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Journal of Paleolimnology 28: 129–145, 2002. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.
Lake Redó ecosystem response to an increasing warming in the Pyrenees during the twentieth century
MOLAR Mountain Lake Research
J. Catalan1,*, S. Pla1, M. Rieradevall1, M. Felip1, M. Ventura1, T. Buchaca1, L. Camarero1, A. Brancelj2, P.G. Appleby3, A. Lami4, J.A. Grytnes5, A. Agustí-Panareda6 & R. Thompson6 1 Department of Ecology, University of Barcelona, Diagonal 645, 08028 Barcelona, Spain (E-mail:
[email protected]) 2 Laboratory for Freshwater and Terrestrial Ecosystems Research, National Institute of Biology. Vecna pot 111. Ljubljana 1000, Slovenia 3 Department of Mathematical Sciences, University of Liverpool, P.O. Box 147, Liverpool L69 3BX, UK 4 CNR – Ist. Ital. Idrobiol, Largo Tonolli, 50, Verbania-Pallanza, Italy 5 Botanical Institute, University of Bergen, Allégaten 41, N-5007 Bergen, Norway 6 Department of Geology and Geophysics, University of Edinburgh, West Main Road, Edinburgh EH9 3JW, Scotland, UK *Present address: CEAB-CSIC, Accés Cala St. Francesc 14, 17300 Blanes, Spain Received 6 December 1999; accepted 9 January 2002
Key words: climate change, alpine lake, paleolimnology, lake sediments, fossil pigments, diatoms, cladocera, chironomids, chrysophytes, long-term lake dynamics Abstract The ecosystem response of Lake Redó (Central Pyrenees) to fluctuations in seasonal air temperature during the last two centuries was investigated by comparison of reconstructed air temperatures with the sediment record. Fine slicing allowed a resolution of 3–6 years according to the 210Pb dating, although it was still difficult to easily investigate the response to air temperature forcing, since extreme fluctuations in temperature occur on interannual timescales. However, the resolution was sufficient to show responses on decadal and century scales. An overall tendency to warming in mean annual temperature in the Central Pyrenees has been caused by summer and in particular by autumn increases. Many of the measured sediment variables apparently responded to these long term trends, but the significance of the relationships was highly conditioned by the structure of the data. The variables responding most on the finer time scales were the microfossils. For diatoms, chironomids and chrysophytes the main variability correlated to summer and to autumn temperatures. For two planktonic species, Fragilaria nanana and Cyclotella pseudostelligera, we found a link of their variability with temperature fluctuations in their growing months (September and October, respectively). This relationship appeared at a certain point during a general warming trend, indicating a threshold in the response. On the other hand, no significant changes in the dominant species could be linked to temperature, nor in any significant subgroup of the 180 diatom species present in the core. In contrast, for most chironomids (particularly Paratanytarsus austriacus, Heterotrissocladius marcidus and Micropsectra radialis) a negative relationship with summer temperature extended throughout the studied period. This response of the whole group gives chironomids a more robust role as indicators for recording temperature changes on long time-scales (e.g., through the Holocene) and for lake signal inter-comparison. Finally, our results indicated that, in all cases, there was a significant resilience to high frequency changes and hysteresis despite extreme fluctuations. Although we were dealing with organisms with one or many generations per year, their populations seemed to follow the decadal trends in air temperature. This is the ninth of 11 papers published in this special issue on the palaeolimnology of remote mountain lakes in Europe resulting from the MOLAR project funded by the European Union. The guest editor was Richard W. Battarbee.
130 Introduction Predicting the responses of whole ecosystems to global change is still quite problematic (Schindler et al., 1996). Remote ecosystems independent of direct human influence may provide some clues to the sort of responses that might be expected. Although lakes represent only a small part of the biosphere, they are particularly suitable for studying ecosystem responses to changing external forcing (Catalan & Fee, 1994). The life spans of most limnic organisms are short and thus respond rapidly. So the history of their dynamics and their neighbouring ecosystems are recorded in detail in their sediments (Anderson & Battarbee, 1994). For many lakes, fluctuations in the loadings of substances delivered to the lake are due to anthropogenic activities in the catchment. Thus responses to climate variability are often masked or cannot be untangled from responses to human perturbations. In contrast, lakes in remote areas, such as Arctic or high-mountain regions, provide unique opportunities to address climate response studies, although they are not completely isolated from long-range pollution transport. The potential to study climate-lake linkages at remote sites is usually limited by the scarcity of on-site meteorological data and long term lake ecosystem monitoring. To overcome these limitations, in the present study we combined three distinct approaches: (1) onsite air temperature reconstructions from long instrumental records of nearby stations; (2) multi-parameter sediment record analysis, and (3) short seasonal limnological studies. The Pyrenees have experienced a clear warming trend throughout the 20th century, which has accelerated during the last 25 years. In this paper we analyse how the Lake Redó ecosystem has reacted to this warming trend. We show that very specific responses of some species were more unambiguously related to air temperature changes than were biogeochemical or sedimentological signatures.
