Alkenone Production Research Articles

Controls on the molecular distribution and carbon isotopic composition of alkenones in certain haptophyte algae

Although the biochemical functions and biosynthetic pathways of alkenones are still largely unknown, alkenone unsaturation ratios are now used extensively to infer ancient sea surface temperature, and their isotopic compositions have been used to reconstruct ancient atmospheric CO2levels. The inferred relationships between alkenone unsaturation ratios, isotopic compositions, and growth conditions are based on empirical laboratory and field studies and, in the case of isotope fractionation, on simple models of carbon acquisition and fixation. Significant uncertainty still exists concerning the physiological and ecological factors affecting cellular production of alkenones, unsaturation ratios, and isotopic composition. Phytoplankton culture conditions have been shown to affect alkenone unsaturation (U37K′), cellular alkenone content, intracellular isotopic compositions (Δδ), and changes in fractionation (εP) as a function of the quotient of algal growth rate and aqueous carbon dioxide concentration (μ/CO2). Such studies imply that plant physiology can affect the interpretation of environmental signals. The factor(s) controlling cellular alkenone concentrations and unsaturation ratios are reviewed, as well as the carbon isotopic composition of the alkenone‐producing algae. A new technique is presented to determine growth rates of the alkenone‐containing algae in natural settings that will facilitate testing laboratory‐based hypotheses concerning the carbon isotopic fractionation and its relationship to growth rate/growth status of alkenone‐producing algae in the field.

Temperature dependency of long-chain alkenone distributions in recent to fossil limnic sediments and in lake waters

Distribution patterns of C 37 and C 38 polyunsaturated long-chain alkenones (LCAs) serve as proxies for the determination of paleotemperatures for marine surface waters. We studied Recent/Subrecent and Late Glacial/Holocene sediments from Germany, Austria, Russia, and the U.S. to test for a correspondence between LCA distribution and surface water temperature in limnic systems. Previously, reports of LCA occurrence were restricted to sediments of 6 wide distributed freshwater and alkaline lakes. In this study 13 of 27 investigated lakes contained LCAs in surface sediments with concentrations varying between 12 to 205 μg/g TOC. Late Glacial to Holocene sediment sequences from Lake Steisslingen and Lake Wummsee, (Germany), Lake Pichozero (Russia), and Brush Lake (U.S.A.) contained abundant LCAs with averaged concentrations of 33 to 7536 μg/g TOC. For the first time we observed the occurrence of LCAs within in the water column of oligotrophic Lake Stechlin (NE-Germany). Alkenones were restricted to the zone of maximum chlorophyll concentration within the water column indicating that LCAs have a biosynthetic origin and can be attributed to phototrophic (micro)algae. Attempts to identify the producing organism, however, were not successful. Culture experiments allow various phytoplankton to be excluded as producers. Alkenone-producing algae are evidently of small size, hindering microscopical identification. LCAs commonly occur in high concentrations in Late Glacial sediments, mainly during the cold period of the Younger Dryas, whereas the Holocene usually is devoid of polyunsaturated alkenones. The episodic occurrence of LCAs restricts their utility as proxies for continuous geological records. Furthermore, lack of microscopical verification and the episodic distribution allow for different producers of unsaturated alkenones in Recent and Late Glacial sediments. An empirical relationship between LCA distribution and temperature was observed. In fossil sediments from Lake Steisslingen, there is a good correspondence between Uk37 and the temperature-controlled δ 18O isotope ratio of lake chalk. Comparison of LCA patterns obtained from the uppermost centimetres of lake sediments with averaged summer surface water temperatures of the lakes studied, demonstrates a trend of covariance ( r 2: Uk′37 = 0.90, Uk37 = 0.67; n = 9). Hence, the same mechanism that causes temperature-dependence of LCA patterns in marine systems might be effective in limnic settings. Identification of alkenone producers and their culture under controlled temperature are still mandatory before LCAs can be routinely applied as paleotemperature proxy in limnic systems.

Primary signal: Ecological and environmental factors—Report from Working Group 2

Alkenone‐based proxies are routinely used for paleoceanographic and climatologic reconstructions despite the fact that their calibration to environmental parameters is still a matter of debate. Significant differences are observed among culture calibrations using different strains of alkenone producers, between regional field calibrations within the euphotic zone, and between water column‐ and core top‐based calibrations. The reasons for these discrepancies are not well understood and call for further evaluation. The possibility is raised that several aspects of genetics, physiology, and ecology of alkenone‐producing haptophytes may be responsible, and suggestions of future research are proposed.

