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Differences in forage-acquisition and fungal enzyme activity contribute to niche segregation in Panamanian leaf-cutting ants - PubMed

  • ️Wed Jan 01 2014

Differences in forage-acquisition and fungal enzyme activity contribute to niche segregation in Panamanian leaf-cutting ants

Pepijn W Kooij et al. PLoS One. 2014.

Abstract

The genera Atta and Acromyrmex are often grouped as leaf-cutting ants for pest management assessments and ecological surveys, although their mature colony sizes and foraging niches may differ substantially. Few studies have addressed such interspecific differences at the same site, which prompted us to conduct a comparative study across six sympatric leaf-cutting ant species in Central Panama. We show that foraging rates during the transition between dry and wet season differ about 60 fold between genera, but are relatively constant across species within genera. These differences appear to match overall differences in colony size, especially when Atta workers that return to their nests without leaves are assumed to carry liquid food. We confirm that Panamanian Atta specialize primarily on tree-leaves whereas Acromyrmex focus on collecting flowers and herbal leaves and that species within genera are similar in these overall foraging strategies. Species within genera tended to be spaced out over the three habitat categories that we distinguished (forest, forest edge, open grassland), but each of these habitats normally had only a single predominant Atta and Acromyrmex species. We measured activities of twelve fungus garden decomposition enzymes, belonging to the amylases, cellulases, hemicellulases, pectinases and proteinases, and show that average enzyme activity per unit of fungal mass in Atta gardens is lower than in Acromyrmex gardens. Expression profiles of fungal enzymes in Atta also appeared to be more specialized than in Acromyrmex, possibly reflecting variation in forage material. Our results suggest that species- and genus-level identities of leaf-cutting ants and habitat-specific foraging profiles may give predictable differences in the expression of fungal genes coding for decomposition enzymes.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Differences in forage diversity.

Differences in forage diversity between leaf-cutting ant species (nested within genera), using solid lines for Atta and dotted lines for Acromyrmex, and with typical foraging habitat indicated with dark green (forest), yellow (forest edge), and orange (open sunlit areas): (A) Heatmap showing differences between species and genera in the use of forage categories, with numbers representing mean proportions ±SE of the forage types. Darker colors indicate higher mean acquisition proportions, with the top-dendrogram illustrating similarities between species/genera across means of the five forage categories (vertical axis). Ant species names are given as abbreviations (volc, octo, echi, col, sex, cep). (B) Dendrogram based on the Inverse Simpson Diversity Index of the five forage categories, indicating the degree of evenness across foraging categories (numbers below the branches are mean D-values ±SE per species and means per genus), showing that Acromyrmex has a broader (more even) spectrum (D = 1.86±0.08 SE) of forage material than Atta (D = 1.42±0.13 SE; F1,49 = 5.435, p<0.05). Numbers above the branch nodes represent Approximately Unbiased p-values (AU, red) and Bootstrap Probability values (BP, green).

Figure 2
Figure 2. Differences in fungus garden enzyme activity.

Differences in fungus garden enzyme activity between species grouped as in Figure 1 with solid lines for Atta and dotted lines for Acromyrmex, and with dark green, yellow and orange indicating the same habitat categories: (A) Heatmap showing differences between species and genera in fungus garden activity of enzyme classes, expressed as mean area in cm2±SE of colored halos on AZCL plates across all assays for enzymes belonging to the amylases (1), cellulases (2), hemicellulases (4), pectinases (3) and proteinases (2). Darker colors in the heatmap indicate higher mean activities, and the top-dendrogram illustrates similarities between species across all means for the five groups of enzymes, estimated by “pvclust” with 1000000 bootstraps. (B) Dendrogram based on the inverse Simpson Diversity Index of proportional enzyme activity showing that Acromyrmex fungus gardens have more even secretions across enzyme categories (D = 4.55±0.05 SE) than Atta (D = 4.18±0.07 SE, F1,52 = 15.006, p<0.0001). Numbers above the branch nodes represent Approximately Unbiased p-values (AU, red) and Bootstrap Probability values (BP, green).

Figure 3
Figure 3. Principal Component Analyses on forage diversity and enzyme activity.

Principal Component Analyses (PCA) using either the five enzyme groups of Figure 2 (A and B) or the five forage material categories of Figure 1 (C and D) as predictor variables (black arrows). Red arrows represent response vectors for forage material (A) or enzymes (C). The B and D panels complement the respective A and C panels by plotting PCA’s scores across the fungus garden measurements (B, 45 for Atta and 32 for Acromyrmex) the sampled ant trails (D, 30 for Atta and 21 for Acromyrmex; Table 1), largely separating the ant genera along the x-axes, confirming that Atta primarily focuses on tree-leaf material (compare panels C and D) and Acromyrmex on herbaceous leaves, flowers and (less pronounced) fruit. Comparison of the A and B panels illustrates that enzyme activity was generally higher in Acromyrmex (towards the right).

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Funding was provided by the Danish National Research Foundation (DNRF57). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.