Study site Lake Redó (42° 38′ N 0° 46′ E) is located at 2,240 m a.s.l. in the Central Pyrenees. It is deep (maximum depth 73 m, mean depth 32 m) and relatively large for a high mountain lake (24 ha, representing 16% of the watershed area) (Figure 1). The catchment has an area of 149 ha, 25% consists of bare rock while the rest is covered by alpine meadows. The bedrock is gran-
odioritic and soils are umbric-leptosols with an average depth of 35 cm. The lake water is very dilute (mean conductivity, 11.5 µS cm–1), and slightly acidic (average pH, 6.3). The most abundant cation is Ca2+ (72 µeq l–1); HCO3– (46 µeq l–1) and SO42– (26 µeq l–1) are the dominant anions. The lake is oligotrophic: the average concentration of total phosphorus is 0.2 µmol l–1, and the soluble reactive fraction is generally lower than 0.01 µmol l–1. Among the nitrogen forms, NO3– is relatively high (11 µeq l–1) compared with dissolved organic nitrogen (4 µeq l–1) and NH4+ (1 µeq l–1). The ice-covered period lasts for about 6 months each year, from late December to mid June.
Methods Coring and sampling Three sediment cores were collected with a gravity corer in the deepest part of the lake in January, 1997. All three were about 30 cm in length. One was kept as a back-up, and the other two were extruded and sliced immediately in a hut at the lake shore. Core RCM1 was sliced at 3 mm intervals and subsampled for pigments and elemental analysis (C, N, S), cladocera, and chironomids. Core RCM2 was sliced at 1.5 mm for the first 6 cm and at 3 mm for the rest of the core. Subsamples were dedicated to particle size analyses, diatom, chrysophycean stomatocysts and dating with 210Pb. Loss on ignition (LOI) at 550 °C was carried out on the two cores and used for core correlation. Cylindrical sediment traps (110 cm long, 9 cm φ), following the suggestions of Bloesch and Burns (1980) and Blomqvist and Håkanson (1981), were suspended at depths of 10, 25 and 58 m in the central part of the lake. They were emptied every month from February 1997 to April 1998. Subsamples (200 ml) were preserved in formaldehyde at 4% in plastic bottles for diatom and chrysophycean stomatocyst analysis. Water column samples were taken once a month at 9 m intervals from July 1996 to July 1998 using Ruttner bottles. Subsamples were used for chemical, pigment and phytoplankton analysis. During the sampling period, an automatic weather station was running on shore measuring air temperature, wind, humidity, radiation and precipitation. A thermistor chain recorded temperature in the lake at ten depths in order to determine the lake dynamics. Details of the analytical methods are given in Wathne (1997) and data are described in detail in Ventura et al. (2000) and Catalan et al. (2002, this
131
Figure 1. Location, catchment and bathymetric map of Lake Redó (Central Pyrenees). Coring and water sampling point, biological transect and on-site lake study facilities locations are indicated.
issue). Seasonal samplings were carried out on benthic macroinvertebrates and diatoms along the ice-free seasons, complemented with a SCUBA sampling transect from the upper littoral zone to 20 m deep on July 15, 1997. Sampling procedures and detailed results of these studies can be found in Rieradevall et al. (in press). The present paper is mainly based on the core studies and air temperatures, the rest of data are used only when relevant for the interpretation of the sediment record. Core dating Core RCM2 samples were analysed for 210Pb, 226Ra, and 137 Cs by direct gamma assay in the Liverpool University Environmental Radioactivity Laboratory, using Ortec HPGe GWL series well-type coaxial low background intrinsic germanium detectors (Appleby et al.,
1986). 210Pb was determined via its gamma emissions at 46.5 keV, and 226Ra by the 295 and 352 keV γ-rays emitted by its daughter isotope 214Pb following 3 weeks storage in sealed containers to allow radioactive equilibration. 137Cs was measured by its emissions at 662 keV. The absolute efficiencies of the detectors were determined using calibrated sources and sediment samples of known activity. Corrections were made for the effect of self absorption of low energy γ-rays within the sample (Appleby et al., 1992). Radiometric dates were calculated using either the CRS and CIC 210Pb dating models (Appleby & Oldfield, 1978) following an assessment as to which model was most appropriate following the procedures described in Appleby and Oldfield (1983), Appleby et al. (1991), Appleby (1993, 1998). Core RCM1 chronology was established by sequence slotting technique (Thompson & Clark, 1993) using LOI for correlating with the master core RCM2.
