Additive Pressures of Elevated Sea Surface Temperatures and Herbicides on Symbiont-Bearing Foraminifera

Abstract

Elevated ocean temperatures and agrochemical pollution individually threaten inshore coral reefs, but these pressures are likely to occur simultaneously. Experiments were conducted to evaluate the combined effects of elevated temperature and the photosystem II (PSII) inhibiting herbicide diuron on several types of symbiotic algae (diatom, dinoflagellate or rhodophyte) of benthic foraminifera in hospite. Diuron was shown to evoke a direct effect on photosynthetic efficiency (reduced effective PSII quantum yield ΔF/F′m), while elevated temperatures (>30°C, only 2°C above current average summer temperatures) were observed to impact photosynthesis more indirectly by causing reductions in maximum PSII quantum yield (Fv/Fm), interpreted as photodamage. Additionally, elevated temperatures were shown to cause bleaching through loss of chlorophyll a in foraminifera hosting either diatoms or dinoflagellates. A significant linear correlation was found between reduced Fv/Fm and loss of chlorophyll a. In most cases, symbionts within foraminifera proved more sensitive to thermal stress in the presence of diuron (≥1 µg L−1). The mixture toxicity model of Independent Action (IA) described the combined effects of temperature and diuron on the photosystem of species hosting diatoms or dinoflagellates convincingly and in agreement with probabilistic statistics, so a response additive joint action can be assumed. We thus demonstrate that improving water quality can improve resilience of symbiotic phototrophs to projected increases in ocean temperatures. As IA described the observed combined effects from elevated temperature and diuron stress it may therefore be employed for prediction of untested mixtures and for assessing the efficacy of management measures.

Combined effects of warming and ocean acidification on coral reef Foraminifera Marginopora vertebralis and Heterostegina depressa

“…In an experiment increasing nutrient levels and elevating pCO 2 , photosymbiont concentration in M. rossi was reduced more under the combined stress than when individual stressors acted in isolation (Reymond et al 2013). van Dam et al (2012) showed that populations of Foraminifera exposed to the herbicide Diuron become disproportionately more sensitive to temperature and both factors acted additively on the foraminiferal photosynthetic response. Ecotoxicological studies on the interaction of climate change with additional stressors, such as pesticide exposure, indicate a prevalence of synergistic interactions across different organisms (Holmstrup et al 2010;Kohler and Triebskorn 2013).…”

“…Elevated temperatures and eutrophication can also have interactive negative effects on growth and survivorship in Marginopora vertebralis . Negative effects of elevated temperatures are more severe in the presence of low concentrations of the herbicide Diuron (van Dam et al 2012).…”

Combined effects of temperature and the herbicide diuron on Photosystem II activity of the tropical seagrass Halophila ovalis

“…This has application in plant growth models that build predictions based on multiple environmental conditions, and for the interpretation of routine seagrass health monitoring where both temperature and diuron exposure are known. Previously the effects of diuron and thermal stress has been shown to cause additive effects on in symbiotic corals41 and their isolated symbionts71 and in foraminifera55. Although outcomes for PSII activity in seagrass was also worse for combinations of temperature stress and herbicide exposure, the sub-additivity reported here may reflect a greater flexibility in PSII function across a wider thermal range as seagrasses are generally considered far more tolerant of thermal stress than corals and foraminifera72.…”

“…As a result, sub-optimal temperatures (both low and high) may cause reduced binding efficiency of diuron and thus change sensitivity to PSII herbicides, explaining the reduced IC 50 s at 20 °C and 40 °C. From another perspective, the presence of diuron (or other PSII herbicides) is likely to narrow the optimal temperature range for seagrass, resulting in stress responses at lower maximum temperatures, as reported for corals and foraminifera545571. Throughout the GBR lagoon and catchment area seasonally high sea surface temperatures coincide with the monsoonal flood plume events and the highest herbicide concentrations are detected near seagrass habitats under these conditions33.…”

“…Since both stressors act on the processes and/or integrity of PSII (see above), their combined effects can be assessed using chlorophyll fluorescence techniques. Recent studies which applied PAM fluorometry have demonstrated that the presence of PSII herbicides increases the vulnerability of tropical symbiotic organisms such as corals54 and foraminifera55 to thermal stress. However, tropical seagrasses are more likely to be exposed to herbicides in coastal runoff than coral reefs33, and so far there have been no studies examining the combined effects or potential interactions of thermal stress and herbicides on seagrass physiology and health.…”