Extreme Inverted Trophic Pyramid of Reef Sharks Supported by Spawning Groupers

Abstract

The extent of the global human footprint [1] limits our understanding of what is natural in the marine environment. Remote, near-pristine areas provide some baseline expectations for biomass [2, 3] and suggest that predators dominate, producing an inverted biomass pyramid. The southern pass of Fakarava atoll-a biosphere reserve in French Polynesia-hosts an average of 600 reef sharks, two to three times the biomass per hectare documented for any other reef shark aggregations [4]. This huge biomass of predators makes the trophic pyramid inverted. Bioenergetics models indicate that the sharks require ∼90 tons of fish per year, whereas the total fish production in the pass is ∼17 tons per year. Energetic theory shows that such trophic structure is maintained through subsidies [5-9], and empirical evidence suggests that sharks must engage in wide-ranging foraging excursions to meet energy needs [9, 10]. We used underwater surveys and acoustic telemetry to assess shark residency in the pass and feeding behavior and used bioenergetics models to understand energy flow. Contrary to previous findings, our results highlight that sharks may overcome low local energy availability by feeding on fish spawning aggregations, which concentrate energy from other local trophic pyramids. Fish spawning aggregations are known to be targeted by sharks, but they were previously believed to play a minor role representing occasional opportunistic supplements. This research demonstrates that fish spawning aggregations can play a significant role in the maintenance of local inverted pyramids in pristine marine areas. Conservation of fish spawning aggregations can help conserve shark populations, especially if combined with shark fishing bans.

Natural variation in coral reef trophic structure across environmental gradients

“…For example, spawning aggregations that attract and concentrate predators can lead to temporarily inverted trophic pyramids that would not exist outside of this specific temporal period (Mourier et al . ). Such inverted pyramids have been reported from small‐scale surveys on remote coral reefs (Friedlander and DeMartini ; DeMartini et al .…”

Food quantity–quality interactions and their impact on consumer behavior and trophic transfer

“…Their existence, however, is often attributed to continuous subsidies from external habitats, migration of top predators across ecosystem boundaries or temporal storage effects (Mourier et al. , McCauley et al. ).…”

Mass spawning aggregation of the giant bumphead parrotfish Bolbometopon muricatum

“…The location of the spawning aggregation adjacent to a channel in the western barrier reef on the outside of the lagoon may serve to advect gametes away from high densities of planktivores on the reef crests (Colin, ). In contrast to grouper (family Serranidae, Epinephelinae) spawning aggregations in the Pacific Ocean (Mourier et al, ), sharks were absent from the spawning aggregation, presumably due to large size of B. muricatum (Gladstone, ). Large sharks [notably Carcharhinus leucas (Valenciennes 1839) and Carcharhinus limbatus (Valenciennes 1839)] have been observed at the same spawning site for red snapper Lutjanus bohar (Forsskål 1775) spawning aggregations, which suggests that sharks are selective in targeting spawning aggregations of reef fish.…”