Research Article

Metabolic asymmetry and the global diversity of marine predators

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Science  25 Jan 2019:
Vol. 363, Issue 6425, eaat4220
DOI: 10.1126/science.aat4220

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Cold is better for polar predators

Generally, biodiversity is higher in the tropics than at the poles. This pattern is present across taxa as diverse as plants and insects. Marine mammals and birds buck this trend, however, with more species and more individuals occurring at the poles than at the equator. Grady et al. asked why this is (see the Perspective by Pyenson). They analyzed a comprehensive dataset of nearly 1000 species of shark, fish, reptiles, mammals, and birds. They found that predation on ectothermic (“cold-blooded”) prey is easier where waters are colder, which generates a larger resource base for large endothermic (“warm-blooded”) predators in polar regions.

Science, this issue p. eaat4220; see also p. 338

Structured Abstract

INTRODUCTION

One of the most general patterns in ecology is that diversity increases toward the equator. In the ocean, however, mammal and bird richness generally peak in colder, temperate waters. This pattern is especially puzzling given the thermal stress that cold water imposes on warm-bodied endotherms, which must maintain constant, elevated body temperatures through metabolic activity. In contrast, ectothermic fish and reptiles that rely on ambient heat to regulate their body temperature show the highest diversity in tropical and subtropical habitats.

RATIONALE

Large, predatory vertebrates regulate food webs across marine systems. Their distribution varies strongly with thermoregulatory strategy, but the underlying mechanisms are unclear. Using theory and data, we sought to clarify the physiological and ecological processes that lead to opposing patterns of diversity in marine predators.

RESULTS

To identify spatial patterns of diversity, we synthesized range maps from 998 species of marine sharks, teleost fish, mammals, birds, and sea snakes. We found that most families of endothermic mammals and birds show elevated richness in temperate latitudes, whereas ectothermic sharks and fish peak in tropical or subtropical seas. These findings are reinforced by our analysis of phylogenetic diversity, which weights diversity by species’ evolutionary relatedness.

The strong latitudinal signal is suggestive of thermal controls on diversity, but other environmental features may be relevant. In particular, large, productive, or coastal habitats tend to support more species regardless of thermoregulatory strategy. Endotherm phylogenetic diversity and richness generally peak between 45° and 60° latitude, but when we take the ratio of endotherm to ectotherm richness—correcting for shared spatial drivers—endotherm richness increases systematically toward the coldest polar oceans.

We then determined quantitatively and theoretically how these differences are linked to thermal physiology. We found that the metabolic response to ambient temperature is asymmetric between endotherms and ectotherms: Endothermic metabolism is generally constant, but in ectothermic fish, burst speed, routine swimming speed, neural firing rates, saccadic eye movement, and visual flicker fusion frequencies fall exponentially in colder water. This has trophic and competitive implications for marine species. Ectothermic prey are sluggish in the cold and easier for mammals and birds to capture, whereas slow-moving, predatory sharks are easier to avoid. As a result, marine endotherms are competitively favored over ectothermic predators as water temperatures decline.

We tested our theory against a global dataset of pinniped and cetacean abundance and foraging rates. As predicted, we found that mammal consumption and density increase log-linearly with water temperature after correcting for productivity. From the equator to the poles, marine mammal consumption of available food increases by a factor of ~80.

CONCLUSION

Our results and theory highlight the importance of energetics in species interactions and the ecological and evolutionary consequences of endothermy at global scales. Although elevated metabolism is costly, it provides foraging and competitive benefits that underpin the distribution and abundance of marine endotherms. Our findings also have implications for conservation. Rising ocean temperatures are predicted to exert substantial additional constraints on mammal and bird populations independent of food production or habitat conditions, and may alter the balance of marine endotherms and ectotherms across the globe.

Water temperature drives differences in metabolism and diversity between marine endotherms and ectotherms.

Marine endothermic predators show contrasting patterns of phylogenetic diversity with ectotherms, where phylogenetic diversity is the sum of evolutionary distances between co-occurring species and darker colors represent higher diversity. Unlike most other taxa, mammal and bird phylogenetic diversity peaks in cold, temperate latitudes. Theory and data suggest that this reflects differences in thermoregulation. In particular, thermal gradients across latitude generate an asymmetric response in metabolic, sensory, and locomotory rates between endotherms (which maintain constant rates) and ectotherms (which respond exponentially). As a result, colder water is more favorable to endothermic predators pursuing sluggish ectothermic prey or avoiding slower ectothermic sharks.

Abstract

Species richness of marine mammals and birds is highest in cold, temperate seas—a conspicuous exception to the general latitudinal gradient of decreasing diversity from the tropics to the poles. We compiled a comprehensive dataset for 998 species of sharks, fish, reptiles, mammals, and birds to identify and quantify inverse latitudinal gradients in diversity, and derived a theory to explain these patterns. We found that richness, phylogenetic diversity, and abundance of marine predators diverge systematically with thermoregulatory strategy and water temperature, reflecting metabolic differences between endotherms and ectotherms that drive trophic and competitive interactions. Spatial patterns of foraging support theoretical predictions, with total prey consumption by mammals increasing by a factor of 80 from the equator to the poles after controlling for productivity.

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