In situ measured seasonal variations in Fv/Fm of two common Red Sea corals
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- Winters, G., Loya, Y. & Beer, S. Coral Reefs (2006) 25: 593. doi:10.1007/s00338-006-0144-3
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Pulse amplitude modulated (PAM) fluorometry has been suggested as a tool for estimating environmental stresses on corals. However, information regarding natural changes in maximal quantum yields (Fv/Fm) of corals during “normal” (i.e. non-bleaching) years has been limited. In this study, seasonal variations in Fv/Fm for Stylophora pistillata and Favia favus, measured in situ, correlated with seasonal changes in solar irradiance but not in sea temperature. Interactions between sea temperature and irradiance were further studied by growing these corals and Pocillopora damicornis under controlled conditions. Exposure to high light with normal or high temperatures resulted in lower Fv/Fm values than exposure to low light at both temperatures. Thus, high irradiances may cause decreased Fv/Fm values in corals at least as much as, if not more than, high temperatures. Such seasonal variations should be taken into account when using PAM fluorometry as a diagnostic tool for predicting coral bleaching.
KeywordsPAM fluorometryMaximal quantum yield (Fv/Fm)Coral monitoringCoral bleachingIrradianceRed Sea
The development of the submersible pulse amplitude modulated (PAM) fluorometer, the Diving-PAM, has provided a quick and non-intrusive means for in situ measurements of photosynthetic parameters of the algal symbionts (zooxanthellae) harboured within corals (Beer et al. 1998; Ralph et al. 1999), and the effects of environmental stressors on them (Jones et al. 1999; Okamoto et al. 2005). One of the parameters in such measurements is the maximal quantum yield of electron transport through photosystem II (Fv/Fm); compared to “normal” values, a stressful change in many environmental conditions has been shown to reduce Fv/Fm values, indicating a lowered photosynthetic capacity. Indeed, thermally induced coral bleaching has been reported to correlate not only with a decrease in zooxanthella density and/or pigment content (Brown et al. 1995; Brown 1997), but also with declining Fv/Fm values (Warner et al. 1999; Jones et al. 2000; Okamoto et al. 2005). Because of this, and because such reduced Fv/Fm values were in some cases also shown to precede visible signs of bleaching (Lesser and Gorbunov 2001; Warner et al. 2002), PAM fluorometry has the potential of being incorporated into coral health monitoring programs. However, Warner et al. (2002) showed that Fv/Fm values for Caribbean Montastraea spp. also varied seasonally in non-bleaching years between winter highs (ca. 0.7) and summer lows (ca. 0.5). Furthermore, low summer values of 0.48 coincided with a bleaching event while only slightly higher summer values (0.52) did not. Thus, while it seems that Fv/Fm values can be related to bleaching events, it also appears that the seasonal variation in Fv/Fm must be taken into consideration when trying to evaluate coral bleaching using this method.
The objective of this study was to examine the driving force behind seasonal variations in Fv/Fm in common Red Sea corals. Fv/Fm was measured in situ over a long time period (1.5 years), and compared with simultaneous measurements of irradiance and seawater temperature. In addition, separate and combined effects of light and seawater temperature were examined in a controlled environment experiment.
Materials and methods
Colonies of Stylophora pistillata (n = 5) were collected at 5 m depth from the reef outside the Inter-University Institute (IUI) in Eilat, Israel (Gulf of Aqaba, Northern Red Sea, 29°30′N, 34°55′E). The maximum tidal range at this location is approximately 0.8 m (http://www.isramar.ocean.org.il/TideElat). Each colony was broken into 3–5 cm branches, which were mounted on plastic holders with non-toxic glue (AquaMend, USA), and then placed back into the sea at depths of 5, 10 and 20 m. Small, 4–6 cm diameter, colonies of the massive coral Favia favus were also collected from 5 m depth at the same site, mounted in the same way and returned to depths of 5 and 20 m (n = 6 at each depth). All corals were left for 2 months in the sea before measurements began.
Fv/Fm was measured monthly between January 2004 and July 2005 using a Diving-PAM (Walz, Germany). All measurements were performed in situ, while SCUBA diving, 1 h after sunset in order to maximize the frequency of open photosystem II reaction centres (cf. Winters et al. 2003). The PAM fluorometer’s fibre-optical probe was kept at a fixed distance (1.5 cm) and angle (70°) from each sample using a specially built plastic holder. A repeated measures ANOVA was used for both species to test the effect of sampling date on Fv/Fm. The three depths were included as a second factor in a two-way ANOVA. Multiple regression analysis (Statistica 6.0, Statsoft, USA) was used to account for the combined effects of irradiance and seawater temperature. Significant differences were assessed at P < 0.05.
Irradiance (global solar radiation, above the sea surface at the IUI pier) and seawater temperature (at 5 m depth, adjacent to the corals) were measured continuously using a CM 21 Pyranometer (310–2,800 nm, Kipp and Zonen, Holland) and a HOBO Pro data logger (Onset Computers, USA), respectively.
