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Irradiance, Water Column O2, and Tide Drive Internal O2 Dynamics and Meristem H2S Detection in the Dominant Caribbean-Tropical Atlantic Seagrass, Thalassia testudinum

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Abstract

Water column hypoxia, low partial pressure of oxygen (pO2), and hydrogen sulfide (H2S) intrusion, a phytotoxin, are factors linked to global seagrass decline. While many lab experiments have examined these relationships, field studies are needed to elucidate complex drivers of internal pO2 in situ. Herein, we examined plant pO2 and H2S dynamics using microsensors in a dominant tropical seagrass Thalassia testudinum in Florida Bay, a subtropical estuary with recurrent seagrass die-off events. Based on 12 field deployments (48–72 h) across seasons, we show that T. testudinum has a high capacity for daytime leaf oxidation (42–53 kPa) that sustains oxic conditions in its tissues and supersaturates the water column with O2 (> 21 kPa). Although internal daytime O2 is rapidly consumed near sunset, daytime seagrass O2 production leads to supersaturation in the water column beyond sunset. This is an important feedback mechanism as high water column pO2 at night buffers against internal leaf hypoxia via diffusion. Even with high daytime irradiance, however, shoot meristems went anoxic/hypoxic (0.6 kPa) at night, indicating high plant and ecosystem O2 consumption. Hydrogen sulfide was only detected in the meristem when water column pO2 was close to anoxia (< 1 kPa) coincident with maximum water column temperatures (33 °C), an occurrence likely to increase with global warming. Our results support the hypothesis that meristem H2S intrusion in Florida Bay, and likely globally, is primarily driven by insufficient internal plant oxidation by the water column at night, even when high irradiance sustains supersaturation of tissue O2 during the day.

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Acknowledgements

We thank Zachary W. Fratto from Everglades National Park (ENP) for providing the ENP monitoring data from our site, Kasey McLeod for her support working in the field, and Unisense Inc. for their technical expertise and troubleshooting of microsensors. Two anonymous reviewers are thanked for improving the manuscript.

Funding

This work was supported by the South Florida Water Management District (#4500113844).

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Authors and Affiliations

  1. Biological Sciences Department, Aquatic Plant Ecology Lab, Florida Atlantic University, 777 Glades Rd, Boca Raton, FL, 33431, USA

    M. S. Koch & C. R. Johnson

  2. Department of Biology, University of Copenhagen, Universitetsparken 4, 3rd Floor, 2100, Copenhagen, Denmark

    O. Pedersen

  3. Coastal Ecosystems Division, South Florida Water Management District, West Palm Beach, FL, 33406, USA

    C. J. Madden

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  1. M. S. Koch
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Correspondence to M. S. Koch.

Additional information

Communicated by Melisa C. Wong.

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12237_2022_1064_MOESM1_ESM.docx

Supplementary file1: Table S1. The beginning and end dates of each microsensor field deployment and their ID numbers given in supplemental tables in the manuscript. The number of day/night replicates during each deployment are presented in parentheses.

Table S2. Seasonal daytime (sunrise-sunset) water column physiochemical parameters and irradiance (I) during 29 individual days of seasonal deployments within Thalassia testudinum meadows at the Johnson Key study site in Florida Bay. Average, minimum, and maximum daytime water column pO2 (kPa), temperature (oC), and salinity, and average and maximum canopy height irradiance (µmol photons m-2 s-1) and day length (DL) are presented. Data was collected every minute during deployments. Parameters were averaged by season (a) winter, (b) spring, (c) summer, (d) fall. Significant differences among season are denoted by superscript letters (ANOVA, post-hoc Tukey, p < 0.05). Parameter variance, minimum and maximum ranges for each date and the beginning and ending times of each record are presented. Deployment # in parentheses (Table S1). na = data not available.

Table S3. Nighttime seasonal water column physiochemical parameters and irradiance during 20 individual nights during seasonal deployments within Thalassia testudinum meadows at the Johnson Key study site in Florida Bay. Average, minimum and maximum nighttime water column pO2, temperature, and salinity are presented. Data was collected every minute during deployments. Significant differences among season denoted by superscript letters (P < 0.01 temperature; P < 0.05 salinity; P = 0.07 pO2 max). Parameter variance for each date and the beginning and ending times of each record are presented. Deployment # in parentheses (Table S1). na = data not available.