132 Bulk sediment analyses Particle size measurements on wet sediment were carried out using a laser particle analyser; in this paper we use two descriptors namely weight percentage corresponding to particles smaller than 63 µm (p < 63); and the mean particle volume in that range size (PMV). Elemental C, N and S from the organic fraction were analysed by means of a NCS analyser FISONS NA 1500. Pigments were extracted using the method described in Lami et al. (1994). Total chlorophylls and their derivatives; and total carotenoids were estimated spectrophotometrically. Single carotenoid and chlorophylic compounds were measured by HPLC (Lami et al., 1994). Diatoms and chrysophycean stomatocysts All samples were treated with H2O2 (33%) and mounted in Naphrax (R.I. = 1.7) following the method of Battarbee (1986). Diatoms and chrysophycean cyst concentrations in the samples were estimated by addition of a known number of latex microspheres to a known weight of dried sediment (Battarbee & Kneen, 1982). Diatoms were counted under oil immersion at 1200× using phase contrast, and cysts under interference contrast at the same magnification. A minimum of 500 diatom valves and 250 cysts were counted from each slide. Scanning electron microscopy was used to determine chrysophycean cysts; we followed Duff et al. (1995) when possible and new cysts were coded according to Pla (2001). Diatom cells with and without chloroplasts, as indicators of alive and dead cells, respectively, were evaluated from 100 ml sub-samples from sediment traps at 640× in an inverted microscope following the Utermöhl method (Sournia, 1987). Water column phytoplankton samples were counted using the same method. Chironomids and cladocera To obtain the remains of the chironomid head capsules, the sediment was sieved through a 100 µm screen after deflocculation with hot 10% KOH for 15 min. The head capsules were hand sorted from a Bolgorov tray with forceps under the magnification of a stereoscopic microscope. They were then mounted on slides in Euparal media, after dehydratation with 70% absolute ethanol. For species identification, we followed Wiederholm (1983) and Schmid (1993). Looking for higher taxonomical resolution, we reared larvae collected in the lake during the ice-free season in 1996 and 1997. Rear-
ings were carried out in constant temperature rooms at 18 °C with fourth instar larvae, pre-pupae and pupae whenever possible. After pigment extraction, the same sediment sub-samples were used for cladocera analysis following a similar deflocculation procedure as for chironomids; slides were prepared according to Frey (1986). At least 200 remains were counted per sample. Only chydorid species were considered in this study. Air temperature reconstructions and data analysis Data from meteorological stations close to Lake Redó cover just a few decades. Therefore, the reconstruction of air temperature in Lake Redó was carried out based on the long Pic du Midi (Bigorre) (43.07 N, 0.15 W, 2862 m.a.s.l.) temperature series, which was taken as representative for the Central Pyrenees. The effect of different altitude between the lake and the station was corrected using a temperature lapse rate obtained by spatial interpolation of radiosonde air temperature data from 1990–1997, taking into account monthly variability (–5.24, –5.13, –5.38, –5.82, –5.72, –5.84, –5.65, –5.82, –5.48, –5.27, –5.41, –5.19 °C km–1 from January–December, respectively). In order to complete the series from 1781–1997 a stepwise multiple regression was used to establish linear transfer functions of temperatures between the Pic du Midi series and twentyone long lowland records from across Europe. Twelve transfer functions were obtained, one for each calendar month. The skill of these transfer functions was assessed to range between 40–99%. The low skill values generally corresponded to the winter months. The procedure is described in detail by Agustí-Panareda and Thompson (2002, this issue). The resulting temperature retrodictions were validated using the data recorded by the automatic weather station installed at the shore of the lake for the period 1996–1997. Typical retrodiction errors were estimated to range from 1–2 °C for individual low-sun months and 0.5–1 °C for individual high-sun months. Decadal average temperature estimates would be expected to be root ten times better than for the single months.