Alkenones and particulate fluxes in sediment traps from the central equatorial Pacific

We investigated a year-long (September 1992 to August 1993) time series of total mass, calcium carbonate, organic carbon, opal, and alkenone fluxes in sinking particles collected with sediment traps moored at 1770 and 4220 m in the central equatorial Pacific. The total mass fluxes varied from 14.7 to 68.7 mg/m 2/day at 1770 m, with greater fluxes in October–November and February–April, and from 14.6 to 50.4 mg/m 2/day with peak fluxes during October–November at 4220 m. High flux in the spring season shown at 1770 m was not indicated at 4220 m; instead, a slight increase was shown during a broad period from March to June. The calcium carbonate fluxes varied from 10.8 to 49.1 mg/m 2/day with higher fluxes in October–November and March–April at 1770 m, and from 8.9 to 37.0 mg/m 2/day with a higher flux in October–November at 4220 m. The organic carbon fluxes varied from 0.36 to 5.91 mg/m 2/day, with higher fluxes in October–November and March–April at 1770 m, and from 0.72 to 2.58 mg/m 2/day at 4220 m. The annual mean organic carbon flux was 1.84 and 1.28 mg/m 2/day at 1770 and at 4220 m, respectively. These values were less than half of those reported for the EqPac sediment trap experiment. The opal fluxes varied from 0.55 to 4.4 mg/m 2/day at 1770 m and from 1.23 to 2.95 mg/m 2/day at 4220 m. Alkenone fluxes varied significantly from 0.05 to 0.84 μg/m 2/day, with high values in November, February–March, and June at 1770 m. For the 4220 m trap, these values ranged from 0.05 to 0.25 μg/m 2/day, with slightly higher fluxes in April–May and June–July, which followed periods of high alkenone fluxes observed in February–April and June–July, respectively, at 1770 m depth. These values were remarkably low compared with those reported by the previous studies at other sites. U 37 K′ values were constantly high >0.95 throughout the collection period. However, relatively low U 37 K′ values (0.92 and 0.93) were occasionally observed during February to March. Estimated alkenone temperatures from those U 37 K′ values were about 27–29°C and consistent with the observed temperature of the upper layer at ca.100 m depth. The seasonal change of the U 37 K′ values could be affected by not only water temperature but also the relative amount of ‘warm’ and ‘cold’ types of alkenone producer in the central equatorial Pacific.

Production rates of C37 alkenones determined by 13C-labeling technique in the euphotic zone of Sagami Bay, Japan

The production rates of C37 alkenones in the euphotic zone of Sagami Bay, Japan were determined by the 13C-labeling technique in conjunction with gas chromatography–mass spectrometry. The maximum in the alkenone production rate (C37:2 plus C37:3 alkenones) was observed at 5 m depth and the specific production rate, calculated from the rate of production relative to standing stock in suspended particles, was 0.64 day−1 at this depth. Temperature, based on the newly-produced alkenone unsaturation index (Uk′37), was close to in situ temperatures at the depth where alkenones production was active.

Anomalously low alkenone temperatures caused by lateral particle and sediment transport in the Malvinas Current region, western Argentine Basin

We analysed the alkenone unsaturation ratio ( U K′ 37) in 87 surface sediment samples from the western South Atlantic (5°N–50°S) in order to evaluate its applicability as a paleotemperature tool for this part of the ocean. The measured U K′ 37 ratios were converted into temperature using the global core-top calibration of Müller et al. (1998) and compared with annual mean atlas sea-surface temperatures (SSTs) of overlying surface waters. The results reveal a close correspondence (<1.5°C) between atlas and alkenone temperatures for the Western Tropical Atlantic and the Brazil Current region north of 32°S, but deviating low alkenone temperatures by −2° to −6°C are found in the regions of the Brazil–Malvinas Confluence (35–39°S) and the Malvinas Current (41–48°S). From the oceanographic evidence these low U K′ 37 values cannot be explained by preferential alkenone production below the mixed layer or during the cold season. Higher nutrient availability and algal growth rates are also unlikely causes. Instead, our results imply that lateral displacement of suspended particles and sediments, caused by strong surface and bottom currents, benthic storms, and downslope processes is responsible for the deviating U K′ 37 temperatures. In this way, particles and sediments carrying a cold water U K′ 37 signal of coastal or southern origin are transported northward and offshore into areas with warmer surface waters. In the northern Argentine Basin the depth between displaced and unaffected sediments appears to coincide with the boundary between the northward flowing Lower Circumpolar Deep Water (LCDW) and the southward flowing North Atlantic Deep Water (NADW) at about 4000 m.