The separate and combined effects of light and temperature were also investigated in a controlled environment experiment by exposing corals pre-adapted to high or low light to normal or increased temperatures. Four branches from five colonies of S. pistillata and Pocillopora damicornis were collected from 5 m depth, together with 20 colonies of 3–5 cm diameter F. favus. These were mounted in the way described above and allowed to recover on an outdoor water table (1 × 3 × 0.1 m), half of which was covered by a black net providing 90% shade (“low light”, LL; midday irradiance 200–300 μmol photons m−2 s−1) and half covered by another black net providing 30% shade (“high light”, HL; midday irradiance 900–1,000 μmmol photons m−2 s−1). Irradiance under the two nets was measured separately using LI-190 2π quantum sensors connected to a LI-1400 data logger (Li-Cor, USA). Following a 2-month photoacclimation period, the water table was further divided into two sections using foam barriers: A normal (low) temperature (LT) section averaging 24.3°C (± 0.16 SE) and a high temperature (HT) section. Water within the HT section was heated 1°C per week, to 31°C, resulting in a final temperature of 31.3°C ± 0.03 SE (monitored using a HOBO temperature logger). This temperature was 3°C higher than maximal summer water temperatures in the Gulf of Aqaba. Following 3 weeks of exposure to the HT, measurements of Fv/Fm were performed daily 1 h after sunset for all corals. No visual signs of bleaching were apparent at that time. A two-way ANOVA was used for comparison of Fv/Fm values of corals growing under the different light and temperature regimes. Significant differences were assessed at P < 0.05.
Results and discussion
For both coral species measured, within all depths, sampling date had a significant effect on Fv/Fm. Highest values were obtained during the winter (November 2004) and the lowest during summer (June–July 2005) (Fig. 1b, c). Coral fragments growing at 20 m depth always showed significantly higher Fv/Fm values than those growing at shallower depths. However, for S. pistillata, no significant differences were found between fragments growing at 5 and 10 m. No significant interaction was observed between sampling date and depth for either species (Fig. 1b, c). These seasonal cyclic variations in Fv/Fm are similar to those found by Warner et al. (2002) for two Caribbean Montastraea spp. growing at 1–14 m. Thus, low Fv/Fm values in the summer and high values in the winter may be common in corals of various types and from various geographic locations.
Coefficient of determination (r2) for monthly average Fv/Fm values compared to the diurnal maximal global radiation (maximum radiation) or to the monthly averages of diel maximum seawater temperature (maximum temperature) for Stylophora pistillata (n = 5) and Favia favus (n = 6) growing at various depths
r2 of Fv/Fm and maximum radiation
r2 of Fv/Fm and maximum temperature
Adjusted r2 of Fv/Fm with both maximum radiation and temperature
High values of Fv/Fm in the winter may reflect the ability of zooxanthellae to optimize light harvesting during low-light periods (due to both fewer hours of daylight and reduced maximal irradiance), while reduced Fv/Fm values measured in the summer months could reflect photoinhibition during high irradiance periods (Winters et al. 2003). High-light stress has also previously been shown to reduce Fv/Fm values in corals. Brown et al. (1999) showed that a midday depression in Fv/Fm values measured for Goniastrea aspera coincided with maximal insolation, and concluded this to represent dynamic photoinhibition. A depression in Fv/Fm in shallow as compared to deeper growing corals has been shown in Montastraea spp. (Lesser and Gorbunov 2001; Warner et al. 2002) and S. pistillata (Winters et al. 2003), the latter attributed to chronic photoinhibition in the shallow growing colonies. The present results also show that such differences between deep and shallow growing corals are consistent throughout the seasons. The summer decline in Fv/Fm did not lead to bleaching in S. pistillata and F. favus; very little bleaching is observed in the northern Red Sea. However, as bleaching events are also related to reduced Fv/Fm values (Warner et al. 1999; Jones et al. 2000; Okamoto et al. 2005), the present results highlight the importance of high irradiance (in addition to temperature) as contributing to possible coral bleaching events (as was also shown in the study of Brown et al. 1994). This conclusion is further confirmed by the experimental work where corals were grown at high and low light and normal and high temperatures; for three species, exposure to HL but normal temperatures resulted in a significant decrease of Fv/Fm values compared to corals exposed to LL but increased water temperatures. While the data from this experiment were collected prior to any signs of bleaching, the S. pistillata and P. damicornis fragments in the LL and HL ended up severely bleached after 4 weeks at the HT. No such bleaching was found for F. favus colonies within the same treatments after 6 weeks (after which the experiment was terminated). Hence, a differential response to stress was found between the species. The finding in this study that bleaching of S. pistillata and P. damicornis branches in the HT and HL treatments began after the decline in Fv/Fm values demonstrates, again, the ability of the Diving-PAM to detect stresses which would lead to bleaching prior to any visual signs.
While Fv/Fm has become one of the most commonly used parameters for the study of plant stress, including stress in coral photosymbionts, it also has a potential to be misused. For example, Okamoto et al. (2005) measured Fv/Fm of corals growing at depths of 2–15 m before a bleaching event during November 2000, and compared the values to measurements taken during the bleaching event of August 2001. Because Fv/Fm values from corals at different depths were pooled together and measurements from different seasons were compared, it is difficult to assess what part of the reduction in Fv/Fm was due to the seasonal change and what part was indeed due to bleaching. Incorporating base line data, e.g. the changes in Fv/Fm values that corals experience during non-bleaching years, such as demonstrated in this study, may allow the background signal due to normal seasonal changes in coral physiology to be distinguished from true early signs of bleaching.
Funding from the Rufford Foundation for Nature Conservation and PADI Foundation to GW, and from the Israel Science Foundation and the Raynor Chair for Environmental Conservation Research to YL, is greatly acknowledged.