Human-modified landscapes alter mammal resource and habitat use and trophic structure

Abstract

The broad negative consequences of habitat degradation on biodiversity have been studied, but the complex effects of natural-agricultural landscape matrices remain poorly understood. Here we used stable carbon and nitrogen isotopes to detect changes in mammal resource and habitat use and trophic structure between preserved areas and human-modified landscapes (HMLs) in a biodiversity hot spot in South America. We classified mammals into trophic guilds and compared resource use (in terms of C₃- and C₄-derived carbon), isotopic niches, and trophic structure across the 2 systems. In HMLs, approximately one-third of individuals fed exclusively on items from the agricultural matrix (C₄), while in preserved areas, ∼68% depended on forest remnant resources (C₃). Herbivores, omnivores, and carnivores were the guilds that most incorporated C₄ carbon in HMLs. Frugivores maintained the same resource use between systems (C₃ resources), while insectivores showed no significant difference. All guilds in HMLs except insectivores presented larger isotopic niches than those in preserved areas. We observed a complex trophic structure in preserved areas, with increasing δ¹⁵N values from herbivores to insectivores and carnivores, differing from that in HMLs. This difference is partially explained by species loss and turnover and mainly by the behavioral plasticity of resilient species that use nitrogen-enriched food items. We concluded that the landscape cannot be seen as a habitat/nonhabitat dichotomy because the agricultural landscape matrix in HMLs provides mammal habitat and opportunities for food acquisition. Thus, favorable management of the agricultural matrix and slowing the conversion of forests to agriculture are important for conservation in this region.

Keywords: agriculture; diet; landscape matrix; noninvasive sampling; stable isotope analysis.

Fig. 1.

Hypotheses of resource use and trophic structure. Regarding resource use, the reduction in forest cover causes a transition in the use of resources by mammals between preserved areas (predominantly C₃) and HMLs (predominantly C₄). Regarding trophic structure, in preserved areas, with more complete assemblages than HMLs, the trophic structure is more complex, and there is a stepwise increase in δ¹⁵N values from herbivores to carnivores. In HMLs, due to species loss and turnover in combination with the presence of agricultural matrices, which offers nitrogen-enriched food items, δ¹⁵N values fluctuate among trophic guilds, resulting in a modified trophic structure.

Fig. 2.

Comparison of δ¹³C and δ¹⁵N values among mammal trophic guilds in the Atlantic Forest, state of São Paulo, Brazil. Mean δ¹³C_corrected and δ¹⁵N_corrected values ±SD for mammal trophic guilds in (A and D) preserved areas, (B and E) HMLs, and (C and F) both systems together. Lowercase letters indicate relationships with significant differences (P < 0.01, P < 0.05). Her, herbivores; Fru, frugivores; Omn, omnivores; Ins, insectivores; Car, carnivores.

Fig. 3.

Resource use of mammals in the Atlantic Forest, state of São Paulo, Brazil. Percentages of individuals with C₃, mixed, or C₄ diets in trophic guilds (as indicated) in (A) preserved areas and (B) HMLs.

Fig. 4.

Mammal isotopic niches in the Atlantic Forest, state of São Paulo, Brazil. Corrected standard ellipse area (SEAc in ‰²; dotted lines), mean resource use (solid lines), and the percentage overlap of the different mammal trophic guilds in preserved areas (black) and HMLs (gray). (A) Herbivores, (B) frugivores, (C) omnivores, (D) insectivores, and (E) carnivores. Mean δ¹³C and δ¹⁵N values ±SD of the main resources consumed by each guild are included in the panels (filled forms indicate preserved areas; empty forms indicate HMLs).