr vs unburned 75 0.559 <0.001* Unburned 30 vs unburned 75 0.048 0.996 Pairwise comparisons Difference P.adjusted Annual vs 2 yr 0.378 0.026* Annual vs 3 yr 0.234 0.344 2 yr vs 3 yr 0.144 0.785 Annual vs unburned 30 0.746 <0.001* Annual vs unburned 75 0.794 <0.001* 2 yr vs unburned 30 0.368 0.033* 2 yr vs unburned 75 0.416 0.011* 3 yr vs unburned 30 0.512 <0.001* 3 yr vs unburned 75 0.559 <0.001* Unburned 30 vs unburned 75 0.048 0.996 Tukey’s HSD pairwise comparisons were used to determine significant differences in ant species density between burn regime treatments (N = 2 for annual and N = 3 each other treatment). P-values were adjusted for multiple comparisons using the Bonferroni method. P-values of significant comparisons are in bold. *P < 0.05. View Large Burn Frequency Effect on Community Composition Burn treatment had a significant effect on the composition of the ant community as described by species presence (pseudo-F = 2.59; df = 4, 7; permutation P = 0.001). Species present in frequently burned plots are generally associated with open canopy, dry habitats of fire-maintained longleaf pine forest, and differed from those in long-unburned plots, which included more moisture-favoring species. Sampling period, in contrast, did not have a significant effect (pseudo-F = 1.35; df = 2, 7; permutation P = 0.179). Treatment explained four times more variation (R2 = 52%) than sampling period (R2 = 13%). Further supporting these results, frequently burned and long-unburned communities showed clear differences in NMDS means (Fig. 5A). Burn frequency also had a significant effect on the composition of the ant community as described by individual ant species abundances (pseudo-F = 1.99; df = 4, 7; permutation P = 0.001). The most common species in long-unburned were more abundant than in frequently burned plots. Additionally, species present across all treatments were more abundant in long-unburned treatments, in general, compared with frequently burned treatments. Overall, more species were detected across at least one-third of samples in long-unburned treatments (seven ant species) than in frequently burned treatments (one ant species) (Table 1). Sampling period explained approximately 12% of the variability within the data set, but it was not found to significantly impact individual ant species abundances (pseudo-F = 1.04; df = 2, 7; permutation P = 0.38). Fig. 5. View largeDownload slide NMDS analysis of ant community composition, depicted as (A) species presence per transect and (B) species abundance per transect. Presence and abundance data display a strong signal for difference in mean (location) of frequently burned versus long-unburned treatments. In both models, treatment has a significant effect on ant community composition (A: npMANOVA, pseudo-F = 2.59; df = 4, 7; permutation P = 0.001) and (B: npMANOVA, pseudo-F = 1.99; df = 4, 7; permutation P = 0.001). Fig. 5. View largeDownload slide NMDS analysis of ant community composition, depicted as (A) species presence per transect and (B) species abundance per transect. Presence and abundance data display a strong signal for difference in mean (location) of frequently burned versus long-unburned treatments. In both models, treatment has a significant effect on ant community composition (A: npMANOVA, pseudo-F = 2.59; df = 4, 7; permutation P = 0.001) and (B: npMANOVA, pseudo-F = 1.99; df = 4, 7; permutation P = 0.001). Although we lacked the power to detect pairwise differences between individual fire frequency treatments, the npMANOVA comparing ant species presence in frequently burned treatments (annual, 2 yr, 3 yr) and long-unburned treatments (30 and 75 yr) as separate groups detected a significant delineation in community composition on this broader level (pseudo-F = 4.93; df = 1, 12; permutation P = 0.001). Dispersion (variance from the mean) under frequent burning was greater than in long-unburned treatments, indicating that ant species assemblages in frequently burned plots tend to be more variable (F = 7.25; df = 1, 12; P = 0.02) (Fig. 5). A snapshot of the species-level differences in ant communities across treatments is reflected in the identities and abundances of the 10 most commonly encountered ant species per treatment, depicted as frequency histograms (Fig. 6). The most common species differ between frequently burned and long-unburned treatments. Abundance of the single most common species in frequently burned treatments (S. molesta-group spp.) is notably lower than that of the most common species in long-unburned treatments (P. dentigula and Nylanderia faisonensis (Forel) (Hymenoptera: Formicidae)). In both the annually burned and 3-yr burn plot, P. dentata is the second most abundant species; however, in the 2-yr burn it ranks ninth in abundance. In total, nine species of common, generalist ants detected in the 2-yr burn treatment were not detected in the annual burn plot (Table 1). Species-specific differences between annual and 2-yr burn treatments range from occurrences that may be attributable to chance (i.e., singletons) to more substantial distinctions. For example, no species of Nylanderia was found in the annually burned plot, whereas three Nylanderia species (Nylanderia parvula (Smith), N. faisonensis, and Nylanderia wojciki (Trager) (Hymenoptera: Formicidae)) were detected in the 2- and 3-yr burn plots. Fig. 6. View largeDownload slide Ten most abundant ant species per treatment. Abundance was calculated as the number of the thirty 1 m2 sampling units where the species was detected. 