An Ecosystem in Transition: The Emergence of Mixotrophy in the Arabian Sea

Abstract

In the last decade and half, the northern Arabian Sea has witnessed a radical shift in the composition of winter phytoplankton blooms. Diatoms typical of the winter monsoon and favored by nutrient-enriched waters from convective mixing have been replaced by thick and widespread blooms of a large, green dinoflagellate Noctiluca scintillans (Noctiluca). Unlike the exclusively heterotrophic red Noctiluca found in temperate waters, the green species of Noctiluca from the Arabian Sea is a mixotroph. It harbors hundreds of green, free-swimming cells of the symbiont Pedinomonas noctiluca, recently renamed as Protoeuglena noctilucae, Wang et al. (2016), within the central vacuole of its cytoplasm, and can sustain itself either through carbon fixation by its endosymbionts or via ingestion of exogenous prey. Data collected by us aboard Indian research vessels in the Arabian Sea suggest that these recent outbreaks of green Noctiluca blooms are being caused by the spread of hypoxic waters into the euphotic zone and possibly exacerbated by land runoff and enhanced stratification of the water column. Noctiluca is not a preferred food for micro- and mesozooplankton. Instead, its major consumers are mostly salps and jellyfish. It uses inorganic nutrients and grazes on other phytoplankton. Thus, it competes with both its prey and predators for resources, posing special challenges for ecosystem modeling studies. The emergence of this mixotroph as the major plankton player in the ecosystem will require a revision of our earlier understanding of the Arabian Sea food web dynamics and allied biogeochemistry gained from the Joint Global Flux Studies (JGOFS) expeditions of the 1990s.

Joaquim I. Goes and Helga do R. Gomes

Helga and Joaquim were born in Nairobi, Kenya, to parents who formed part of a large diasporic community from a Portuguese colony in India named Goa. Political turmoil forced them to return to Goa where they completed their education. They met at the National Institute of Oceanography (NIO) in Goa where Helga was pursuing her doctorate and Joaquim was a researcher. Oddly, they did not notice each other at the undergraduate college where they both studied. Joaquim believes that it was the free rides on his motorbike, and the many days spent on cruises in the balmy Indian Ocean that brought them together. After her Ph.D. on the characterization of phytoplankton extracellular products, Helga stayed on as a postdoctoral researcher at the NIO because she firmly believed that there was no better or more beautiful place to live in India than Goa. She still believes so! In 1992, Joaquim was offered a Doctoral fellowship by the Japanese Ministry of Education and they moved to Nagoya University, Japan. Clueless in a pre-internet age, they dived headlong into a new culture and language, and loved every bit of it from the sashimi and onsen to kanji. After Japan lost its ocean color satellite, Joaquim changed the course of his research. Molina and Rowland had just won the Nobel Prize for their work on the formation of the Ozone Hole. Little was then known on how ocean biology would respond to excess solar UV radiation. Working with the late and well-known geochemist, Prof. Nobuhiko Handa, Joaquim showed how enhanced exposure to UV radiation would profoundly impact phytoplankton photosynthesis. Later, Joaquim pursued his Postdoctoral studies under the late Prof. Toshiro Saino developing an algorithm to estimate nitrate distribution from remotely sensed products. A larger than life character, Prof. Saino loved science, good food, and wine and Joaquim and Helga had found the perfect mentor and friend. Fortuitously, Prof. Saino invited Joaquim to Hawaii for the Japan-USA workshop on ocean color where Joaquim met Barney Balch, who invited him to Bigelow Laboratory, Maine. Once again they embarked on a new journey, this time in a land of lobsters and vast expanses of untouched land often covered in a foot of snow. A year into his Postdoc, Joaquim was appointed as a Senior Research Scientist while Helga continued as a Research Associate. In 2010, they both felt the need for another adventure so they moved to the big city of New York where they now work at Lamont Doherty, Columbia University in the Palisades, New York.