Results and discussion The warming trend and their seasonal patterns in the Pyrenees during the 19th and 20th centuries The retrodicted monthly mean air temperatures were averaged to yield the annual mean air temperature at
133 Lake Redó (Figure 2). The main feature was that the frequency of the oscillations between warm and cold years was very high, except for the last 25 years. To better visualise fluctuations at different time scales, several degrees of smoothing were carried out. A locally weighted regression smoothing (LOESS) with several different values for span was used (Cleveland et al., 1993). The lower the span (e.g., 0.05), the less the smoothing and the closer the smoothed line followed the original data points; whereas the higher the span (e.g., 0.5) the more the long term patterns of change in air temperature were emphasised. This latter smoothing showed the contrasting trends of the 19th and 20th centuries. From 1781 to around 1840, there was a tendency to a slight cooling (ca. 0.2 °C), whereas thereafter there was a tendency to warming which continues to the present. A less severe smoothing (span 0.05) showed the fluctuations superimposed on these main tendencies, indicating two particularly cool periods in the 1810’s and the 1970’s. The latter was embedded in the general warming trend of the 20th century and, as a consequence, produced the steepest warming period within the series, with an increase from the
1970’s to present of more than 3 °C in mean annual air temperature. The patterns of air temperature variation for the four seasons are quite different for the last two hundred years (Figure 3). The largest interannual variability occurred in autumn (September–November) and the lowest in summer (June–August). These two seasons both showed clear warming trends, the autumn being particularly strong. Spring (March–May) temperature showed a long-term flat pattern and winter (December– February) a slight cooling until the 1920’s and thereafter a slight warming. However, the softer smoothing showed how spring reflected better than any other season the cooling in the 1970’s. Summer and autumn had also some years of extremely low temperature, but not winter. Sediment dating Dating of the sediment record was required to establish how the lake ecosystem responded to the air temperature changes described above. Equilibrium of total 210 Pb activity with the supporting 226Ra was reached at
Figure 2. Mean annual air temperature at Lake Redó for the last two centuries and two examples of smoothing.
134
Figure 3. Temperature deviations from seasonal mean air temperatures at Lake Redó for the last two centuries. The seasonal temperature was calculated from reconstructed mean monthly values according to the following grouping: winter (December–February); spring (March–May); summer (June–August) and autumn (September–November). The lake is usually ice covered from late December to mid June.
a depth of about 9 cm in RCM2 (Figure 4). The unsupported 210Pb activity versus depth profile had two distinct parts, an upper zone (0–3 cm) with a shallow gradient and a number of minor irregularities, and a deeper zone (3–7 cm) with a steeper gradient in which unsupported 210 Pb activity declines more or less exponentially with depth. Between 7–9 cm there was a small irregularity that may record a 19th century disturbance. The 137Cs activity versus depth profile had a well defined but relatively poorly resolved peak. The maximum activity occurred at 1 cm depth, though the peak was skewed and high concentrations were recorded between 0.8–2.5 cm. Traces of 241Am recorded between 0.9–2.8 cm confirmed the presence of weapons fallout between these depths, but did not allow identification of the 1963 depth with any precision. It is possible that the peak at 1 cm recorded the 1986 Chernobyl accident. The 137Cs profile between 1–2.5 cm would then be due to a blurring of the Chernobyl and weapons fallout records. 210 Pb dates calculated using the CRS and CIC dat-
ing models are shown in Figure 4, together with the dated points suggested by the 137Cs record. The CRS model placed 1986 and 1963 at depths of 1 and 2.2 cm respectively, in good agreement with the conjecture of a Chernobyl origin for the 137Cs peak at 1 cm and a 1960’s origin for sediments just above 2.5 cm. In contrast, the 137Cs results invalidated the much higher sediment accumulation rates for the past few decades suggested by the CIC model. Therefore, dates provided by the CRS model were adopted as a chronology for the sediment record. Error limits were significantly higher for the 19th century period. The CRS model calculations indicated low accumulation rates throughout most of the past 170 years (0.004–0.008 g cm–2 yr–1) with episodes of more rapid sedimentation in the latter half of the 19th century, and again during the past 20 years. From 1837 (7.5 cm depth) backwards a constant accumulation rate (0.0038 g cm–2 yr–1) was assumed, increasing the dating uncertainty for this period.
135
Figure 4. Radiometric chronology at Lake Redó core RCM2 showing CRS and CIC model 210Pb dates together with dates determined from the 137Cs and 241Am stratigraphy. Sedimentation rates correspond to the CRS model.
Comparison of the air temperature fluctuations with the sediment record The core dating indicated an average sediment accumulation rate of about 0.5 mm yr–1, hence each sample corresponded to some 3–6 years of sediment accumulation, given the slicing thickness employed. As we have seen above, the fluctuations between extremely cold and extremely warm years occurred at periods shorter than the time resolution of our samples (Figures 2 & 3). Each sample potentially integrated responses of the ecosystem to very diverse, even completely opposed, weather conditions. This fact introduced a severe constraint for the comparison between air temperature fluctuations and the sediment record. However, even in the case of an annual resolution of the samples, such as is possible for varved sediments, we should not necessarily expect equivalent responses to equivalent weather fluctuations, since annual ecosystem dynamics depends not only on the actual annual forcing but also on the initial conditions, which depend on what happened in the previous year and indeed in several years before. Unfortunately, the magnitude of this historical dependence is unknown to us. Therefore, we decided to compare the sediment record with various temperature series formed from smoothers of different strength. The most severe smoothers provided the long
term tendency (e.g., LOESS span 0.5 in Figure 1), while softer smoothers progressively approached the inter-annual variability. However, it is not sensible to apply span values using time intervals shorter than the resolution of our samples. Since chrysophycean cysts were only analysed for each second sample, we used 0.05 as a lower limit for LOESS span, which gave a decadal time scale. The long-term warming tendency of the air temperature (Figure 2 & 3) provides an additional constraint in our comparisons. Any diagenetic process on-going in the upper sediment could be confused with a response to that warming. This risk was made quite evident with the high correlation that existed between air temperatures and the depth of the samples in the core, which was obviously not a variable responding to any forcing. To decrease this indeterminacy, we decided to compare the sediment record with the softest smoothing possible. The date of each sample at midpoint was used to interpolate the corresponding mean temperatures (annual, winter, spring, summer, autumn) using the LOESS smoothing with span 0.05. This was done for each core. The interpolated temperatures for comparison with the different response variable in the sediment record are shown in Figure 5. Linear regressions between the available response variables and temperature predictors were carried out.