1In the annually burned plot, Brachmyrmex depilis, Strumigenys eggersi, and Trachymyrmex septentrionalis were as abundant as Soleonopis invicta. 2In the 2-yr burn plot, Brachmyrmex depilis, Strumigenys eggersi, Camponotus floridanus, Pheidole dentigula, Solenopsis picta, and Temnothorax texanus were as abundant as Pheidole dentata. 3In the 30-yr unburned plot, Strumigenys clypeata was as abundant as Crematogaster minutissima. Fig. 6. View largeDownload slide Ten most abundant ant species per treatment. Abundance was calculated as the number of the thirty 1 m2 sampling units where the species was detected. 1In the annually burned plot, Brachmyrmex depilis, Strumigenys eggersi, and Trachymyrmex septentrionalis were as abundant as Soleonopis invicta. 2In the 2-yr burn plot, Brachmyrmex depilis, Strumigenys eggersi, Camponotus floridanus, Pheidole dentigula, Solenopsis picta, and Temnothorax texanus were as abundant as Pheidole dentata. 3In the 30-yr unburned plot, Strumigenys clypeata was as abundant as Crematogaster minutissima. Ant abundance in long-unburned treatments was high; the most abundant species in both plots were detected more frequently than the most abundant ants in frequently burned treatments. However, the ant community composition in long-unburned treatments diverged from that commonly associated with longleaf pine, and included species associated with mesic hardwood forest. Instead of a diverse community of longleaf pine-associated species, these plots were dominated by a smaller number of species. For example, moisture-favoring P. dentigula and N. faisonensis were among the most abundant species in long-unburned treatments. Native and Exotic Species Although the majority of ant species detected were native to the southeastern United States (34 of 39 species), the presence of five exotic ant species was noted: Cardiocondyla obscurior Wheeler, Cyphomyrmex rimosus (Spinola), Pheidole moerens Wheeler, S. invicta, and Strumigenys eggersi Emery (Hymenoptera: Formicidae). All were sampled within frequently burned treatments; P. moerens and S. eggersi were also detected in the 30-yr unburned treatment. All ant species collected from the 75-yr unburned treatment were native. Exotic ant species density was marginally higher in frequently burned than in long-unburned treatments, but this relationship was not significant (F = 0.8; df = 4, 143; P = 0.53) (Fig. 4). Notably, the non-native ant species of greatest economic importance, S. invicta, was only detected in frequently burned treatments, and was not found in either long-unburned treatment (Table 1). Discussion To the best of our knowledge, this study is the first to date to characterize the species-level effects of different managed fire frequencies on arthropods in a longleaf pine ecosystem. Different forest management approaches such as fire frequency, season, and suppression are known to differentially affect the plant community (Platt et al. 1988, Glitzenstein et al. 2003, Alba et al. 2015) and soil characteristics (Switzer et al. 1979, Varner et al. 2005, Ryan et al. 2013). Therefore, it comes as no surprise that fire frequency affects the arthropod community. This study demonstrates that forest management maintaining different plots with varying fire frequency supports a diverse ant community at one experimental site representative of the longleaf pine flatwoods ecosystem. This species-level study is revealing about community-level differences that can be obscured at a more general taxonomic level, even though the generalizability of this research may be limited by pseudoreplication, as sampling was conducted at a single site with a single plot sampled for each burn frequency, and by the limited time frame of sampling. Different fire frequencies may have nontrivial influences on the composition of species in the community, although they may not always result in different numeric species richness. Fire frequency also may affect the density at which colonies occur in the landscape and, importantly, may play a significant role in the establishment of exotic species. The rate of habitat disturbance caused by increased fire frequency may increase the probability that queens of exotic species select the site for colony founding and subsequently establish successfully. This arthropod-focused concern is of broad relevance to management of mesic flatwoods, which are widely distributed in Florida (FNAI 2010) and across the U.S. Southeastern Coastal Plain (Oswalt et al. 2012). Species Richness and Community Composition Most biodiversity studies in longleaf pine forest ecosystems advocate for frequent (every 1–3 yr) burns to promote herbaceous ground cover diversity and abundance of vertebrates of conservation interest, such