Patterns of spread of coral disease in the Florida Keys

Reefs in the Florida Keys are experiencing a dramatic increase in the number of localities and number of species with coral disease. In extensive surveys from Key Largo to Key West in 160 stations at 40 randomly chosen sites, there has been a dramatic increase in (1) the number of locations exhibiting disease (82% of all stations are now affected, a 404% increase over 1996 values), (2) the number of species affected (85% of all species are now affected, a 218% increase over 1996 values), and (3) the rate of coral mortality (the deep fore-reef at Carysfort experienced a 60% reduction of living coral cover during the survey). Two null hypotheses (1) that the incidence of disease has remained constant through time and (2) that the apparent increase in disease is due to a lack of comparable earlier data, are both falsified. Different diseases exhibit different patterns of spread: some diseases (e.g. black band) exhibit low incidence and jump rapidly between sites; other diseases (e.g. white pox) exhibit patchy distributions and increase in frequency at affected sites from one year to the next. The central question of why so many corals are becoming simultaneously susceptible to a host of marine pathogens remains unanswered.     

Century‐scale records of coral growth rates indicate that local stressors reduce coral thermal tolerance threshold

Coral bleaching, during which corals lose their symbiotic dinoflagellates, appears to be increasing in frequency and geographic extent, and is typically associated with abnormally high water temperatures and solar irradiance. A key question in coral reef ecology is whether local stressors reduce the coral thermal tolerance threshold, leading to increased bleaching incidence. Using tree‐ring techniques, we produced master chronologies of growth rates in the dominant reef builder, massive Montastraea faveolata corals, over the past 75–150 years from the Mesoamerican Reef. Our records indicate that the 1998 mass bleaching event was unprecedented in the past century, despite evidence that water temperatures and solar irradiance in the region were as high or higher mid‐century than in more recent decades. We tested the influence on coral extension rate from the interactive effects of human populations and thermal stress, calculated here with degree‐heating‐months (DHM). We find that when the effects of chronic local stressors, represented by human population, are taken into account, recent reductions in extension rate are better explained than when DHM is used as the sole predictor. Therefore, the occurrence of mass bleaching on the Mesoamerican reef in 1998 appears to stem from reduced thermal tolerance due to the synergistic impacts of chronic local stressors.     

Turbid reefs moderate coral bleaching under climate‐related temperature stress

Thermal‐stress events that cause coral bleaching and mortality have recently increased in frequency and severity. Yet few studies have explored conditions that moderate coral bleaching. Given that high light and high ocean temperature together cause coral bleaching, we explore whether corals at turbid localities, with reduced light, are less likely to bleach during thermal‐stress events than corals at other localities. We analyzed coral bleaching, temperature, and turbidity data from 3,694 sites worldwide with a Bayesian model and found that K_d490, a measurement positively related to turbidity, between 0.080 and 0.127 reduced coral bleaching during thermal‐stress events. Approximately 12% of the world's reefs exist within this “moderating turbidity” range, and 30% of reefs that have moderating turbidity are in the Coral Triangle. We suggest that these turbid nearshore environments may provide some refuge through climate change, but these reefs will need high conservation status to sustain them close to dense human populations.     

Cellular reactions to sedimentation and temperature stress in the Caribbean coral Montastraea cavernosa

We present evidence of cellular responses to increased sedimentation and temperature in Montastraea cavernosa collected off Broward County, Florida. We sampled corals from six different sites approximately, 500-1000 m off shore, 10-15m depth. Six samples were collected from four sites adjacent to areas of underwater marine dredging (project sites), while the remaining two samples were obtained far away from the influence of the marine dredging (control sites). SSTs around collection time ranged 0.6-0.9 degrees C over the 40-year monthly mean. All specimens collected at project sites exhibited histopathological evidence of mild to moderate sedimentation stress including changes in size and number of mucocytes in epidermis and gastrodermis, attenuation of the epidermal and gastrodermal tissues, presence of cellular debris, and changes in number of zooxanthellae. These findings corroborate results of laboratory-based, sand-application experiments. In addition to the above-noted changes, one specimen exhibited multiple lesions consisting of unusual gastrodermal detachment with infiltration of amoebocytes into the adjacent mesoglea. Tissues surrounding detachment injuries exhibited marked to severe cellular changes. Accumulations of amoebocytes at lesion sites are seldom observed in wild corals. This response may be part of an organized reaction to injury and infection, as has been documented in sea anemones and gorgonians; however, further research is needed on the nature and role(s) of the scleractinian amoebocytes.     