Table S4. Seasonal porewater (10-15 cm depth) salinity, pHpw, and total sulfide (ΣTSpw). Gaseous H2S was calculated based on total sulfide, temperature, salinity, and pH according to Millero (1986). Parameters were averaged by season (a) winter, (b) spring, (c) summer, (d) fall. Seasonal significance (p < 0.05) is denoted by superscript letters (ANOVA, post-hoc Tukey), Means ± SD (n = 5).

Fig. S1. The sequence of cues for meristem placement is described below and illustrated in this schematic of a meristem cross-section of Thalassia testudium from the Johnson Key site in Florida Bay. We observed a sequence of Δ pO2 as the microsensors were moved into the shoot meristem as follows: (1) the ambient water column pO2 is measured as the O2 sensor approached the meristem, (2) a rapid drop in pO2 was detected at the surface of the non-photosynthetic base of the outer leaf sheath, (3) an increase in pO2 was detected once inside the aerenchyma tissue of the outermost leaf sheath, (4) a drop in pO2 occurred as the sensor penetrated the inner leaf sheath, and (5) a pO2 above the water column was detected once inside the meristem tissue aerenchyma of the inner leaf sheath. Location of sensor placement in the meristem is shown in Fig. 2c.

Fig. S2. Linear (right column) and non-linear or bi-phasic (left column) leaf pO2 dynamics from sunrise to 11:00 am during full sun deployments (n = 8) across seasons: (a) November 7, 2018 (b) February 17, 2019, (c) November 19, 2019, (d) March 9th, 2019, (e) April 18, 2019 (f) June 22, 2019, (g) September 19, 2019, (h) November 20, 2019. See Table 2 for regression details.

Fig. S3. Leaf pO2 from maximum in the afternoon to sunset. Irradiance during this time is also shown and the lag of leaf pO2 decline in response to decreasing irradiance identified with a double arrow. The lag times and leaf Δ pO2 following the lag are presented in Table 4. Replicates include those with afternoon leaf pO2 dynamics through sunset (n = 10).

Fig. S4. Linear relationship between leaf and meristem partial pressure during the morning (sunrise to 11:00) for all seasons. The date on the figures is the day microsensor measurements were taken.

Fig. S5. Linear relationship between leaf and meristem partial pressure during the afternoon (14:00 to sunset) for all seasons. The date on the figures is the day microsensor measurements were taken.

Fig. S6. Rates of decline in leaf (dark line) and meristem (grey line) pO2 following sunset. Linear regressions and equations are shown on graphs from sunset to when internal pO2 reached hypoxia (1.5 kPa) or sunrise the following day. Further data on nighttime parameters are presented in Table 6.

Fig. S7. Nighttime leaf and meristem pO2 as a function of water column pO2 during replicates where both leaf and meristem microsensor data were available. Dates of replicates on shown on each graph. Linear regression lines, linear equations, and unity lines (dashed) are shown. Arrows indicate area of line where regression was determined. Regression information is presented in Table 7within manuscript.

Fig. S8. Nighttime leaf and meristem pO2 as a function of water column pO2 during each replicate where only leaf or meristem microsensor data were available. Leaf data are shown in black and in the two right panels, while the meristem data are in grey and on the left three panels. Dates of replicates are shown on each graph. Linear regression lines, linear equations, and unity lines (dashed) are shown. Regression information is presented in Table 7.

Fig. S9. Temperature (top) and dissolved oxygen (bottom) in 30 min intervals from May 1 to October 1, 2019 in the water column at the long-term hydrostation of Everglades National Park adjacent to Johnson Key (JK) within about 200 meters of our microsensor measurements within Thalassia testudinum meadows. Arrows depict the June 21-22, 2019 date where meadow surface waters, leaves and meristems were hypoxic and H2S intrusion was detected in the meristem. Note: the ENP JK water quality station does not support underlying dense seagrass and is close to the mangrove fringe of JK; thus, the absolute water quality values may differ from those measured within the seagrass canopy reported herein. (DOCX 4724 KB)

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Koch, M.S., Johnson, C.R., Madden, C.J. et al. Irradiance, Water Column O2, and Tide Drive Internal O2 Dynamics and Meristem H2S Detection in the Dominant Caribbean-Tropical Atlantic Seagrass, Thalassia testudinum. Estuaries and Coasts 45, 2543–2559 (2022). https://doi.org/10.1007/s12237-022-01064-y

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