Evidence of long-term NAO influence on East-Central Europe winter precipitation from a guano-derived δ15N record

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Evidence of long-term NAO influence on East-Central Europe winter precipitation from a guano-derived δ15N record
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Scientific Reports
Cleary, Daniel M.
Wynn, Jonathan G.
Ionita, Monica
Forray, Ferenc L.
Onac, Bogdan P.
Springer Nature
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North Atlantic oscillation ( lcsh )
Precipitation (Meteorology) ( lcsh )
Caves -- Romania ( lcsh )
serial ( sobekcm )
Europe -- Central Europe
Europe -- Eastern Europe


Currently there is a scarcity of paleo-records related to the North Atlantic Oscillation (NAO), particularly in East-Central Europe (ECE). Here we report δ15N analysis of guano from a cave in NW Romania with the intent of reconstructing past variation in ECE hydroclimate and examine NAO impacts on winter precipitation. We argue that the δ15N values of guano indicate that the nitrogen cycle is hydrologically controlled and the δ15N values likely reflect winter precipitation related to nitrogen mineralization prior to the growing season. Drier conditions indicated by δ15N values at AD 1848–1852 and AD 1880–1930 correspond to the positive phase of the NAO. The increased frequency of negative phases of the NAO between AD 1940–1975 is contemporaneous with higher δ15N values (wetter conditions). A 4‰ decrease in δ15N values at the end of the 1970’s corresponds to a strong reduction in precipitation associated with a shift from negative to positive phase of the NAO. Using the relationship between NAO index and δ15N values in guano for the instrumental period, we reconstructed NAO-like phases back to AD 1650. Our results advocate that δ15N values of guano offer a proxy of the NAO conditions in the more distant past, helping assess its predictability.
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Volume 7

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2 moisture source11, there is a lack of paleo-records of the NAO in ECE. Furthermore, to place recent NAO variability in a long-term context, there is a pressing need to develop longer records. Here we use coupled carbon and nitrogen isotope ratio data (13C and 15N values) of a 286 cm guano core from MC in ECE, in an attempt to characterize the hydroclimate inuence on the N-cycle since the latest part of the Little Ice Age (LIA; AD 1650 to 1850) and up to AD 2012. We rst compare these data to the December-January-February (DJF) NAO index that represents the strength of the system during the winter months. en we use DJF meteorological records and a ECE reconstructed precipitation series from Pauling et al .12 that directly and indirectly relate to the NAO to further examine the impact of changes in vegetation and hydrology of ECE on the isotopic composition of guano.n—ƒ‘ƒ†Ž‹ƒ–‡Bat guano is primarily composed of loose organic material, such as insect chitin, with a geochemistry character ized by an abundance of transition metals13, 14. Although there are numerous organic compounds in guano, chitin is the most abundant in MC deposit. erefore, measured 15N values reect chitin derived N, while the contribution of other N sources to bulk guano is likely insignicant. If bats are not changing their roost sites, guano can accumulate as thick deposits (3 m or more) over long time periods (centuries to thousands of years)13, 15. Depending on the morphology and hydrology of each cave system, ooding of underground passages may cause guano deposits to be interbedded with clay and silt layers. Such circumstances oer additional information with respect to local cave environmental changes while guano was being deposited16,17. Bat guano may provide an ideal record of past vegetation because the 13C value of plants in the region is transferred from plant to insect to bat and ultimately recorded in guano. e 13C values of foliage are distinct between the two main photosynthetic pathways (C3 and C4)18. Additional variation in 13C values occurs within C3 plants in response to the water use eciency of photosynthesis19. e preservation of these values within guano provides new and critical information on the changing vegetational assemblage through time20– 25. Although more complex, recent studies have demonstrated that 15N values in bulk guano can be interpreted as an integrator of the nitrogen cycle (N-cycle)26, 27. When nitrogen is a limiting nutrient, nitrogen is conserved and as a result less nitrogen is lost and 15N values decrease (i.e., a relatively closed N-cycle)28, 29. A relatively open cycle results in high 15N values under the opposing conditions. When it can be demonstrated that a climatic inuence controls whether the N-cycle is open or closed, 15N values can also be used as a paleoclimatic proxy26. Since the NAO has a strong inuence on precipitation and temperature it is possible that the nitrogen isotopic composition of cave bat guano, which has already been shown to reect changes in water availability could provide insight into the inuence of the NAO beyond the historical record.‡•—Ž–•ƒ†‹•…—••‹‘•e nitrogen isotopic composition of bat guano may be aected by diagenesis aer deposition via processes of ammonia volatilization or denitrication13, 30. e conditions under which alteration may have been significant are in part reected in variation of %N along the prole (see Cleary et al .26). e %N in the MC core (see Supplementary Dataset1 ) shows little deviation from near surface values (~11.3%) to the lower most portion of the core (mean t t 10.6%). erefore, the increasing trend in 15N values between AD 1650 and AD 1980 (see Supplementary Fig. S2) is likely unrelated to diagenesis and can be interpreted as primary variation, considered here as a proxy of the NAO variability. e subsequent interval of lower 15N values (7.5 to 9.5‰; AD 1980 to 2012) represents a change in local N-cycle (see discussion below) as opposed to diagenetic processes. It is dicult to elucidate past 15N values at any stage of the food web (plant-insect-bat-guano), however it is possible to interpret 15N as an integrator of the N-cycle28. e isotopic fractionations, N pool mixing, and N gains/losses produce the 15N value of the system (soil, biomass, consumers). erefore this resulting value integrates these processes and can be used to interpret the state of the N-cycle. e fractionations occurring Figure 1. Correlation map between (a) winter (DJF) NAO index and winter precipitation (PP), and (b) temperature (TT) derived from the CRU TS3.24.01 data set54. Green contours outline Romania. Dotted areas indicate correlation coecients signicant at 95% signicance level on a standard t-test. e gure was produced using Matlab 2014b (


