The turnover of plant-frugivore interactions along plant range expansion: consequences for natural colonization processes

Abstract

Plant-animal mutualisms such as seed dispersal are key interactions for sustaining plant range shifts. It remains elusive whether the organization of interactions with seed dispersers is reconfigured along the expansion landscape template and, if so, whether its effects accelerate or slow colonization. Here we analyse plant-frugivore interactions in a scenario of rapid population expansion of a Mediterranean juniper. We combined network analyses with field surveys, sampling interactions between individual plants and frugivores by DNA-barcoding and phototrapping over two seasons. We assess the role of intrinsic and extrinsic intraspecific variability in shaping interactions and we estimate the individual plant contributions to the seed rain. The whole interaction network was highly structured, with a distinct set of modules including individual plants and frugivore species arranged concordantly along the expansion gradient. The modular configuration was partially shaped by individual neighbourhood context (density and fecundity) and phenotypic traits (cone size). Interaction reconfiguration resulted in a higher and more uneven propagule contribution, with most effective dispersers having a prominent role at the colonization front stand, where a distinct subset of early arriving plants dominated the seed rain. Our study offers new insights into the key role of mutualistic interactions in colonization scenarios by promoting fast plant expansion processes.

Keywords: ecological networks; frugivory; mutualistic interactions; plant range shifts; reproductive ecology; seed dispersal.

Figure 1.

Individual-based frugivory network of Juniperus phoenicea along a range expansion gradient. Dots represent individual plants and squares represent frugivore species. As a spatially explicit network, the location of the plants within the panel for each stand corresponds to their actual georeferenced positions. The dotted lines represent a fictitious separation, as the stands are distant from each other (see electronic supplementary material, figure S3b). Frugivore visits to the focal plants (network links) are represented by grey lines. The colours of the network nodes represent the modules to which the individual plants and animals belong (A = red; B = salmon; C = grey). The three rectangles illustrate the three different study stands along the expansion gradient, from a mature forest area to the colonization front (MAR = mature stand; OJI = intermediate-maturity stand; COL = colonization front stand).

Figure 2.

Estimated number of seeds dispersed by each individual plant in the three network modules. Each dot represents an individual plant and the colours illustrate the stand provenance. Note the log scale on the y-axes to improve visualization.

Figure 3.

Ranked z-scores representing the deviation of each individual juniper from the stand mean number of seeds dispersed, i.e. how each individual contribution to the total seed rain deviates from the stand mean along the natural expansion gradient (MAR = mature stand; OJI = intermediate-maturity stand; COL = colonization front stand). Points represent individual plants and colours indicate network module assignment. Note that a more homogeneous normal distribution in the contribution would be represented with half of the individuals above the mean and half below the mean (OJI case), while a strongly skewed distribution with some outliers would result in a strongly truncated line (COL case).

Figure 4.

(a) Comparison between 1977 and 2020 aerial images of the studied colonization front stand (COL). The three individual plants marked are the individuals with an outstanding contribution to the seed rain. This contrast of images demonstrates that these now highly fecund individuals were pioneer individuals already established at this colonization front in 1977. We have validated the correct individual assignment by overlaying geographical coordinates, together with in situ spatial triangulation based on fixed landmarks. The historical image of 1977 comes from plane flights called ‘Vuelo Interministerial‘ carried out by the Instituto Geográfico Nacional (available at: https://fototeca.cnig.es/fototeca/). The 2020 satellite image is available in Google Earth Pro (see https://www.google.com/intl/es/earth/versions/#earth-pro). (b) Relationship between the plant canopy cover and the number of estimated dispersed seeds for each plant. The dark grey line represents the fitted log–log linear regression and the grey area spans the slope confidence interval at 95%. Note the log scale on the y-axes to improve visualization. Individual canopy cover here is used as a proxy for plant age. Plant individuals identified in A are indicated.