Ecological and environmental factors affecting alkenone distributions in seawater and sediments

The use of alkenones to estimate past sea surface temperatures has gained wide acceptance, but there are still some issues that need to be resolved before alkenone proxies can be used confidently in all environmental settings. A particular concern is defining what seawater temperature is recorded by the alkenone distributions preserved in sediments. Does it, for example, reflect a seasonal average or a snapshot of bloom conditions or some other combination of environmental effects? This paper reviews some of the environmental and ecological factors that might affect alkenone distributions and, in particular, the influence of depth and seasonality on alkenone production in the water column.

Biomarker stratigraphic records over the last 150 kyears off the NW African coast at 25°N

Terrigenous and marine biomarkers were investigated in a core off Northwest Africa in the Northeast Atlantic (25°N, 16°W, 1445 m depth) to assess changes in the sedimentation pattern of organic carbon (OC) over the last 150 kyears. Alkenone derived temperatures recorded a warming of 4.5°C during the last deglaciation. n-Alkanol Mass Accumulation Rates (MAR) fluctuated in parallel with Northeast Trade Winds (NETW) intensity. OC and sterol MAR both increased during glacial times indicating enhanced fertility of the ocean in response to intensified NETW. Alkenone/OC ratios were higher by a factor of two over stages 4–6 than stages 1–3 thus reflecting distinct coccolithophorid inputs. This transition coincides with a major change of alkenone producers inferred from coccolith counts.

Long-chain alkenone patterns in the Baltic sea—an ocean-freshwater transition

Two different patterns of long-chain alkenones are found in surficial sediments of the Baltic Sea, which is the largest brackish water body on Earth. One pattern occurs in surficial sediments from the Western Baltic Sea where surface-water salinitiy is in excess of 7.7 PSU. It corresponds to the pattern produced by the marine coccolithophorid Emiliania huxleyi with a suite of C 37 di- to tetra-unsaturated methyl ketones and C 38 di- and tri-unsaturated methyl and ethyl ketones. A second pattern, resembling that found in lake sediments in lacking C 38 methyl ketones and having distinctly higher C 37:4 methyl ketone concentrations, dominates in surficial sediments of the eastern and northern Baltic Sea, where salinities are lower than 7.7 PSU. Correspondence of sea-surface temperature (SST) estimates from the U 37 K and U 37 K′ indices (using marine calibrations) with mean SST in the euphotic zone from July-August (the main haptophyte growth season) is poor. Thus, these indices are not applicable as sedimentary thermometers in surficial sediments of the Baltic Sea. The different patterns may either reflect the salinity-dependent occurrence of specific alkenone producers or changes in the alkenone biosynthesis due to physiological stress caused by salinity variations. Furthermore, advection of saline and oxygenated North Sea water may transport marine algal material characterized by a marine E. huxleyi-like alkenone pattern into the western Baltic Sea, thus covering the signature of the local alkenone producers with a Baltic Sea pattern.

Depth ranges of alkenone production in the central Pacific Ocean

We report analytical results of long‐chain (C37−C39) alkenones in the surface sediments taken along a latitudinal transect at 175°E from 48°N to 15°S. Unsaturation degree of C37 alkenones (Uk′37) indicated that alkenone temperature is the highest (about 28.3°C) in the tropical Pacific and decreases toward 48°N (about 10.1°C). Although the latitudinal trend of the alkenone temperature is generally similar to that of the observed sea surface temperature of the surface mixed layer, the former exhibits markedly lower values than the latter does in the midlatitude (35°−19°N). On the basis of the comparisons between water column temperatures and alkenone temperatures in the surface sediments, we estimated that in the midlatitudes alkenones are produced in the thermocline waters, whereas in the high (48°−40°N) and low (10°N−2°S) latitudes they are produced in the surface mixed layer. This result is supported by the depth distribution of Emiliania huxleyi and Gephyrocapsa oceanica along a 155°W transect in the central Pacific. The latitudinal distribution of the alkenone production layers estimated from UK′37 is found to be consistent with that of the nitrate, suggesting that the depth of alkenone production is mainly controlled by the nutrient supply from deeper waters. Alkenones in the sediments exhibited relatively large abundances in 43°−27°N with a maximum at 30°N, which may be explained by high productivity of haptophyte algae in Kuroshio Extension.