3 during the metabolic processes within bats and insects as nitrogen is transferred from plant to guano remain xed through time. Since these fractionations follow conservative pathways, variation in the nitrogen isotopic composition of guano can ultimately be related to changes that occur in the soil inorganic nitrogen reservoir from which plants access nitrate and ammonia28, 29. Such changes have been connected to the state of the N cycle (open: more nitrogen loss and higher 15N values; closed: less nitrogen loss and lower 15N values)29 and attributed to hydrological inuence on the state of the N-cycle31–33. Cleary et al .26 suggested variation in 15N values of guano (ultimately related to those of foliage) are strongly correlated to instrumental record of winter precipitation. is may result from a lag between the preservation of 15N values in foliage during the growth phase (spring-early summer), which reect soil N conditions from months immediately prior to growth (late fall-winter). In temperate forests, the maximum plant-available N occurs just prior to the onset of the growing season due to limited plant uptake of N that has been produced largely by microbial mineralization in months prior34. Although there may be signicant wet deposition of N dur ing the spring and summer months, this ux into terrestrial ecosystems is on average lower than that produced via mineralization35, 36. is pool of plant-available N is soluble; thus during the winter season it is very sensitive to leaching processes, which is in turn driven by winter climatic conditions such as snow melt and the type of winter precipitation (snow vs. rain) when temperatures that straddle the threshold of freezing37, 38. Since the state of the N-cycle is controlled by the amount of N in the system, we infer that any change in the N-cycle is in response to the impact of winter hydroclimate on leaching processes. During the subsequent growing season when plants begin to access the soil N-pool, the state of the N-cycle established by the amount of leaching in the winter is then recorded in the new foliage. Increased leaching would reect a more open N-cycle and result in higher 15N val ues39 at each level of the food chain and ultimately guano. erefore, although bats forage in the summer months, nitrogen delivered to the soil via spring/summer precipitation will likely not inuence the 15N values of guano. Cleary et al .26 compared 15N values of bat guano to corresponding 13C values and to meteorological data from a nearby weather station in the Mada region (Metaliferi Mountains, W. Romania), and interpreted that water availability is a primary control of 15N values of guano. