Evolution of body size, vision, and biodiversity of coral-associated organisms: Evidence from fossil crustaceans in cold-water coral and tropical coral ecosystems

Abstract

Background: Modern cold-water coral and tropical coral environments harbor a highly diverse and ecologically important macrofauna of crustaceans that face elevated extinction risks due to reef decline. The effect of environmental conditions acting on decapod crustaceans comparing these two habitats is poorly understood today and in deep time. Here, we compare the biodiversity, eye socket height as a proxy for eye size, and body size of decapods in fossil cold-water and tropical reefs that formed prior to human disturbance. Results: We show that decapod biodiversity is higher in fossil tropical reefs from The Netherlands, Italy, and Spain compared to that of the exceptionally well-preserved Paleocene (Danian) cold-water reef/mound ecosystem from Faxe (Denmark), where decapod diversity is highest in a more heterogeneous, mixed bryozoan-coral habitat instead of in coral and bryozoan-dominated facies. The relatively low diversity at Faxe was not influenced substantially by the preceding Cretaceous/Paleogene extinction event that is not apparent in the standing diversity of decapods in our analyses, or by sampling, preservation, and/or a latitudinal diversity gradient. Instead, the lower availability of food and fewer hiding places for decapods may explain this low diversity. Furthermore, decapods from Faxe are larger than those from tropical waters for half of the comparisons, which may be caused by a lower number of predators, the delayed maturity, and the increased life span of crustaceans in deeper, colder waters. Finally, deep-water specimens of the benthic crab Caloxanthus from Faxe exhibit a larger eye socket size compared to congeneric specimens from tropical reefs, suggesting that dim light conditions favored the evolution of relatively large eyes. Conclusions: The results suggest a strong habitat control on the biodiversity of crustaceans in coral-associated environments and that the diversity difference between deep, cold-water reefs and tropical reefs evolved at least ~63 million years ago. Futhermore, body size and vision in crustaceans evolved in response to environmental conditions in the deep sea. We highlight the usefulness of ancient reefs to study organismal evolution and ecology.