Depth and seasonality of alkenone production along the California Margin inferred from a core top transect

Alkenone unsaturation indices (Uk'37) of marine sediment could prove particularly useful on organic‐rich continental margins where carbonate dissolution hampers the use of other paleoclimatic proxies [McCaffrey et al., 1990; Kennedy and Brassell, 1992]. Forty core top samples of Recent sediment from a latitudinal transect (23°–40°N) along the California margin yield Uk'37 values that correlate linearly with modern mean annual sea surface temperatures (SSTs) in the range of 12°–23°C. Reproducibility of the unsaturation value in closely spaced cores is near analytical error. Uk'37 data define a relationship to temperature nearly identical to the Prahl et al. [1988] laboratory cultures of Emiliania huxleyi. The close agreement is particularly significant in light of the nannofossil composition of the sediments, where the abundance of the coccolith taxon Gephyrocapsa oceanica (known to synthesize alkenones) equals or exceeds that of E. huxleyi. Comparison with seasonal temperature variations at different depths indicates that little if any alkenone production occurs at depths &gt;30 m along the continental margin (water depths &lt;2 km). Sediments in more pelagic locations exhibit small but consistent biases toward winter and/or subsurface production similar to previously reported sediment trap and core top data from the Oregon margin [ Prahl et al., 1993; Doose et al., 1997].

Calibration of the alkenone paleotemperature index U 37K′ based on core-tops from the eastern South Atlantic and the global ocean (60°N-60°S)

We have analysed alkenones in 149 surface sediments from the eastern South Atlantic in order to establish a sediment-based calibration of the U 37 K′ paleotemperature index. Our study covers the major tropical to subpolar production systems and sea-surface temperatures (SST’s) between 0° and 27°C. In order to define the most suitable calibration for this region, the U 37 K′ values were correlated to seasonal, annual, and production-weighted annual mean atlas temperatures and compared to previously published culture and core-top calibrations. The best linear correlation between U 37 K′ and SST was obtained using annual mean SST from 0 to 10 m water depth (U 37 K′ = 0.033 T + 0.069, r 2 = 0.981). Data scattering increased significantly using temperatures of waters deeper than 20 m, suggesting that U 37 K′ reflects mixed-layer SST and that alkenone production at thermocline depths was not high enough to significantly bias the mixed-layer signal. Regressions based on both production-weighted and on actual annual mean atlas SST were virtually identical, indicating that regional variations in the seasonality of primary production have no discernible effect on the U 37 K′ vs. SST relationship. Comparison with published core-top calibrations from other oceanic regions revealed a high degree of accordance. We, therefore, established a global core-top calibration using U 37 K′ data from 370 sites between 60°S and 60°N in the Atlantic, Indian, and Pacific Oceans and annual mean atlas SST (0–29°C) from 0 m water depth. The resulting relationship (U 37 K′ = 0.033 T + 0.044, r 2 = 958) is identical within error limits to the widely used E. huxleyi calibrations of Prahl and Wakeham (1987) and Prahl et al. (1988) attesting their general applicability. The observation that core-top calibrations extending over various biogeographical coccolithophorid zones are strongly linear and in better accordance than culture calibrations suggests that U 37 K′ is less species-dependent than is indicated by culture experiments. The results also suggest that variations in growth rate of algae and nutrient availability do not significantly affect the sedimentary record of U 37 K′ in open ocean environments.