Species‐specific responses to climate change and community composition determine future calcification rates of Florida Keys reefs

Anthropogenic climate change compromises reef growth as a result of increasing temperatures and ocean acidification. Scleractinian corals vary in their sensitivity to these variables, suggesting species composition will influence how reef communities respond to future climate change. Because data are lacking for many species, most studies that model future reef growth rely on uniform scleractinian calcification sensitivities to temperature and ocean acidification. To address this knowledge gap, calcification of twelve common and understudied Caribbean coral species was measured for two months under crossed temperatures (27, 30.3 °C) and CO₂ partial pressures (pCO₂) (400, 900, 1300 μatm). Mixed‐effects models of calcification for each species were then used to project community‐level scleractinian calcification using Florida Keys reef composition data and IPCC AR5 ensemble climate model data. Three of the four most abundant species, Orbicella faveolata, Montastraea cavernosa, and Porites astreoides, had negative calcification responses to both elevated temperature and pCO₂. In the business‐as‐usual CO₂ emissions scenario, reefs with high abundances of these species had projected end‐of‐century declines in scleractinian calcification of >50% relative to present‐day rates. Siderastrea siderea, the other most common species, was insensitive to both temperature and pCO₂ within the levels tested here. Reefs dominated by this species had the most stable end‐of‐century growth. Under more optimistic scenarios of reduced CO₂ emissions, calcification rates throughout the Florida Keys declined <20% by 2100. Under the most extreme emissions scenario, projected declines were highly variable among reefs, ranging 10–100%. Without considering bleaching, reef growth will likely decline on most reefs, especially where resistant species like S. siderea are not already dominant. This study demonstrates how species composition influences reef community responses to climate change and how reduced CO₂ emissions can limit future declines in reef calcification.     

Responses of coral‐associated bacterial communities to heat stress differ with Symbiodinium type on the same coral host

This study compared the effect of heat stress on coral‐associated bacterial communities among juveniles of the coral, Acropora tenuis, hosting different Symbiodinium types. In comparison to a control temperature treatment (28 °C), we documented dramatic changes in bacterial associates on juvenile corals harbouring ITS 1 type D Symbiodinium when placed in a high (32 °C) temperature treatment. In particular, there was a marked increase in the number of retrieved Vibrio affiliated sequences, which coincided with a 44% decline in the photochemical efficiency of the D‐juveniles. Interestingly, these Vibrio sequences affiliated most closely with the coral pathogen, Vibrio coralliilyticus, which has been implicated in some coral disease outbreaks. In contrast, A. tenuis hosting ITS 1 type C1 Symbiodinium did not exhibit major bacterial shifts in the elevated temperature treatment, indicating a more stable bacterial community during thermal stress; concomitantly a decline (10%) in photochemical efficiency was minimal for this group. D juveniles that had been exposed to moderately elevated sea temperatures (30 °C) in the field before being placed in the control temperature treatment displayed a decrease in the number of Vibrio affiliated sequences and bacterial profiles shifted to become more similar to profiles of corals harbouring type C1 Symbiodinium. In combination, these results demonstrate that thermal stress can result in shifts in coral‐associated bacterial communities, which may lead to deteriorating coral health. The lower resilience of A. tenuis to thermal stress when harbouring Symbiodinium D highlights the importance of inter‐kingdom interactions among the coral host, dinoflagellate endosymbiont and bacterial associates for coral health and resilience.     

Environmental controls on the global distribution of shallow‐water coral reefs

Aim Elucidating the environmental limits of coral reefs is central to projecting future impacts of climate change on these ecosystems and their global distribution. Recent developments in species distribution modelling (SDM) and the availability of comprehensive global environmental datasets have provided an opportunity to reassess the environmental factors that control the distribution of coral reefs at the global scale as well as to compare the performance of different SDM techniques. Location Shallow waters world‐wide. Methods The SDM methods used were maximum entropy (Maxent) and two presence/absence methods: classification and regression trees (CART) and boosted regression trees (BRT). The predictive variables considered included sea surface temperature (SST), salinity, aragonite saturation state (Ω_Arag), nutrients, irradiance, water transparency, dust, current speed and intensity of cyclone activity. For many variables both mean and SD were considered, and at weekly, monthly and annually averaged time‐scales. All were transformed to a global 1° × 1° grid to generate coral reef probability maps for comparison with known locations. Model performance was compared in terms of receiver operating characteristic (ROC) curves and area under the curve (AUC) scores. Potential geographical bias was explored via misclassification maps of false positive and negative errors on test data. Results Boosted regression trees consistently outperformed other methods, although Maxent also performed acceptably. The dominant environmental predictors were the temperature variables (annual mean SST, and monthly and weekly minimum SST), followed by, and with their relative importance differing between regions, nutrients, light availability and Ω_Arag. No systematic bias in SDM performance was found between major coral provinces, but false negatives were more likely for cells containing ‘marginal’ non‐reef‐forming coral communities, e.g. Bermuda. Main conclusions Agreement between BRT and Maxent models gives predictive confidence for exploring the environmental limits of coral reef ecosystems at a spatial scale relevant to global climate models (c. 1° × 1°). Although SST‐related variables dominate the coral reef distribution models, contributions from nutrients, Ω_Arag and light availability were critical in developing models of reef presence in regions such as the Bahamas, South Pacific and Coral Triangle. The steep response in SST‐driven probabilities at low temperatures indicates that latitudinal expansion of coral reef habitat is very sensitive to global warming.     

Differential survival of nursery‐reared Acropora cervicornis outplants along the Florida reef tract

In recent decades, the Florida reef tract has lost over 95% of its coral cover. Although isolated coral assemblages persist, coral restoration programs are attempting to recover local coral populations. Listed as threatened under the Endangered Species Act, Acropora cervicornis is the most widely targeted coral species for restoration in Florida. Yet strategies are still maturing to enhance the survival of nursery‐reared outplants of A. cervicornis colonies on natural reefs. This study examined the survival of 22,634 A. cervicornis colonies raised in nurseries along the Florida reef tract and outplanted to six reef habitats in seven geographical subregions between 2012 and 2018. A Cox proportional hazards regression was used within a Bayesian framework to examine the effects of seven variables: (1) coral‐colony size at outplanting, (2) coral‐colony attachment method, (3) genotypic diversity of outplanted A. cervicornis clusters, (4) reef habitat, (5) geographical subregion, (6) latitude, and (7) the year of monitoring. The best models included coral‐colony size at outplanting, reef habitat, geographical subregion, and the year of monitoring. Survival was highest when colonies were larger than 15 cm (total linear extension), when outplanted to back‐reef and fore‐reef habitats, and when outplanted in Biscayne Bay and Broward–Miami subregions, in the higher latitudes of the Florida reef tract. This study points to several variables that influence the survival of outplanted A. cervicornis colonies and highlights a need to refine restoration strategies to help restore their population along the Florida reef tract.     

Optimizing return‐on‐effort for coral nursery and outplanting practices to aid restoration of the Great Barrier Reef

Coral nursery and outplanting practices have grown in popularity worldwide for targeted restoration of degraded “high value” reef sites, and recovery of threatened taxa. Success of these practices is commonly gauged from coral propagule growth and survival, which fundamentally determines the return‐on‐effort (RRE) critical to the cost‐effectiveness and viability of restoration programs. In many cases, RRE has been optimized from past successes and failures, which therefore presents a major challenge for locations such as the Great Barrier Reef (GBR) where no local history of restoration exists to guide best practice. In establishing the first multi‐taxa coral nursery on the GBR (Opal Reef, February 2018), we constructed a novel scoring criterion from concurrent measurements of growth and survivorship to guide our relative RRE, including nursery propagule numbers (stock density). We initially retrieved RRE scores from a database of global restoration efforts to date (n = 246; 52 studies) to evaluate whether and how success commonly varied among coral taxa. We then retrieved RRE scores for Opal Reef using initial growth and survivorship data for six key coral taxa, to demonstrate that RRE scores were high for all taxa predominantly via high survivorship over winter. Repeated RRE scoring in summer is therefore needed to capture the full dynamic range of success where seasonal factors regulating growth versus survivorship differ. We discuss how RRE scoring can be easily adopted across restoration practices globally to standardize and benchmark success, but also as a tool to aid decision‐making in optimizing future propagation (and outplanting) efforts.     

Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.     

Antimicrobial and stress responses to increased temperature and bacterial pathogen challenge in the holobiont of a reef‐building coral

Global increases in coral disease prevalence have been linked to ocean warming through changes in coral‐associated bacterial communities, pathogen virulence and immune system function. However, the interactive effects of temperature and pathogens on the coral holobiont are poorly understood. Here, we assessed three compartments of the holobiont (host, Symbiodinium and bacterial community) of the coral Montipora aequituberculata challenged with the pathogen Vibrio coralliilyticus and the commensal bacterium Oceanospirillales sp. under ambient (27°C) and elevated (29.5 and 32°C) seawater temperatures. Few visual signs of bleaching and disease development were apparent in any of the treatments, but responses were detected in the holobiont compartments. V. coralliilyticus acted synergistically and negatively impacted the photochemical efficiency of Symbiodinium at 32°C, while Oceanospirillales had no significant effect on photosynthetic efficiency. The coral, however, exhibited a minor response to the bacterial challenges, with the response towards V. coralliilyticus being significantly more pronounced, and involving the prophenoloxidase‐activating system and multiple immune system‐related genes. Elevated seawater temperatures did not induce shifts in the coral‐associated bacterial community, but caused significant gene expression modulation in both Symbiodinium and the coral host. While Symbiodinium exhibited an antiviral response and upregulated stress response genes, M. aequituberculata showed regulation of genes involved in stress and innate immune response processes, including immune and cytokine receptor signalling, the complement system, immune cell activation and phagocytosis, as well as molecular chaperones. These observations show that M. aequituberculata is capable of maintaining a stable bacterial community under elevated seawater temperatures and thereby contributes to preventing disease development.     

Interactive effects of acclimation temperature and short‐term stress exposure on resistance traits in the butterfly Bicyclus anynana

The ability to buffer detrimental effects of environmental stress on fitness is of great ecological importance because, in nature, pronounced environmental variation may regularly induce stress. Furthermore, several stressors may interact in a synergistic manner. In the present study, plastic responses in cold, heat and starvation resistance are investigated in the tropical butterfly Bicyclus anynana Butler, 1879, using a full factorial design with two acclimation temperatures (20 and 27 °C) and four short‐term stress treatments (control, cold, heat, starvation). Warm‐acclimated butterflies are more heat‐ but less cold‐tolerant as expected. Short‐term cold and starvation exposure reduce cold and heat resistance, and short‐term heat exposure decreases cold but increases heat resistance. Starvation resistance is not affected by any of the short‐term treatments. Thus, the effects of short‐term stress exposure are either neutral or negative, except for a positive effect of heat exposure on heat resistance, indicating the negative effects of pre‐exposure to stress. Interestingly, significant interactions between acclimation temperature and short‐term stress exposure for heat and cold resistance are found, demonstrating that larger temperature differences incur more damage. Therefore, animals may not generally be able to benefit from pre‐exposure to stress (through ‘hardening’), depending on their previously experienced conditions. The complex interactions between environmental variation, stress and resistance are highlighted, warranting further investigations.     