136 The response variables were used without any smoothing or interpolation. They were taken as representative of the midpoint of the sample interval. For microfossils, the species were ordinated with a principal component analysis (PCA) of the square root transformation of the percentage data. The more relevant species contributing to first four axes of variability are indicated in Table 1. In Table 2, the fraction of the variance explained for the relationships analysed that were apparently significant are listed. However, their significance (p-values) must be interpreted with caution. In particular one single p-value should not be interpreted literally for several reasons. The samples are not independent, but are temporally autocorrelated (Legendre & Legendre, 1998). This serial or autocorrelation destroys the assumptions involved when the p-values are inferred and often leads to a higher correlation than if the samples were inde-
pendent. It could be possible to do some permutations with certain restrictions to give a better estimate of the p-values; but this would only partly avoid the problem with autocorrelation. As an alternative, we decided to use, instead of the usual 0.05, a lower p-value (0.02) as a significance threshold. On the other hand, the remaining restriction introduced by the fact that most pronounced temperature change occurred recently was illustrated by the correlation between sample depth and temperature (Table 2). Therefore, the statistical significance for each single variable has to be taken with caution, as an exploration of the potential link with climate. A conservative test of the relationship between response variables and the air temperature would be to accept only those response variables with higher correlations with air temperature than sample depth. Finding plausible interpretations in terms of the limnological processes and patterns occurring in lake Redó would also
Figure 5. Interpolated temperature data (LOESS span 0.05) corresponding to mid-sample dates in cores RCM2 and RCM1 plotted down core together with measured variables that showed a significant linear relationship with at least one of the seasonal time-series.
137 Table 1. Microfossils with high scores (> 0.6) on any of the principal components (PC) of group variability for the sediment record of Lake Redó (Central Pyrenees) in the last two centuries. Since the variance is scaled to 1, the axis eigenvalues indicate the proportion of variance explained PC1 Diatoms (180 taxa) Axes eigenvalue Cyclotella pseudostelligera Fragilaria nanana Achnanthes curtissima Aulacoseira distans nivalis Aulacoseira lirata Achnanthes sp. Achnanthes minutissima Navicula schassmannii Aulacoseira alpigena Chrysophytes (65 cysts) Axes eigenvalue S317C S239.339 S019 S091 S346 S005A S345 S320 S300 S034 S243 Chironomids (23 taxa) Axes eigenvalue Paratanytarsus austriacus Heterotrissocladius marcidus Micropsectra radialis Zavrelinyia sp. Corynoneura arctica Tanytarsus lugens - group Cladocera (5 species) Axes eigenvalue Alona affinis Eurycercus lamellatus Alona sp. Chydorus sphaericus Acroperus harpae
0.174 0.97 0.93 –0.22 –0.29 –0.14 –0.01 –0.28 –0.24 –0.08
0.169 –0.82 –0.74 0.74 0.64 0.64 0.10 –0.04 0.26 0.10 –0.31 0.27
0.347 –0.92 –0.76 –0.70 –0.66 –0.51 –0.15
0.416 –0.92 0.91 0.42 0.37 0.37
provide more arguments for trusting the statistical significance of our results. A few conclusions can already be derived from this statistical screening: (1) relationships between response variables and air temperature fluctuations were exclusively established through the ice-free season tempera-
PC2 0.091 0.06 0.07 –0.85 0.73 0.64 –0.63 –0.62 –0.36 0.13
0.125 –0.01 0.26 –0.05 0.17 0.19 –0.71 –0.67 0.60 –0.10 0.49 –0.06
0.120 –0.20 –0.30 0.59 –0.9 0.26 –0.46
0.252 0.12 0.33 –0.90 0.31 –0.21
PC3 0.044 –0.19 0.17 0.18 –0.16 0.30 0.07 –0.09 –0.63 0.60
0.087 0.14 0.23 0.25 0.09 0.07 –0.24 –0.45 –0.09 0.70 –0.62 0.60
0.108 –0.06 0.22 0.33 0.06 –0.73 0.17
0.189 –0.33 –0.25 –0.06 0.85 0.03
PC4 0.038 –0.06 0.11 –0.19 –0.08 –0.09 0.28 0.07 0.11 0.12
0.081 0.49 –0.23 0.15 –0.10 0.21 –0.14 –0.24 0.29 0.33 –0.32 –0.15
0.084 0.02 0.09 –0.16 0.26 0.23 –0.76
0.134 –0.01 –0.04 –0.11 –0.10 0.90
tures. As a consequence, there were no apparently detectable effects in the sediment record of the variations in the length of the ice cover; (2) there were more variables significantly responding to autumn temperature than to summer temperatures, and on average the variance explained by autumn temperatures was also sig-
138 Table 2. Fraction of variance for divers sediment variables which was explained by mean air temperature. The most significant results (pvalues ≤ 0.02) are shown in bold. Asterisks indicate variables where the fraction of variance explained is higher than by just sample depth