Hydrocarbons, sterols and alkenones in sinking particles in the Indian Ocean sector of the Southern Ocean

Hydrocarbons, sterols and alkenones were analyzed in samples collected from a 10 month sediment trap time series deployed in the Indian Ocean sector of the Southern Ocean. Fluxes and within-class distributions varied seasonally. During higher mass and organic carbon (OC) flux periods, which occurred in austral summer and fall, fresh marine inputs were predominant. Vertical fluxes were most intense in January, but limited to one week in duration. They were, however, low compared with other oceanic regions. In contrast, low mass and OC flux periods were characterized by a strong unresolved complex mixture (UCM) in the hydrocarbon fraction and a high proportion of stanols as a result of zooplanktonic grazing. Terrigenous inputs were not detectable. The alkenone compositions were consistent with previous data on suspended particles from Antarctic waters. However, U 37 K′ values diverged from the linear and exponential fits established by Sikes, E. L. and Volkman, J. K. Calibration of alkenone unsaturation ratios (U 37 K′) for paleotemperature estimation in cold polar waters. Geochimica et Cosmochimica Acta, 1993, 57, 1883–1889], in the low temperature range. The seasonal pattern of alkenone production implied that IPT (integrated production temperature) is likely to be strongly imprinted by austral summer and fall SST (sea surface temperature).

Alkenones as Proxies of Sea Surface Temperatures: Seasonal Production of Alkenones in Guaymas, Carmen and Santa Barbara Basins

Use of molecular proxies in palaeoceanography began with the realization (Brassell et el., 1986) that the biosynthesis of unsaturation in alkenones (codified as U~7) by haptophyte algae is temperaturedependent and can survive in sediments to provide a record of sea-surface temperatures (SSTs). A combination of culture experiments, field collections and sediment analyses (e.g. Prahl et el., 1988; RosellMel6 et el., 1995) has established the veracity of U3K7 as a measure of SSTs and subsequent investigations have further confirmed, developed and calibrated the application of alkenones as palaeoclimatic indicators. They also prompt continuing efforts to examine and critically evaluate environmental controls on the timing and intensity of seasonal production of alkenones in the modern ocean and concurrent assessment of the transport of these alkenone SST records through the water column to the underlying sediments. Here, sediment trap studies help provide a critical link between the production of alkenones in surface waters and their sedimentary records that form the basis for molecular pa laeocl imat ic studies. Specifically, exploration of U3K7-temperature relationships in sediment trap particulates recovered during long-term, high-frequency, time series affords the opportunity to monitor seasonal changes in alkenone production and to determine the temporal character of the temperature signal recorded by the annual flux of alkenone sedimentation. The locations chosen in this study provide characteristics well-suited to addressing these goals. The Gulf of California (GoC) experiences a sharp seasonal contrast in SSTs as seasonal shifts in winds cause changes in surface water masses which produce an annual temperature range of >15~ The recent historical record of alkenones in the Santa Barbara basin (SBB) is well documented (e.g. Kennedy and Brassell, 1992) enabling direct comparison of current sedimentation with past events. Furthermore alkenoneBiogeochemical Laboratories, Department of Geological Sciences, Indiana University, Bloomington, IN 47405, USA

Production and transport of long-chain alkenones and alkyl alkenoates in a sea water column in the northwestern Pacific off central Japan

Abstract Sinking particles collected from year-long time-series sediment traps at 1674, 4180, 5687 and 8688 m depths, the underlying bottom sediment at 9200 m depth, and suspended particles from surface and subsurface waters in the northwestern North Pacific off Japan were analyzed for long-chain alkenones and alkyl alkenoates (A&A) which are derived mainly from Gephyrocapsacean algae, especially Emiliania huxleyi and Gephyrocapsa oceanica. Alkenone temperature records in sediment trap samples at 1674 m were almost similar to observed sea surface temperatures (SST) with a time delay of one half to one full month. However, alkenone temperatures in trap samples were about slightly lower than measured SST in late spring to early fall. The lowering might be caused by formation of the seasonal thermocline. Nevertheless, these temperature drops observed in trap samples were smaller than those actually observed in a subsurface layer off central Japan. Vertical profiles of A&A concentrations and alkenone temperatures in suspended particles collected from the subsurface waters in early fall indicated that these compounds were produced mostly in a surface mixed layer above the depth of the chlorophyll maximum even in warm seasons. These results suggested that alkenone temperatures strongly reflected SST rather than the temperatures of thermocline waters in these study areas even in such a warm season. Pronounced maxima in A&A fluxes found in sediment trap samples at 1674 m in late spring to summer showed that A&A productions were highest during the periods of spring bloom, according to a time delay between alkenone temperatures and observed SST. Seasonal patterns of alkenone records in trap samples at 4180 and 5687 m could also preserve SST signals well, suggesting that A&A in deep sea waters were mainly derived from primary products in the surface layer. A&A fluxes tended to decrease with water depth, and the ratios of A&A to particulate organic carbon (POC) rapidly decreased in underlying bottom sediment. This clearly indicates that A&A were decomposed and diluted by other refractory organic materials in either the water column or the sediment–water interface. However, A&A compositions were consistently uniform between the trap samples and the underlying bottom sediments, so that A&A could not qualitatively alter during early diagenetic processes.

