Individual behavior drives ecosystem function and the impacts of harvest

Abstract

Current approaches for biodiversity conservation and management focus on sustaining high levels of diversity among species to maintain ecosystem function. We show that the diversity among individuals within a single population drives function at the ecosystem scale. Specifically, nutrient supply from individual fish differs from the population average >80% of the time, and accounting for this individual variation nearly doubles estimates of nutrients supplied to the ecosystem. We test how management (i.e., selective harvest regimes) can alter ecosystem function and find that strategies targeting more active individuals reduce nutrient supply to the ecosystem up to 69%, a greater effect than body size-selective or nonselective harvest. Findings show that movement behavior at the scale of the individual can have crucial repercussions for the functioning of an entire ecosystem, proving an important challenge to the species-centric definition of biodiversity if the conservation and management of ecosystem function is a primary goal.

Fig. 1. Conceptual basis for study and map of study system.

(A) Population-level measures of trait variation for different species (colors) in a community, illustrating that variation among individuals within a single population (e.g., blue line) can exceed that of the entire community. (B) Selective harvest (gray lines) may have differential effects on ecosystem processes (being resilient or sensitive to certain harvest techniques), depending on how and what traits are selected for relative to nonselective harvest (i.e., random removal; black line). Dashed line represents a harvest rate that could result in various consequences for ecosystem processes. (C) Map of Abaco Island, The Bahamas, and satellite image of study location, a mangrove-lined estuary (~11.5 ha; 25°56′28″N, 77°16′26″W). White lines indicate the maximum extent of high tide, red lines indicate the minimum extent of low tide, and green circles indicate acoustic receiver locations.

Fig. 2. Individual behavioral traits strongly differ from population-level means.

(A) Histograms of raw data on site use per day and activity per day (time spent foraging) for both the gray and cubera snapper (blue and orange, respectively). Bars and associated dark lines indicate frequency of events within populations. (B) Individual-level site use per day and activity per day. Thin colored lines represent distributions of daily behavioral traits for each observed individual. Thick colored lines represent the population-level distribution (means across all individuals per day). Values associated with “Means” indicate the percentage of individual-level distributions that differ from the population-level means. These tests were run for the observed data (indicated by the colored text) and for simulated individuals that were generated by sampling randomly from normal distributions of site use per day and activity per day (indicated by gray text; distributions are not shown here for simplicity; Materials and Methods). (C) Site use and activity in relation to body size according to individual-level daily estimates (smaller transparent circles) and daily means across all individuals (larger circles with black outline). P values indicate the significance of the relationship between body size and mean behavioral trait. R² is indicated when the relationship is significant.

Fig. 3. Individual behavior affects nutrient supply and translocation and ecosystem-level nutrient dynamics.

(A and B) Distributions of the percent difference between observed estimates of population-level N supply per day (A) and N translocation per day (amount of N distributed across the estuary) (B) and populations simulated using models that are informed by the observed populations and incorporate behavior- and individual-level variation (“Behavior + ind. var.”—black bars and text) and behavior-free models that are informed only by the body size distributions of the observed populations (“Behavior free”—light gray bars and text). Values associated with text represent median differences between observed and simulated data. (C) Primary sources of N (NH₄⁺) supply (g day⁻¹) to the ecosystem: mass supply—calculated as the difference between net input and output from the system due to tidal flushing (Materials and Methods), deposition from rainfall, gray and cubera snapper, and the whole community (all species + gray and cubera snapper; Materials and Methods). Dashed portions of bars indicate estimated contribution of net supply due to behavior. Error bars associated with mass supply indicate the maximum (upper) and minimum (lower) estimates (see Materials and Methods). Error bars for population and community estimates represent 1 SD generated through bootstrapping procedures (Materials and Methods).

Fig. 4. Selective harvest disproportionately reduces ecosystem-level nutrient supply.

Reductions in population level of N supply and translocation for gray and cubera snapper (blue and orange, respectively) from selective and nonselective harvest of 50% of individuals from unfished populations. Asterisks (***) indicate all values are significantly different [P < 0.01; analysis of variance (ANOVA) with Tukey post hoc test]. Behavior selective and body size selective represent fishing that selects against active individuals and large individuals, respectively. We carried out simulated fishing by removing the top 50% of active and large individuals for angling and spearing, respectively. Nonselective is fishing with random removal (see Materials and Methods and figs. S3 and S4 for results for harvest at 30 to 70%).