Particle mean volume Particle < 63 µm LOI Organic carbon Nitrogen Sulphur Total carotenoids Chlorophyll derivates Pigments PC2 Diatoms PC1 Diatom inferred- pH Chrysophytes PC1 Chironomids PC1 Cladocera PC4 Sample depth RCM1 Sample depth RCM2
Annual temperature (LOESS span 0.05) r2 p-value
Winter temperature (LOESS span 0.05) r2 p-value
Spring temperature (LOESS span 0.05) r2 p-value
Summer temperature (LOESS span 0.05) r2 p-value
Autumn temperature (LOESS span 0.05) r2 p-value
0.11 0.08 0.16 0.04 0.08 0.04 0.10 0.05 0.29* 0.32* 0.09 0.11 0.20 0.10 0.28 0.23
0.01 0.03 0.06 0.07 0.05 0.01 0.00 0.00 0.05 0.04 0.07 0.05 0.07 0.01 0.01 0.01
0.00 0.00 0.09 0.10 0.05 0.02 0.02 0.00 0.03 0.06 0.00 0.01 0.07 0.05 0.02 0.03
0.15 0.08 0.12 0.00 0.02 0.01 0.07 0.03 0.14 0.26* 0.14 0.05 0.19* 0.07 0.18 0.19
0.31 0.20 0.06 0.09 0.21 0.19 0.18 0.11 0.41 0.40 0.08 0.20 0.09 0.14 0.48 0.42
0.02 0.12 0.00 0.25 0.09 0.24 0.05 0.17 0.00 0.00 0.03 0.10 0.00 0.06 0.00 0.00
0.24 0.24 0.08 0.11 0.18 0.56 0.92 0.98 0.18 0.14 0.07 0.30 0.11 0.58 0.49 0.43
nificantly larger; (3) however, it was for summer temperatures that a higher percentage of variance than for sample depth was explained (Diatom PC1, Chironomid PC1); and (4) a range of variables was apparently responding: variables related to external loading, such as particle size; integrative variables, such as elemental ratios; and species specific variables, such as microfossils. Concerning microfossils, it was remarkable that for all groups but cladocera it was the first principal component (PC1) of their variability that related to temperature patterns, indicating that climate has been the main driving force of the system during the last two hundred years. Variety of ecosystem responses to air temperature forcing Ecosystem responses to external fluctuations are unlikely to be linear even on relatively short-time scales such as those considered in the present paper. However, relationships other than linear (step-like, exponential, asymptotic) are extremely difficult to demonstrate. However, by taking advantage of the overall clear trends during these two centuries in summer and autumn temperature, and the steep warming during the last 25 years, it is possible to comment on the diversity of responses shown in Lake Redó. Figures 6 and 7 show plots of the significant responses plotted against either summer or autumn mean temperatures. The series was divided into four intervals (roughly every half century)
0.64 0.65 0.04 0.06 0.17 0.37 0.45 0.69 0.30 0.08 0.097 0.68 0.11 0.19 0.44 0.27
0.01 0.04 0.02 0.76 0.38 0.48 0.12 0.30 0.02 0.00 0.01 0.29 0.01 0.10 0.01 0.00
0.00 0.00 0.07 0.07 0.00 0.01 0.01 0.04 0.00 0.00 0.05 0.02 0.07 0.02 0.00 0.00
in order to show the general pattern for the series as well as for shorter time scales. Particle size showed a step-like relationship with autumn temperature and less clearly with summer temperature (Figures 5a & 6). Particle mean volume (PMV) decreased quickly in the mid 1860’s, when the warming trend of the autumn temperature reached 2.4 °C. This apparent threshold could be associated with a change in rainfall at that time, but this apparent relationship could also be a simple artefact caused by the occurrence of the temperature trends within the two sedimentation phases, which could be related to other causes up to now unknown. Elemental nitrogen and total carotenoids, which can be considered indicators of lake primary production, showed a progressive decrease with autumn warming until 1950 when they stabilise (Figures 5b & 7). Their decrease might be related to some delay in the deepening of the summer thermocline and, as a consequence, a parallel reduction in the internal loading of nutrients. As shown in Figure 8, Lake Redó has two conspicuous productivity periods along the year, namely the spring period, at the onset of the stratification, and in autumn during overturn. Productivity adjustment to changes in forcing did not happen on short time scales (Figure 7). It appeared to be a highly resilient response, looking as if quasi-stationary states of productivity were slowly modified (Catalan et al., 2002, this issue). On the other hand, the significant relationship between pigment composition (PC2) and autumn warm-
139
Figure 6. Plots of a range of response variables analysed in core RCM2 against summer and autumn air temperatures. Data symbols refer to four different time periods (1781–1849, 1850–1899, 1900–1949, 1950–1997). Separate linear regression are plotted for each of the four time periods. Vertical grids indicate one temperature standard deviation for the whole period.
