Linking Anthropogenic Landscape Perturbation to Herbivory and Pathogen Leaf Damage in Tropical Tree Communities

Abstract

Anthropogenic disturbance of tropical humid forests leads to habitat loss, biodiversity decline, landscape fragmentation, altered nutrient cycling and carbon sequestration, soil erosion, pest/pathogen outbreaks, among others. Nevertheless, the impact of these alterations in multitrophic interactions, including host-pathogen and vector-pathogen dynamics, is still not well understood in wild plants. This study aimed to provide insights into the main drivers for the incidence of herbivory and plant pathogen damage, specifically, into how vegetation traits at the local and landscape scale modulate such interactions. For this purpose, in the tropical forest of Calakmul (Campeche, Mexico), we characterised the foliar damage caused by herbivores and pathogens in woody vegetation of 13 sampling sites representing a gradient of forest disturbance and fragmentation in an anthropogenic landscape from well preserved to highly disturbed and fragmented areas. We also evaluated how the incidence of such damage was modulated by the vegetation and landscape attributes. We found that the incidence of damage caused by larger, mobile, generalist herbivores, was more sensitive to changes in landscape configuration, while the incidence of damage caused by small and specialised herbivores with low dispersal capacity was more influenced by vegetation and landscape composition. In relation to pathogen symptoms, the herbivore-induced foliar damage seems to be the main factor related to their incidence, indicating the enormous importance of herbivorous insects in the modulation of disease dynamics across tropical vegetation, as they could be acting as vectors and/or facilitating the entry of pathogens by breaking the foliar tissue and the plant defensive barriers. The incidence of pathogen damage also responded to vegetation structure and landscape configuration; the incidence of anthracnose, black spot, and chlorosis, for example, were favoured in sites surrounded by smaller patches and a higher edge density, as well as those with a greater aggregation of semi-evergreen forest patches. Fungal pathogens were shown to be an important cause of foliar damage for many woody species. Our results indicate that an increasing transformation and fragmentation of the tropical forest of southern Mexico could reduce the degree of specialisation in plant-herbivore interactions and enhance the proliferation of generalist herbivores (chewers and scrapers) and of mobile leaf suckers, and consequently, the proliferation of some symptoms associated with fungal pathogens such as fungus black spots and anthracnose. The symptoms associated with viral and bacterial diseases and to nutrient deficiency, such as chlorosis, could also increase in the vegetation in fragmented landscapes with important consequences in the health and productivity of wild and cultivated plant species. This is a pioneering study evaluating the effect of disturbances on multitrophic interactions, offering key insights on the main drivers of the changes in herbivory interactions and incidence of plant pathogens in tropical forests.

Keywords: anthropic disturbance; herbivory damage; multitrophic interactions; plant-pathogen damage; tropical humid forest.

Figure 1

(a) Satellite map of the study area in the Calakmul natural reserve, circumferences illustrate 5000 m around sampling plots. Colours indicate the type of vegetation coverage at each site. (b) NMDS ordinations mapping landscape traits in terms of the composition of the vegetation at 5000 m around the sampling plots. (c) NMDS ordinations mapping landscape traits in terms of shape and area of semideciduous forest at 5000 m around sampling plots. (d) NMDS ordinations mapping landscape traits in terms of configuration of the vegetation at 5000 m around the sampling plots. Pearson correlation coefficients of landscape traits are located adjacently to their correspondent NDMS axes scores. Significant correlations are displayed in bold font. Nomenclature of the landscape attributes considered in ordinations: Afi (Agricultural field coverage), SFo* (Secondary semi-evergreen forest coverage), SFo (Semi-evergreen forest coverage), TFo (Thorn forest coverage), Area (Mean area of semi-evergreen forest patches coverage), ED (Edge density of semi-evergreen forest patches), Shape (Shape index of semi-evergreen forest patches), CLUMPY (Clumpiness index of patches adjacent to patches of other land-cover classes), IJI (Interspersion and juxtaposition index of the semi-evergreen forest), MESH (degree of vegetation subdivision—effective mesh size), ENN (Mean nearest neighbour distance among patches).

Figure 2

Non –Metric Multidimensional Scaling Ordinations mapping plant communities’ dissimilarities in terms of species composition (a) and vegetation structure (b). Vegetation traits considered for the ordinations were plant area index (PAI, m²/m²), total number of branches (No. branches), average of the tallest trees (Canopy Height, m), total number of individuals (No. individuals), and total basal area (SBA, m²/ha). Pearson correlation coefficient is presented for the structure of the vegetation describing the relationship between vegetation attributes and ordination axes. Phylogenetic tree of all species considered in this study (c) was calculated through the mean nearest taxonomic distance (MNTD). Branch length represent in millions of years, scalebar = 50 my.

Figure 3

Non-Metric Multidimensional Scaling Ordinations mapping plant communities’ dissimilarities in terms of herbivory (a) and symptomatology (b).

Figure 4

Tripartite network interaction of the tree species present at the 13 sampling plots, displaying, at the right-side, interactions with herbivore insect guilds that cause specific foliar damage and, at the left-side, the interactions with symptoms related to plant pathogens. The d index represents the degree of interaction specialisation of each foliar damage with the tree species. Each described damage is complemented by a representative image of the foliar damage found during field work. The acronyms of the species are provided in the supplementary material.