Does energy flux predict density‐dependence? An empirical field test

Abstract

Changes in population density alter the availability, acquisition, and expenditure of resources by individuals, and consequently their contribution to the flux of energy in a system. While both negative and positive density-dependence have been well studied in natural populations, we are yet to estimate the underlying energy flows that generate these patterns and the ambivalent effects of density make prediction difficult. Ultimately, density-dependence should emerge from the effects of conspecifics on rates of energy intake (feeding) and expenditure (metabolism) at the organismal level, thus determining the discretionary energy available for growth. Using a model system of colonial marine invertebrates, we measured feeding and metabolic rates across a range of population densities to calculate how discretionary energy per colony changes with density and test whether this energy predicts observed patterns in organismal size across densities. We found that both feeding and metabolic rates decline with density but that feeding declines faster, and that this discrepancy is the source of density-dependent reductions in individual growth. Importantly, we could predict the size of our focal organisms after eight weeks in the field based on our estimates of energy intake and expenditure. The effects of density on both energy intake and expenditure overwhelmed the effects of body size; even though higher density populations had smaller colonies (with higher mass-specific biological rates), density effects meant that these smaller colonies had lower mass-specific rates overall. Thus, to predict the contribution of organisms to the flux of energy in populations, it seems necessary not only to quantify how rates of energy intake and expenditure scale with body size, but also how they scale with density given that this ecological constraint can be a stronger driver of energy use than the physiological constraint of body size.

Influence of food, body size, and fragmentation on metabolic rate in a sessile marine invertebrate

“…In B. neritina , Svensson and Marshall () showed that food availability affects colony growth. Similarly, body size and fitness decrease with increasing conspecific densities (Allen, Buckley, & Marshall, ; Ghedini, White, & Marshall, ; Hart & Marshall, ). High conspecific densities, furthermore, result in decreased individual metabolic rates along with decreased feeding rates (Ghedini et al., ).…”

“…Similarly, body size and fitness decrease with increasing conspecific densities (Allen, Buckley, & Marshall, ; Ghedini, White, & Marshall, ; Hart & Marshall, ). High conspecific densities, furthermore, result in decreased individual metabolic rates along with decreased feeding rates (Ghedini et al., ). Here, reduced oxygen availabilities (Lagos, Barneche, White, & Marshall, ), or the presence of metabolites from conspecifics (Thompson et al., ), have been proposed to drive the observed decrease in metabolic rates.…”

Metabolic scaling across succession: Do individual rates predict community‐level energy use?

“…We suspect that a lower‐than‐expected metabolic rate may have been driven by metabolic suppression in response to a high density of conspecifics. This hypothesis is supported by recent studies, which have shown that per capita metabolic rates are reduced in dense populations (DeLong et al., ; Malerba, White, & Marshall, ), where conspecific density reduces energy use beyond the constraints of body size (Ghedini et al., ). Therefore, the overestimation of community metabolism could result from the high densities of Pyura reducing per capita metabolic rates in this species.…”

“…Therefore, the overestimation of community metabolism could result from the high densities of Pyura reducing per capita metabolic rates in this species. These densities might have altered the scaling exponent in a way that could not be predicted from our data on metabolic scaling of single Pyura individuals and that did not occur at lower densities (see Ghedini et al., for details). Nevertheless, whilst our results suggest that the use of physiological rates and individual body size might have limitations and likely exceptions, overall we found that they were good proxy of total community metabolism.…”

“…That metabolism scaled isometrically was surprising because, for each of the dominant species measured, metabolism scaled allometrically with individual mass (between 0.47 and 0.74). Furthermore, the mean size of the most abundant species ( Pyura ) and its abundance increased over time and larger and denser individuals are both predicted to decrease individual's mass‐specific energy use and thereby decrease community metabolism per gram of total biomass (DeLong et al., ; Ghedini et al., ; Gillooly et al., ). Yet, we resolved this paradox by reconstructing overall community metabolism from the size structure of the dominant members in the community and showed that individual metabolism was ultimately a good predictor of whole community metabolism.…”