ing could be a spurious correlation because the pigment proportions in the top layers of the sediments (corresponding to the strongest warming phase) may not yet
have been modified by diagenesis (Hurtley & Armstrong, 1991). The statistical relationship may have arisen from the step in PC2 near the time of the ac-
140
Figure 7. Plots of a range of response variables analysed in core RCM1 against summer or autumn air temperatures. Data symbols refer to four different time periods (1781–1849, 1850–1899, 1900–1949, 1950–1997). Separate linear regressions are plotted for each of the four time periods. Vertical grids indicate one temperature standard deviation for the whole period.
celeration in warming (Figure 5b), it might be a climatic response but it also might simply be a diagenetic boundary. High values of elemental sulphur in some late 20th century samples, contrasting with the rest of the core, were difficult to interpret as well, since they were still part of the active biogeochemical dynamics of the lake.
Concerning microfossils, diatom composition showed the strongest response, both in relation to summer and autumn air temperatures (Figures 5a & 6). The response was only evident from 1900 onwards and, in contrast with elemental nitrogen and total carotenoids, diatoms showed a enhanced change during the last 50 years, indicating that the temperature variability was better
141 recorded by species changes than matter fluxes. On the other hand, the large fluctuations in temperature during the last half of the 20th century helped to show the hysteresis in the response. Diatoms did respond to the coldest years of the 1970’s in the direction expected from the early 19th century behaviour, but without reaching the assemblage composition equivalent to assemblages for equivalent low temperatures in the previous century (Figure 6). The two diatom species (Fragilaria nanana, Cyclotella pseudostelligera) with a higher loading on PC1 (Table 1) were planktonic species, the only ones commonly growing at present in the water column. In the seasonal cycles studied, these two species had a very distinctive distribution pattern (Figure 9). Fragilaria grew in September and was succeeded by Cyclotella in October. They cover the latest part of the stratification period, when the epilimnion was better mixed, and epilimnetic phytoplankton likely experienced a more variable light field. Given the well-defined monthly growth pattern for these two diatoms, it appeared worthwhile to directly compare the temperature fluctuations during September and October with the respective Fragilaria and Cyclotella sediment patterns (Figure 10). The response of the two species was slightly different, although the two showed a similar threshold when within the warming tendency they started to significantly increase in the first quarter of the 20th century. Fragilaria after a sharp increase
stabilised and thereafter fluctuated following the main September temperature fluctuations, whereas Cyclotella maintained the exponential increase following the October progressive warming (Figure 10). The assemblage dominant diatom species had no influence on PC1 but in PC2, which was not related to temperature (Table 1). The chrysophycean cysts response was weakly significant (Table 2), and its limnological interpretation is difficult owing to our scarce knowledge on the ecology and phenology of the species and their correspondence with cysts. The S137C cyst negative response to warming probably corresponds to a Mallomonas species. The Pyrenean lakes are usually poor in Mallomonas species compared to equivalent lakes at higher latitudes. In the case of chironomids, and in contrast to other response variables, the relationship between the assemblage and climatic change was exclusively with summer temperature (Table 2). Nearly all species appearing and certainly the most abundant have a negative relationship with PC1 (Table 1), indicating that the whole chironomid assemblage was negatively affected by warmer summers, but with different degree for each species. Nevertheless, it is challenging to find a satisfactory interpretation for this relationship, because chironomid larvae have their population minimum in Lake Redó during summer, since adults emerge in early summer (Rieradevall, unpublished data). Heterotrissocladius is a cold stenotherm genus that declines in
Figure 8. Seasonal water column changes of chlorophyll in Lake Redó. Dotted lines are isotherms to indicate the thermal structure and mixing patterns of the water column. The ice covered period is indicated, with the thickness of the ice and snow cover scaled to depth.
