Emergent properties of species-habitat networks in an insular forest landscape

Abstract

Deforestation and fragmentation are pervasive drivers of biodiversity loss, but how they scale up to entire landscapes remains poorly understood. Here, we apply species-habitat networks based on species co-occurrences to test the effects of insular fragmentation on multiple taxa-medium-large mammals, small nonvolant mammals, lizards, understory birds, frogs, dung beetles, orchid bees, and trees-across 22 forest islands and three continuous forest sites within a river-damming quasi-experimental landscape in Central Amazonia. Widespread, nonrandom local species extinctions were translated into highly nested networks of low connectance and modularity. Networks' robustness considering the sequential removal of large-to-small sites was generally low; between 5% (dung beetles) and 50% (orchid bees) of species persisted when retaining only <10 ha of islands. In turn, larger sites and body size were the main attributes structuring the networks. Our results raise the prospects that insular forest fragmentation results in simplified species-habitat networks, with distinct taxa persistence to habitat loss.

Fig. 1.. Conceptual diagram illustrating the fragmented landscape, co-occurring species, and the resulting species-habitat networks and their properties.

The diagram represents both all taxa combined [multitaxa, (A)] and each individual taxon [single-taxon (B)] species-habitat networks based on species co-occurrences. In (A), the fragmented landscape is represented in gray, including six hypothetic habitat fragments, each of which is represented by a different color. The color code attributed to each of these fragments is maintained in (B). Network properties were examined at the landscape level (C) and node level (D), which includes both site and species traits. Landscape-level properties included network connectance, modularity, nestedness, and robustness (C), and node-level properties included normalized degree and nestedness contribution (D). At the site level, predictors included landscape-, patch-, and habitat-related metrics such as forest patch size, degree of isolation, and habitat quality. At the species level, predictors included species functional traits hypothesized to affect species persistence across the landscape such as the degree of dispersal capacity and habitat specialization.

Fig. 2.. Sampling sites within the Balbina Hydroelectric Dam Landscape in Central Brazilian Amazonia.

Sampling sites include 22 forest islands (in red and highlighted by a 500-m buffer) and three continuous forest sites in the mainland (indicated by red squares). The inset map shows an aerial view of the Balbina insular landscape (photo credit: E. M. Venticinque), including the reservoir open-water matrix.

Fig. 3.. Graphic representation of the species-habitat networks.

We considered networks both (A) combining all taxa and each taxon separately: (B) medium-large mammals, (C) small nonvolant mammals, (D) lizards, (E) understory birds, (F) frogs, (G) dung beetles, (H) orchid bees, and (I) trees. Nodes correspond to survey sites (squares, dark green colored) and species (circles, color-coded for each taxonomic group). In (A), nodes are sized according to degree (log₁₀ x) of sites and species, and links between sites and species are color-coded according to the taxonomic group to which each species belongs. In (B) to (I), nodes are sized according to the normalized degree and color-coded for each taxonomic group. In (G), the smaller module is not scaled but amplified for visualization purposes.

Fig. 4.. Landscape-level properties characterizing the network structure of each taxonomic group and all groups combined.

Landscape-level properties include (A) connectance, (B) modularity, (C) nestedness, and (D) robustness, given the sequential loss of forest sites ordered by decreasing area. Taxa include medium-large mammals, small nonvolant mammals, lizards, understory birds, frogs, dung beetles, orchid bees, and trees and all taxa combined. Solid dots represent the observed values of each metric. Boxplots indicate the median, first and third quartiles, and minimum and maximum expected values of each metric obtained using the null model r1 (see main text for details). Red asterisks indicate statistically significant values given by −2 > z > 2 (table S4). Each taxonomic group is represented by the same icon, and the corresponding boxplot is colored as in Fig. 3. Taxa are ordered by observed values.

Fig. 5.. Proportion (%) of species persisting across the Balbina landscape.

Two alternative scenarios are provided given the sequential loss of forest sites ordered by decreasing (A) and increasing forest area (B). The number of secondary species extinctions following habitat removal was obtained using the second.extinct function (22) from the bipartite R package (63), which considers the total number of species recorded for each taxon. Results are indicated for each taxon: medium-large mammals, small nonvolant mammals, lizards, understory birds, frogs, dung beetles, orchid bees, and trees. Each taxon is represented by the same icon and corresponding color-coded circles, as in Fig. 3. Lines correspond to the adjusted trend using the geom_smooth function considering span = 1.5, based on the ggplot2 R package (68).

Fig. 6.. Predictors of site-level network properties for each taxon and all taxa combined.

Network properties included (A) site normalized degree and (B) site nestedness contribution. Predictors included forest area (log₁₀ x; Area), distance to mainland continuous forest (Dist), proportion of closed-canopy forest (%Closed-canopy), and burn severity (Burn). The interaction terms between Area and Dist and Area and Burn were retained in the models only in case this ensured a significant explanation of the response variable, represented by the asterisks. Circles are sized according to the estimate obtained from averaged models (see further details on model results in tables S5 and S6). Blue and red circles denote positive and negative estimates, respectively. Only statistically significant variables (P ≤ 0.05) in average models are shown. Each taxon is represented by the same icon as in Fig. 3.

Fig. 7.. Relationship between species-level network properties and forest area (log₁₀ x; hectares).

Network properties included (A) species normalized degree and (B) species nestedness contribution. Lines represent the adjusted linear model between the network property and forest area. Each taxon is represented by the same icon, and corresponding circles and lines are color-coded as in Fig. 3.