as the red-cockaded woodpecker (Darracq et al. 2016). Ant species richness remained relatively consistent across all plots, regardless of fire frequency, although a high proportion of rarely encountered species in the 75-yr unburned plot suggests that further sampling could reveal additional species in this long-unburned site. However, differences in presence and abundances of individual species indicated significant differences in ant community composition among treatments, with differentiation between frequently burned and long-unburned ant communities. Therefore, unlike previous research indicating a positive relationship between plant species richness and fire frequency (Glitzenstein et al. 2003, Kirkman et al. 2004) up to annual burn intervals, community composition, rather than species richness, defined our treatment differences, with frequently burned plots harboring the most ant species adapted to the sunny, open canopy, and diverse niches representative of longleaf pine flatwoods habitat. This outcome is likely mediated by the effect of frequent fire on plant community structure and microhabitat characteristics. Fire-maintained longleaf pine flatwoods are characterized by open forests with grass and herbaceous-dominated ground cover. The openness, relative lack of moisture- and nutrient-rich leaf litter, and regular disturbance in this habitat evidently encourage a heterogeneous and patchy ant community adapted to these conditions, and facilitate the relatively even distribution of native species in the landscape. Fire suppression, in contrast, allows the proliferation of oaks and other fire-intolerant trees and a dense understory dominated by palmetto, all of which contribute to a deep layer of moisture-retentive leaf litter (Van Lear et al. 2005) that can reach depths greater than 25 cm (Varner et al. 2000). The ant communities in these long-unburned treatments were marginally, not significantly, more species rich and the abundance of individual species was higher. Nevertheless, as expected given the vegetation and soil differences in long-unburned sites, the most abundant ants in these forests were less characteristic of dry, open, and diverse habitats typical of longleaf pine forest and more commonly associated with closed canopy, moisture-retentive habitats, like hardwood forest (Deyrup 2017). Differences in species density between frequently burned and long-unburned treatments were pronounced, with frequently burned plots harboring significantly lower ant species densities than long-unburned plots (Fig. 4), even as ant species richness did not differ across treatments. Among frequent burns, the highest ant densities were in the 2-yr burn plot. While this study’s results cannot be generalized without replication at a larger scale, these results suggest that forest management plans that include burning at 1- to 3-yr intervals should maintain arthropod richness, but that burning annually may decrease the density of species in an area. Exotic Species Frequent disturbance by fire is not entirely beneficial for this longleaf pine flatwoods site since it may facilitate invasive species establishment (Fig. 4). Presence of the red imported fire ant, S. invicta, and other exotic ants was positively related to fire frequency, whereas S. invicta was not detected in long-unburned plots (Table 1). Low richness of exotic ant species in the 30-yr unburned treatment, absence of exotic ants from the 75-yr unburned treatment, and high species density among both long-unburned treatments suggest that in long-unburned plots native ants at higher densities may buffer against exotic species. However, the spatial aggregation of frequently burned versus long-unburned plots could alternately suggest that S. invicta may have invaded one of the frequently burned plots and dispersed to other frequently burned plots, but not long-unburned plots due to the closer proximity of other frequently burned plots. The presence of invasive ants in more disturbed sites, with only the longest unburned site free of exotic ants, supports current theories in invasion biology positing that successful invasive species tend to be disturbance specialists (Belote et al. 2008, Cumberland and Kirkman 2012). Solenopsis invicta, in particular, is known to be associated with disturbance, and its occurrence in fire-maintained pine forest has prompted considerable study of its effect on the ecosystem (Lubertazzi and Tschinkel 2003; Stuble et al. 2009, 2010; King and Tschinkel 2013a). The impacts of S. invicta in longleaf pine forest are well documented, but since these effects are usually confounded with disturbance, concerns about the species’ ability to affect undisturbed habitat are contested (Stuble et al. 2010, 2013; King and Tschinkel 2013a,b). Regardless, restoration and maintenance of longleaf pine requires disturbance by fire to prevent the large-scale disturbance of ecological succession from longleaf pine to mixed hardwood forest. Previous research has demonstrated that S. invicta abundance was positively associated with dormant season fire frequency (Hanula and Wade 2003); this study found that