Network reorganization and breakdown of an ant-plant protection mutualism with elevation

Abstract

Both the abiotic environment and the composition of animal and plant communities change with elevation. For mutualistic species, these changes are expected to result in altered partner availability, and shifts in context-dependent benefits for partners. To test these predictions, we assessed the network structure of terrestrial ant-plant mutualists and how the benefits to plants of ant inhabitation changed with elevation in tropical forest in Papua New Guinea. At higher elevations, ant-plants were rarer, species richness of both ants and plants decreased, and the average ant or plant species interacted with fewer partners. However, networks became increasingly connected and less specialized, more than could be accounted for by reductions in ant-plant abundance. On the most common ant-plant, ants recruited less and spent less time attacking a surrogate herbivore at higher elevations, and herbivory damage increased. These changes were driven by turnover of ant species rather than by within-species shifts in protective behaviour. We speculate that reduced partner availability at higher elevations results in less specialized networks, while lower temperatures mean that even for ant-inhabited plants, benefits are reduced. Under increased abiotic stress, mutualistic networks can break down, owing to a combination of lower population sizes, and a reduction in context-dependent mutualistic benefits.

Keywords: altitudinal gradients; biotic defence; global change; herbivory; myrmecophyte; network specialization.

Figure 1.

Domatia of the three most abundant ant-plant species in our study. (a) Swollen stem domatia of Myristica subalulata being excavated by Anonychomyrma ants, (b) entrance holes of a Chisocheton lasiocarpus domatium occupied by Podomyrma sp. 3, and (c) Podomyrma sp. 3 patrolling the swollen stem domatia of Ryparosa amplifolia.

Figure 2.

Distribution of ant-inhabited plant species (n = 386 trees) and their ant occupants from 700 to 1600 m.a.s.l. No ant-inhabited trees were found at 1600 m. Bars on the left indicate the number of ant-occupied individuals per tree species. Bars on the right indicate the number of occupied trees per ant species. Individual plants were only ever occupied by one species of ant, but most plant species were inhabited by multiple species of ant across multiple plant individuals. Where ants were observed in domatia, but could not be collected, they were recorded as ‘uncertain’.

Figure 3.

Bipartite interaction networks of ant-inhabited plants and their ant occupants from 700 to 1500 m.a.s.l. Upper blocks represent ant species, lower blocks represent plant species and connecting light grey bars indicate species interactions. Species with fewer than 10 occurrences are assigned as ‘other’ (grey blocks), but are not combined (i.e. the foodweb is fully resolved). Width of bars represents the proportion of the total community of ants or plants interacting at a given elevation. Note that the total abundance of ant-plants varied between elevations (sample size in brackets).

Figure 4.

(a) Species richness of plant-inhabiting ants, (b) species richness of ant-inhabited plants, (c) generality, (d) vulnerability, (e) connectance, (f) network specialization (H₂′) and (g) modularity of networks from 700 to 1600 m.a.s.l. Grey bars indicate the 95% prediction intervals based on rarefying a pooled community from 700 and 800 m, and black circles indicate observed data fitted with linear (a,b) and quadratic regressions (c,e). In panels (d), (f) and (g) non-parametric analyses were used, hence no line of best fit is presented, although significant relationships with elevation were detected. Asterisks in panel (f) indicate observed H₂′ values which differed significantly from what would be expected if ant species colonized plant species at random within elevations.

Figure 5.

Responses of Anonychomyrma ants inhabiting Myristica subalulata trees to a surrogate herbivore and control treatment from 700 to 1400 m.a.s.l. (a) Time taken to detect, (b) time spent attacking, (c) time until the first recruit contacted the control/herbivore, and (d) maximum number of ants observed on experimental leaf at one time. Sample size in italics. (Online version in colour.)

Figure 6.

Percentage herbivory damage of (a) all ant-inhabited plants, (b) all inhabited individuals of M. subalulata in the transects, and (c) all individuals of M. subalulata at the time of baiting experiment from 700 to 1400 m.a.s.l. Leaves were assessed on all trees more than or equal to 5 m and categorized from 1 to 4 (0%, less than 5%, 5–33%, more than 33% damage, respectively). Counts across categories were converted into means for the purposes of plotting, using the midpoint for each category. Sample size in italics.