A common scaling rule for abundance, energetics, and production of parasitic and free-living species

Abstract

The metabolic theory of ecology uses the scaling of metabolism with body size and temperature to explain the causes and consequences of species abundance. However, the theory and its empirical tests have never simultaneously examined parasites alongside free-living species. This is unfortunate because parasites represent at least half of species diversity. We show that metabolic scaling theory could not account for the abundance of parasitic or free-living species in three estuarine food webs until accounting for trophic dynamics. Analyses then revealed that the abundance of all species uniformly scaled with body mass to the -¾ power. This result indicates "production equivalence," where biomass production within trophic levels is invariant of body size across all species and functional groups: invertebrate or vertebrate, ectothermic or endothermic, and free-living or parasitic.

Fig. 1

Abundance as a function of body size for parasitic and free-living species in three estuaries: Carpinteria Salt Marsh (CSM), Estero de Punta Banda (EPB), and Bahía de San Quintin (BSQ). (A to C) Abundance versus body size reveals that a single regression line cannot adequately fit the data (general linear models: all interaction Ps < 0.0001; tables S2 and S3). Solid lines and top two equations give the slopes and intercepts for parasitic (P) and free-living (F) species; slope 95% confidence limits: CSM, ±0.14; EPB, ±0.13; BSQ, ±0.11. The broken lines, bottom equations, and R²s pertain to pooled data. (D to F) Temperature-corrected abundance versus body size gives relationships very similar to those seen in (A) to (C), although bird abundance is shifted up by about half an order of magnitude, leading to slightly shallower slopes for free-living and pooled data. Lines and equations as in (A) to (C); slope 95% confidence limits: CSM, ±0.13; EPB, ±0.12; BSQ, ±0.10. (G to I) Temperature-corrected abundance versus body size, statistically controlling for trophic level (Fig. 3 and tables S4 and S5). The scaling slopes are all consistent with the −¾ predicted by metabolic scaling, as slightly modified for the distribution of the number of species along the body-size axis (11); slope 95% confidence limits: CSM, ±0.073; EPB, ±0.073; BSQ, ±0.063. The R² values represent partial R²s for body size. Symbol key for all figures: circles, parasites; crosses, invertebrates; squares, fish; diamonds, birds.

Fig. 2

Variation in trophic level with body size, and in consumer-resource body-size ratios, for parasitic and free-living species in three estuarine food webs. (A to C) Relationship between trophic level and body size. Dashed lines represent separate relationships for parasitic and free-living species (Poisson regressions, all interaction Ps < 0.0001; tables S6 and S7), and solid lines represent significant curvilinear relationships for the two groups pooled (Poisson regressions, all quadratic term Ps < 0.0001; tables S8 and S9). Symbols as in Fig. 1. (D to F) Frequency distributions of logged consumer-resource body-size ratios. Shaded portions of the histograms represent parasites and unshaded portions represent free-living consumers. Values less than 0 are for consumers that are smaller than their resources. These data show wide variation in consumer-resource body-size ratios, in contrast to the more constrained values observed when ignoring parasites.

Fig. 3

(A to C) Abundance as a function of trophic level for parasitic and free-living species in three estuaries. Temperature-corrected abundance decreases with trophic level, as revealed by statistically controlling for body size (Fig. 1, G to I, and tables S4 and S5). The anti-log of the slope provides an estimate of ε, the overall trophic transfer efficiency in each ecosystem. Symbols as in Fig. 1.

Fig. 4

(A to C) Population biomass production versus body size for parasitic and free-living species in three estuaries, statistically controlling for trophic level. The slopes of the fitted lines in each estuary are in distinguishable from zero (tables S10 and S11); 95% confidence limits: CSM, ±0.073; EPB, ±0.073; BSQ, ±0.063. Symbols as in Fig. 1.