S. invicta presence was positively associated with growing season fire frequency. Native Species Several native ant species were found across all treatments, and are species commonly encountered in southeastern forest in mesic to dry habitats with generalist (scavenger and predator) feeding preferences (T. pergandei, P.dentata, P. dentigula, B. depilis, and S. molesta-group spp.). Of these, P. dentata and P. dentigula were detected more frequently in long-unburned plots. Other Pheidole (P. dentigula, P. metallescens), with more specialized feeding (seed predation) and nesting preferences in dry, sandy soils (Deyrup 2017), were generally supported in open, fire-maintained forest. Conversely, several ant genera that nest primarily in standing or fallen dead wood, such as Aphaenogaster and Crematogaster, occurred less frequently in fire-maintained sites. This may be a result of the greater availability of nesting material in long-unburned forest habitat. While Hanula and Wade (2003) also documented that Aphaenogaster spp. were reduced by frequency of burn, they found the same trend in Camponotus spp., a pattern not seen in the data from this study. The genus Strumigenys consists of small, slow-moving leaf litter species that are specialist predators of Collembola. Seven native Strumigenys species were sampled, each one occurring only in a single treatment type. The one exotic species in this genus (S. eggersi) was encountered in all plots except the 75-yr unburned plot. In summary, our results suggest that more similar suites of ants establish and persist in fire-maintained than in fire-excluded longleaf pine habitats. Floral composition, higher leaf litter accumulation, decomposition, and associated higher moisture retention in fire-excluded flatwoods, likely provide habitat (abiotic and biotic) that supports different ant species than fire-maintained flatwoods. Generally in longleaf pine ecosystems, fire exclusion leads to a sharp reduction in herbaceous species diversity, corresponding with the dominance of oaks and shrubs (Van Lear et al. 2005, Oswalt et al. 2012); at this site, plots with lack of fire also encouraged higher abundances of moisture-favoring ant species. Fire, in contrast, continuously re-sets the habitat to an early successional stage and therefore may favor species more resilient to frequent change (Pulsford et al. 2016), more opportunistic in disturbed habitats (Hoffmann and Andersen 2003) and which are adapted to thrive in more open and xeric microclimates. Conclusion Social insects, and especially ants constitute an important component of the longleaf pine ecosystem, but little research has focused on the effects of fire regime on these groups at the species level. This study of the litter-dwelling ant and termite species at a site in central Florida with a long history of fire management highlights some of the community-level distinctions associated with different fire frequencies. Species richness did not differ between treatments despite the fact that fire suppression altered the forest composition to the point of no longer supporting ant species associated with high quality longleaf pine habitat. Communities of ants differed between frequently burned and long-unburned plots, both in terms of species composition and abundance of common species. While previous research on other floral and faunal groups (i.e., within classification groups, such as birds or amphibians) has highlighted the species-specific nature of response to fire and the fact that fire regimes that promote one species may not support another (Lashley et al. 2014), this study found that differences in composition and densities of ants among frequently burned sites (1, 2, and 3 yr) were less pronounced. Our results indicate that burn intervals every 2–3 yr or less produce similar ant community composition, abundance, and species density, suggesting that these burn intervals are sufficient to promote native longleaf-associated ant species at this site. Accompanying frequent burning, land managers are likely to encounter the invasive ant, S. invicta as well as other exotic ants, and may find that these ants proliferate even under well-supported management practices. While interpretation of these results is restricted to this study site, future research with greater treatment replication can provide more broadly applicable information. We additionally suggest that future research on arthropods in burned and unburned longleaf pine forest provides insights into how different fire regimes affect the actual ecosystem services provided by these species to help guide management practices to maintain the microhabitats that benefit them. Acknowledgments We thank Lloyd Davis and Lyle Buss for assistance with ant identification, Ben Baiser and James Colee for statistical guidance, and Michelle Dunbar for curation assistance. This manuscript was greatly improved by the detailed comments of several anonymous reviewers. 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Environmental Entomology – Oxford University Press
Published: Apr 11, 2018
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