Interactive effects of climate change and eutrophication on the dinoflagellate-bearing benthic foraminifer Marginopora vertebralis

Abstract

Elevated sea surface temperatures caused by global climate change and increased nutrient concentrations resulting from land runoff both are stressors for calcifying coral reef organisms. Here, we test the hypothesis that increased temperature leads to bleaching in dinoflagellate-bearing foraminifera similar to corals and that increased nutrients through runoff can exaggerate stress on the holobiont. In an experiment manipulating temperatures alone, we have shown that mortality of Marginopora vertebralis increased with temperatures. Most individuals died after 7 days at 34°C, *5°C above current summer maxima. Survival at 37 days was [98% at 28°C. After 7 days of exposure to 31 or 32°C, photosynthesis of the endosymbionts was compromised, as indicated by several photophysiological parameters (effective quantum yield and apparent photosynthetic rate). In a flow-though experiment manipulating both temperature (three levels, 26, 29 and 31°C) and nitrate concentrations (3 levels, *0.5, 1.0 and 1.4 lmol l -1 NO 3 -), elevated temperature had a significant negative effect on most parameters measured. At 31°C, most photopigments (measured by UPLC) in the foraminifera were significantly reduced. The only pigment that increased was the photoprotective diatoxanthin. Several other parameters measured (maximum and effective quantum yield, O 2 production in light, organic carbon contents) also significantly decreased with temperature. Optode-based respirometry demonstrated that the presence of symbionts at elevated temperatures represents a net carbon loss for the host. Growth rates of M. vertebralis and mortality at the end of the experiment were significantly affected by both temperature increase and nitrate addition. We conclude that these foraminifera bleach in a similar fashion to corals and that global sea surface temperature change and nitrate increases are stressors for these protists. Furthermore, this provides support for the hypothesis that management of local stressors elevates resilience of coral reefs to global stressors.

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

“…Photosynthesis, respiration, and chlorophyll a content Elevated levels of temperature had a significant effect on all photosynthetic parameters, which is consistent with results of previous studies of temperature-induced bleaching in benthic Foraminifera Uthicke et al 2011). Temperatures above 30°C appear to lead to damage on the protein level in the holobiont and reduce carbon fixation rates of the symbionts due to reduced expression of the RuBisCO enzyme (Doo et al 2012).…”

“…For the increased pCO 2 treatment, water chemistry was manipulated by bubbling analytical CO 2 into the header tanks. The water chemistry was controlled by a computer aquarium system (Aquamedic, Germany), as described in Uthicke et al (2011) and Vogel and Uthicke (2012). Water samples for total alkalinity (A T ) and dissolved inorganic carbon (DIC) determinations were taken weekly and analysed by AIMS Laboratory Services (Vindta 3C).…”

“…Experimental approach mimicking 'natural' conditions Specimens were kept inside custom made flow-through housings in each aquarium to achieve higher flow conditions more closely mimicking their habitat than in previous experiments Uthicke et al 2011;Vogel and Uthicke 2012). Flow-through housings contained two levels made from two standard 6-well cellculturing plates with flow-through lids (Electronic Supplementary Material, ESM Fig.…”

“…PAM fluorometry results for M. vertebralis indicated a maximum saturating irradiance (E k ) between 100 and 140 lmol photons m -2 s -1 and for H. depressa between 40 and 60 lmol photons m -2 s -1 (Ziegler and Uthicke 2011). The light levels used in the experiment were chosen to fall below the E k values by Ziegler and Uthicke (2011) and P-I curve P max values determined by Vogel and Uthicke (2012) and were selected to correspond to levels which have shown no changes in mortality rates or chlorophyll a concentrations in previous experimental manipulations of the studied species Uthicke et al 2011;Vogel and Uthicke 2012;Reymond et al 2013). H. depressa was put in the lower level (10-17 lmol photons m -2 s -1 ) of the flow-through housings and M. vertebralis in the top level (38-45 lmol photons m -2 s -1 ) because the latter has a higher E k point, compared with the diatom-bearing species (Ziegler and Uthicke 2011).…”

“…The endosymbiosis is sensitive to thermal and light stress, leading to bleaching analogous to that in corals (Hallock et al 1992;Hallock and Talge 1993). The effect of thermal stress in Foraminifera has been documented in laboratory studies (Talge and Hallock 2003;Uthicke et al 2011). In the field, thermal pollution was documented to effect foraminiferal species composition (Arieli et al 2011).…”