Evaluation of long-chain alkenones as paleo-temperature indicators in the Mediterranean Sea

Long-chain alkenones were analyzed in samples collected from February to July 1989 by a time-series sediment trap located at 200 m depth in the northwestern Mediterranean Sea. The alkenone temperature signal was calibrated using water column particles collected at the sediment trap mooring site. The calibration ( U 37 K′ = 0.041 T−0.21, r 2 = 0.97, 13° C < T < 19° C), differed from the culture calibration of Prahl et al. (1988, Geochimica et Cosmochimica Acta, 52, 2303–2310) and the calibration for the eastern North Atlantic waters between 16°C and 25°C (Cenre and Eglinton, 1993, Deep-Sea Research 1, 40, 1935–1961). The slope of the calibration was, however, similar to the slope of the calibration established using all Pacific Ocean samples (Sikes and Volkman, 1993, Geochimica et Cosmochimica Acta, 57, 1883–1889). The correlation of U 38Me K and water temperature was also significant ( U 38 Me K =0.042 T−0.25, r 2=0.87). Sediment trap results revealed that the production of alkenones during high flux periods predominantly occurred in subsurface waters. This was further supported by the depth distribution of alkenones observed during the monthly cruises: C37 alkenone concentrations in the upper 100 m of the water column indicated a subsurface maximum at approximately 50 m depth in May, June and July, whereas in March and November alkenones were more abundant in the upper 50 m. These results emphasize that accurate reconstruction of SST in core-tops must take into account the seasonality and depth variations of alkenone production. An intercalibration exercise, conducted on Mediterranean and Norwegian Sea water samples, demonstrated that high resolution chromatographic methods are essential to obtain reliable values of U 37 K′ and avoid the overestimation of production temperatures, particularly for colder waters where alkyl alkenoates are abundant.

Production pattern of alkenones in the Mediterranean Sea

Time‐series of downward alkenone fluxes have been investigated at 200 m depth over a one year sediment trap experiment, in the Northwestern Mediterranean Sea. Alkenone flux maxima occurred in autumn and to a lesser extent in May, during the spring bloom. Temperature estimates calculated from the UK′37 index revealed that alkenone producers preferentially develop in subsurface waters (at about 50 m) in spring, whereas the autumn alkenone production occurred upper in the water column (around 30 m). Examination of the core‐top UK′37 index values at various sites of the Northwestern Mediterranean basin, suggested that the spring bloom period do not significantly imprint the temperatures recorded in the sediments. The sedimentary temperature estimates would rather reflect annually integrated SST, with a major influence of the autumnal post‐bloom development of the coccolithophores in the euphotic zone.

Long-chain alkenones and alkyl alkenoates as palaeotemperature indicators: their production, flux and early sedimentary diagenesis in the Eastern North Atlantic

The production and fate of long-chain alkenones and alkenoates was examined with regard to their use as palaeotemperature indicators. Alkenoate abundances were higher than previously reported for other regions and more strongly correlated with temperature than was alkenone unsaturation ( U 37 k ), suggesting biogeographical variability in alkenone and alkenoate production in surface waters. We define the AA 36 ratio to parameterize alkenoate abundance and present an empirical temperature calibration derived from our euphotic zone samples for use in the North Atlantic [ T = 17.35 − 25.12 ( U 37 k ) − 26.73 (AA 36 + 93.90 (U 37 k) (AA 36)]. Significant diagenetic losses of alkenones and alkenoates were found within the water column and near surface sediments. In spite of diagenetic losses, the temperature signal recorded by these compounds in the sediments remains largely unaltered, and corresponds to the euphotic zone water temperature during the springtime period of maximum coccolithophorid production and flux rather than the average annual sea surface temperature.