Dissecting the nonlinear response of maize yield to high temperature stress with model‐data integration

Evidence suggests that global maize yield declines with a warming climate, particularly with extreme heat events. However, the degree to which important maize processes such as biomass growth rate, growing season length (GSL) and grain formation are impacted by an increase in temperature is uncertain. Such knowledge is necessary to understand yield responses and develop crop adaptation strategies under warmer climate. Here crop models, satellite observations, survey, and field data were integrated to investigate how high temperature stress influences maize yield in the U.S. Midwest. We showed that both observational evidence and crop model ensemble mean (MEM) suggests the nonlinear sensitivity in yield was driven by the intensified sensitivity of harvest index (HI), but MEM underestimated the warming effects through HI and overstated the effects through GSL. Further analysis showed that the intensified sensitivity in HI mainly results from a greater sensitivity of yield to high temperature stress during the grain filling period, which explained more than half of the yield reduction. When warming effects were decomposed into direct heat stress and indirect water stress (WS), observational data suggest that yield is more reduced by direct heat stress (?4.6 ± 1.0%/°C) than by WS (?1.7 ± 0.65%/°C), whereas MEM gives opposite results. This discrepancy implies that yield reduction by heat stress is underestimated, whereas the yield benefit of increasing atmospheric CO₂ might be overestimated in crop models, because elevated CO₂ brings yield benefit through water conservation effect but produces limited benefit over heat stress. Our analysis through integrating data and crop models suggests that future adaptation strategies should be targeted at the heat stress during grain formation and changes in agricultural management need to be better accounted for to adequately estimate the effects of heat stress.     

Subcellular dynamics of proteins and metabolites under abiotic stress reveal deferred response of the Arabidopsis thaliana hexokinase‐1 mutant gin2‐1 to high light

Stress responses in plants imply spatio‐temporal changes in enzymes and metabolites, including subcellular compartment‐specific re‐allocation processes triggered by sudden changes in environmental parameters. To investigate interactions of primary metabolism with abiotic stress, the gin2‐1 mutant, defective in the sugar sensor hexokinase 1 (HXK1) was compared with its wildtype Landsberg erecta (Ler) based on time resolved, compartment‐specific metabolome and proteome data obtained over a full diurnal cycle. The high light sensitive gin2‐1 mutant was substantially delayed in subcellular re‐distribution of metabolites upon stress, and this correlated with a massive reduction in proteins belonging to the ATP producing electron transport chain under high light, while fewer changes occurred in the cold. In the wildtype, compounds specifically protecting individual compartments could be identified, e.g., maltose and raffinose in plastids, myo‐inositol in mitochondria, but gin2‐1 failed to recruit these substances to the respective compartments, or responded only slowly to high irradiance. No such delay was obtained in the cold. At the whole cell level, concentrations of the amino acids, glycine and serine, provided strong evidence for an important role of the photorespiratory pathway during stress exposure, and different subcellular allocation of serine may contribute to the slow growth of the gin2‐1 mutant under high irradiance.     

Impact of short‐term exposure to low subzero temperatures on egg hatch in the hemlock looper,Lambdina fiscellaria

The frequency of extreme events, such as cold spells, is expected to increase under global warming. Therefore, the ability of insects to survive rapid changes in temperature is an important aspect to investigate in current population ecology. The hemlock looper (HL), Lambdina fiscellaria (Guenée) (Lepidoptera: Geometridae), a defoliator of boreal balsam fir forests in eastern Canada, overwinters at the egg stage on tree trunks and branches where eggs can be exposed to very low subzero air temperatures. Using eggs from the island of Newfoundland (NL) and Quebec mainland (QC), we undertook field and laboratory experiments to determine: (1) their supercooling point (SCP) in mid‐January and mid‐February; (2) overwintering mortality; (3) cold tolerance to various combinations of subzero temperatures (?25, ?30, ?33, ?35, or ?37 °C) and exposure durations (2, 4, 8, 12, or 16 h); and (4) potential causes of death at subzero temperatures above the SCP. Regardless of population or sampling date, eggs supercooled on average at ?40.1 °C. In the field, 59% of eggs from either population that overwintered in Sainte‐Foy (QC) and Corner Brook (NL) hatched successfully, whereas none did in Armagh (QC) or Epaule (QC). In the laboratory, 50% of eggs survived after 4 h at ?34.4 °C or after 14 h at ?32.9 °C. In contrast, regardless of exposure duration, >50% of eggs hatched at temperatures ≥?33 °C, but <50% did so at ≤?35 °C, suggesting high pre‐freeze mortality. However, when eggs were attached to thermocouples and exposed to temperatures ranging from ?25 to ?37 °C for 16 h, 69% froze at temperatures of ?35 to ?37 °C, but only 2% did at ?25 or ?30 °C. Time to freeze decreased as subzero temperatures declined, and this was more evident in island eggs than in mainland eggs. Overall, eggs can freeze after a brief exposure to subzero temperatures higher than the standard SCP, and are thus highly vulnerable to cold spells.     

