Metabolic dominance of bivalves predates brachiopod diversity decline by more than 150 million years

Abstract

Brachiopods and bivalves feed in similar ways and have occupied the same environments through geological time, but brachiopods were far more diverse and abundant in the Palaeozoic whereas bivalves dominate the post-Palaeozoic, suggesting a transition in ecological dominance 250 Ma. However, diversity and abundance data alone may not adequately describe key changes in ecosystem function, such as metabolic activity. Here, we use newly compiled body size data for 6066 genera of bivalves and brachiopods to calculate metabolic rates and revisit this question from the perspective of energy use, finding that bivalves already accounted for a larger share of metabolic activity in Palaeozoic oceans. We also find that the metabolic activity of bivalves has increased by more than two orders of magnitude over this interval, whereas brachiopod metabolic activity has declined by more than 50%. Consequently, the increase in bivalve energy metabolism must have occurred via the acquisition of new food resources rather than through the displacement of brachiopods. The canonical view of a mid-Phanerozoic transition from brachiopod to bivalve dominance results from a focus on taxonomic diversity and numerical abundance as measures of ecological importance. From a metabolic perspective, the oceans have always belonged to the clams.

Keywords: Phanerozoic; competition; invertebrate; macroevolution; metabolism; palaeoecology.

Figure 1.

Trends in the absolute and proportional diversity, occurrence frequency and metabolic contribution of bivalves versus brachiopods over the past 465 Myr, illustrating that although bivalves constituted a small fraction of taxonomic diversity and fossil occurrences during the Palaeozoic (more than 250 Ma), they already accounted for more than half of all metabolic activity. (a,b) Genus diversity. (c,d) Occurrence frequency. (e,f) Total metabolic activity based on the per genus metric using range-through treatment of genera reported in the PaleoDB. (g,h) Total metabolic activity based on the per occurrence metric. Grey curves in b, d, f and h represent lowess fits to the proportional data. All increasing trends in proportional data are statistically significant based upon Spearman rank order correlation with time (b: ρ = 0.97, p < 0.0001; d: ρ = 0.93, p < 0.0001; f: ρ = 0.98, p < 0.0001; h: ρ = 0.94, p < 0.0001). (Online version in colour.)

Figure 2.

Trends in the contribution of bivalves to total specimens of both bivalves and brachiopods and metabolic activity within fossil assemblages containing both clades, illustrating the long-term increase in mean metabolic activity and the large proportional contribution of bivalves to individual collections even during Palaeozoic time. (a) Mean per capita metabolic rate. (b) Proportion of specimens accounted for by bivalves. (c) Proportion of metabolic activity accounted for by bivalves. Open grey circles—mean values for individual fossil collections. Filled black circles—mean values across collection means within a stage for stages represented by five or more collections. Black curves represent lowess fits to the data. All increasing trends are statistically significant based upon Spearman rank order correlation with time (a: ρ = 0.49, p < 0.0001; b: ρ = 0.41, p < 0.0001; c: ρ = 0.59, p < 0.0001).

Figure 3.

Comparison of mean per taxon, per occurrence and per capita metabolic rates of bivalves and brachiopods over the past 465 Myr, illustrating a long-term increase by nearly three orders of magnitude and close agreement across all metrics relative to change over time. Per taxon rates were calculated both using a range-through method (in which a genus is assumed to be present in all stages between its first and last known occurrences) and a sampled-in-bin method (in which a genus is only included in the calculation of the mean value when it has a known occurrence within a given stage). All increasing trends are statistically significant based upon Spearman rank order correlation with time (per occurrence: ρ = 0.78, p < 0.0001; range-through PaleoDB: ρ = 0.98, p < 0.0001; sampled in bin: ρ = 0.96, p < 0.0001; per capita: ρ = 0.84, p < 0.0001). (Online version in colour.)

Figure 4.

Sensitivity analysis showing that the increase in mean metabolic rate is unaffected by uncertainties related to temperature, the tissue mass and per-gram metabolic rate of brachiopods and the extremes in the size distribution. Results presented here use the mean metabolic rate per occurrence because per genus rates cannot be made spatially explicit to account for temperature gradients and per capita rates are too sparse for the Cenozoic due to the rarity of brachiopods. (a) Influence of temperature on calculated metabolic rates. First, we assumed that all taxa experienced the same temperature (constant temperature: 15°C). Second, we assumed that global mean temperatures did not vary over geological time, but that a linear, 30°C temperature gradient (0–30°C) has always existed from the equator to the poles (latitude correction only). Third, we assumed that both global mean temperature has varied following the palaeoclimate reconstruction of Royer et al. [36] and there has always existed a temperature gradient of approximately 30°C from equator to pole (full temperature correction). (b) Influence of assumptions regarding soft tissue mass and b₀ values on trends in metabolic rates, illustrating the comparatively small effect of uncertainty in these parameters. The long-term increase in mean metabolic rate is indicated even under the unrealistically conservative assumptions that brachiopods and bivalves have the same scaling of shell length to AFDM and the same b₀ values. (c) Influence of small and large taxa on trends in metabolic rates. Mean metabolic rates are virtually unaffected by the exclusion of all genera less than 10 mm in maximum dimension. Mean metabolic rates are systematically lower when the largest 10% of occurrences are excluded from each stage, particularly during the Early Mesozoic, but the direction and magnitude of the Phanerozoic trend in mean metabolic rate is unaffected. (Online version in colour.)

Figure 5.

Trends in the mean sizes (a) and per occurrence metabolic rates (b) of bivalves and brachiopods over the past 465 Myr, illustrating that the long-term increase in overall metabolic rate is due to both the larger sizes of bivalves and their increase in proportional occurrence frequency towards this day, with an additional contribution from a long-term increase in mean bivalve size. Sizes are means across genera from the range-through treatment of the PaleoDB. Mean metabolic rates across genera following the per occurrence treatment with corrections for latitude and secular variation in global mean surface temperature. Increases in size over time are statistically significant across all genera (ρ = 0.96, p < 0.0001) and bivalves alone (ρ = 0.86, p < 0.0001) but not within brachiopods (ρ = 0.13, p = 0.25). Increases in per occurrence metabolic rate over time are statistically significant across all occurrences (ρ = 0.78, p < 0.0001) and bivalves alone (ρ = 0.66, p < 0.0001) but not within brachiopods (ρ = −0.14, p = 0.19). (Online version in colour.)