The effects of ocean acidification on zooplankton: Using natural CO2 seeps as windows into the future

Since the beginning of the Industrial Revolution, carbon dioxide (CO2) has been emitted into the atmosphere at rates unprecedented to Earth’s history. Nearly 30% of the anthropogenic CO2 in the atmosphere has been absorbed in surface waters of the ocean, pushing carbonate chemistry towards increased bicarbonate ions and hydrogen protons and decreased carbonate ions. Consequently, seawater pH has decreased from pre-Industrial Revolution levels of 8.2 to current levels of 8.1, and it is expected to continue to drop to 7.8 by the year 2100 if carbon emissions continue as predicted. The combination of these effects is referred to as ocean acidification. It is at the forefront of marine research as it poses a serious threat to several marine organisms and ecosystems. Ocean acidification has the most notable direct effect on calcifying organisms with calcium carbonate skeletons and shells, because fewer carbonate ions in the water column result in reduced calcification. Coral reefs are especially vulnerable to ocean acidification since reefs are composed of complex carbonate structures. Coral reefs have a high biodiversity; thus, not only will the corals themselves be affected by ocean acidification, but so will many of the animals that dwell in them.

The primary objective of this thesis was to examine the effects of ocean acidification on demersal zooplankton that reside in coral reefs. Ocean acidification research on zooplankton has primarily been single- species experiments on calcifying species or generalist copepod species. Scaling-up to experiments examining ocean acidification effects on entire zooplankton communities is logistically difficult, thus the ability to predict community changes in zooplankton due to ocean acidification has been rather limited. However, a few locations around the world have submarine volcanic CO2 seeps that can be used as natural laboratories to study ecosystem effects of ocean acidification. Two CO2 seeps located in coral reefs in Papua New Guinea were used as windows into the future to examine the effects of ocean acidification on entire zooplankton communities while they live naturally in their environment. Over three expeditions to two CO2 seeps, nocturnal plankton were sampled with horizontal net tows and emergence traps. Additional experiments were also conducted, and collectively this work is summarized in chapters 2-5 as outlined below.

Chapter 2 reports on the observed changes in zooplankton abundance and community composition between control and high-CO2 sites. Consistent results between seep sites and expeditions showed that zooplankton abundances were reduced three-fold under high-CO2 conditions. The abundance loss was partially attributed to habitat change within the coral reef, from more structurally complex corals in the control sites to a replacement of massive bouldering corals in the high-CO2 sites. The loss of structural complexity in the reef meant there were fewer hiding spaces for the zooplankton to seek refuge in during the day. All zooplankton taxa were reduced under high-CO2 conditions but to varying levels, suggesting that each taxon reacts differently to ocean acidification. Since each taxonomic group within the zooplankton communities was reduced to varying levels under ocean acidification, the copepod genus with the largest reduction in abundance was investigated in more detail. Labidocera spp. are pontellid copepods that are generally considered surface-dwellers and are not known to inhabit coral reefs. Therefore, as a preface to the ocean acidification study, the new discovery of these copepods living in coral reefs is first described (Chapter 3). Not only were they found to be residential to the reef, but Labidocera spp. living at the control reefs preferred to reside in coral rubble, macroalgae, and turf algae. Labidocera spp. were one of the most sensitive copepods to high-CO2 conditions and were reduced by nearly 70% in abundance, prompting a more detailed investigation about the effect of ocean acidification on their physiology and habitat preference (Chapter 4). Physiological parameters, e.g. size, feeding, and oocyte development, were unaffected by ocean acidification. Unlike the zooplankton community as a whole, the main cause for the abundance loss of Labidocera spp. was not a shift in the habitat because their preferred substrata were of equal percent coverage across high-CO2 and control sites. Instead, Labidocera spp. were no longer associated with any substrata type. Multiple direct and indirect effects of ocean acidification will act on each zooplankton taxa separately, and their collective response will contribute to the community response. The effects of ocean acidification on zooplankton communities were then scaled up to potential impacts on entire ecosystems. Zooplankton are the primary food source for corals, fish, and other zooplanktivores. The impacts of ocean acidification on zooplankton communities will have cascade effects on the food chain via the pathway of zooplanktivorous organisms. A case study on the stony coral Galaxea fascicularis explored the effects of ocean acidification on the ability of corals, which had lived their entire lives under high-CO2 conditions, to feed on zooplankton (Chapter 5). Under anthropogenic changes, whether it is from bleaching, high turbidity, or ocean acidification, some corals rely more on heterotrophy and consume more zooplankton. Contrary to expectation, this study showed that when given equal quantities of food particles these corals consumed less zooplankton under ocean acidification. Corals rely on heterotrophy for essential nutrients, like nitrogen and phosphorus, which they cannot otherwise obtain from autotrophy and their symbiotic zooxanthellae.

In conclusion, my thesis shows that not only is there fewer zooplankton available to consume, but the existing zooplankton is consumed with lower capture rates under high CO2 conditions. Coral reefs in future oceans will likely have reduced zooplankton abundances as an indirect effect of ocean acidification, partially caused by a change in habitat from branching corals to more massive bouldering corals. Zooplankton abundances were reduced yet the community composition was unaffected by ocean acidification. All zooplankton taxa were reduced yet present under high-CO2 conditions suggesting that the zooplankton are at least able to survive under ocean acidification. Fewer zooplankton will be available to zooplanktivores, but the fatty acid content and nutritional value of the zooplankton as a food source is expected to be similar to current food. Together this is expected to negatively impact the entire coral reef ecosystem, with some coral species unable to consume zooplankton at normal rates. In an ecosystem already highly vulnerable to ocean acidification, coral reefs may be even more threatened if the very basis of their food webs is reduced.

Smith J., 2016. The effects of ocean acidification on zooplankton: Using natural CO2 seeps as windows into the future. PhD thesis, University of Plymouth. Thesis (restricted access).

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