Seed germination responses to seasonal temperature and drought stress are species‐specific but not related to seed size in a desert steppe: Implications for effect of climate change on community structure

Investigating how seed germination of multiple species in an ecosystem responds to environmental conditions is crucial for understanding the mechanisms for community structure and biodiversity maintenance. However, knowledge of seed germination response of species to environmental conditions is still scarce at the community level. We hypothesized that responses of seed germination to environmental conditions differ among species at the community level, and that germination response is not correlated with seed size. To test this hypothesis, we determined the response of seed germination of 20 common species in the Siziwang Desert Steppe, China, to seasonal temperature regimes (representing April, May, June, and July) and drought stress (0, ?0.003, ?0.027, ?0.155, and ?0.87 MPa). Seed germination percentage increased with increasing temperature regime, but Allium ramosum, Allium tenuissimum, Artemisia annua, Artemisia mongolica, Artemisia scoparia, Artemisia sieversiana, Bassia dasyphylla, Kochia prastrata, and Neopallasia pectinata germinated to >60% in the lowest temperature regime (April). Germination decreased with increasing water stress, but Allium ramosum, Artemisia annua, Artemisia scoparia, Bassia dasyphylla, Heteropappus altaicus, Kochia prastrata, Neopallasia pectinata, and Potentilla tanacetifolia germinated to near 60% at ?0.87 MPa. Among these eight species, germination of six was tolerant to both temperature and water stress. Mean germination percentage in the four temperature regimes and the five water potentials was not significantly correlated with seed mass or seed area, which were highly correlated. Our results suggest that the species‐specific germination responses to environmental conditions are important in structuring the desert steppe community and have implications for predicting community structure under climate change. Thus, the predicted warmer and dryer climate will favor germination of drought‐tolerant species, resulting in altered proportions of germinants of different species and subsequently change in community composition of the desert steppe.     

Photosynthetic responses to photosynthetically active radiation and temperature including chilling‐light stress on the heteromorphic life history stages of a brown alga,Cladosiphon okamuranus (Chordariaceae) from Ryukyu Islands,Japan

Photosynthetic responses to temperature and photosynthetically active radiation (PAR) were investigated on the heteromorphic life history stages (macroscopic and microscopic stages) of an edible Japanese brown alga, Cladosiphon okamuranus from the Ryukyu Islands. Measurements were carried out by using optical dissolved oxygen sensors and a pulse‐amplitude modulated fluorometer. Maximum net photosynthetic rates and other parameters of the Photosynthesis – PAR curves at 28°C were somewhat similar in both life history stages, without characteristic photoinhibition at 1000 μmol photons m^?2 s^?1. Results of oxygenic gross photosynthesis and dark respiration experiments over a temperature range of 8–40°C revealed similar temperature optima for both stages (29.7°C, macroscopic stage; 30.3°C, microscopic stage), which support their observed occurrences in the habitat during summer. Maximum quantum yields of photosystem II (PSII ) (F _v /F _m ) were relatively stable at low temperatures with the highest at 15.1°C for the macroscopic stage and at 16.5°C for the microscopic stage; but dropped at higher temperatures especially above 28°C. Continuous exposures (6 h) to 200 and 1000 μmol photons m^?2 s^?1 at 8, 16, and 28°C revealed greater depressions in effective quantum yields of PSII (Φ _PSII ) of the microscopic stage at 8°C, as well as its F _v /F _m that barely increased after 6 h of dark acclimation. Whereas post‐dark acclimation F _v /F _m of both stages exposed to low PAR fairly recovered at 28°C, suggesting their photosynthetic tolerance to such high temperature. Under natural conditions, both heteromorphic stages of C. okamuranus may persist throughout the year in this region. Beyond its northern limit of distribution, the microscopic stage of this species may suffer from photodamage, as enhanced by low winter temperatures; hence, its restricted occurrence.