142
Figure 9. Seasonal distribution of Fragilaria nanana and Cyclotella pseudostelligera in the water column of Lake Redó for the ice-free period of 1997. Isolines indicate cells per ml, and dashed lines isotherms.
relative abundance with decreasing latitude (Walker et al., 1990, 1997). Among the species of the genus, H. marcidus can be considered the most thermophilous, but restricted to waters colder than 18 °C (Saether, 1975). It is found in Europe from Fennoscandia down to the Iberian Peninsula (Illies, 1978) and lives from the littoral until the deepest and coldest areas of alpine lakes (Rieradevall et al., in press). Similarly, Paratanytarsus austriacus and particularly Micropsectra radialis are cold stenotherm species (Fjellheim et al., 1997). We could expect that these species came closer to their limits of temperature tolerance in warmer summers, although we cannot discard that indirect mechanisms related with food availability may occur. On the other hand, since the response was at the scale of several decade, the actual control could be on adults, affecting lake population through recruitment. In contrast with autumn responses, highly conditioned by the strong
trend during the last 20 years, the relationship between chironomids and temperature covered the whole studied period, the species mirrored the ups and downs of summer temperature at scales of several decades (e.g., H. marcidus particularly followed June temperatures, Figure 11). Cladocera were the only microfossil group without any correlation of their first principal component of variation with air temperature. The significative component (PC4) was exclusively related with Acroperus harpae (Table 1). This was a rare species within the cladocera assemblage of the lake. Its microhabitat are macrophytes, which in the case of Lake Redó were aquatic mosses mainly occupying depths above the seasonal thermocline. Its spiky increasing appearance in the sediment record towards the present might be interpreted as a positive influence on its growth of a warmer epilimnion, late in the stratification period.
143
Figure 10. Comparison between air temperature annual means, smoothed (LOESS span 0.05) temperatures and the sediment record for the diatom species (Cyclotella pseudostelligera and Fragilaria nanana), the chironomid (Heterotrissocladius marcidus) and the cladoceran (Acroperus harpae).
Conclusions In spite of the limitations imposed by the different resolution of the air temperature time series and the sediment record, some conclusions can be derived from their comparison that appear robust and not significantly affected by the constraints of the data structure. Interannual variability in air temperature was quite high compared with ecosystem responses recorded in the sediments. Linkages between microfossils and climate were found at time-scales corresponding to smoothings of several decades. Century long trends appeared to be better matched by most sediment variables. However, because of the short record, there was an inherent danger of spurious correlation because of the diagenetic sequences in the upper sediment. The temporal sample resolution, between 3–6 years, limited the investigation to decade scales. The ecosys-
tem responses tended to follow mean forcing of several decades, but quick changes within a decade were also found (e.g., H. marcidus), suggesting that either a critical threshold was reached in the population or that there was a critical concatenation of years forcing in a given direction. When short periods of extremely cold years appeared within a much larger general trend of warming, there was either a weak response, hardly distinguishable at the operative resolution of the sediment record, or there was a response in the direction expected but with remarkable hysteresis. This latter case was well illustrated by diatom response to autumn temperatures. The response to the extreme cold period of the 1970’s was clear but the assemblage composition showed no tendency to return to the situation of the 19th century, when low temperatures were much more frequent but not so extreme.
144 Specific responses of a few species were much clearer than whole ecosystem responses or biogeochemical responses. The species responding were usually epilimnetic, but not all epilimnetic species responded. In some cases (e.g., F. nanana, C. pseudostilligera), knowledge of the present ecological features of the species provided evidence that the response was quite direct to the particular temperature changes of their growing season. Different taxonomical groups or even particular species within groups appeared to be particularly suitable for specific seasons. For instance, chironomids responded to summer temperatures, but did not react to the warming autumn trends. On the contrary, planktonic diatoms responded to autumn trends when conditions for their growth occurred in Lake Redó. In the case of diatoms, clear responses relied on a few species that were a small component of the assemblage. This implies that the response to temperature fluctuations may take quite different forms from lake to lake. However, nearly the whole chironomid assemblage reacted to temperature. Therefore, chironomid assemblages seem to be a more robust temperature indicator for lake inter-comparison and longer time scale studies (e.g., through the Holocene).
Acknowledgements This study was supported by the European Commission, Environment and Climate Programme, contract ENV4 CT95 0007 (MOLAR project).
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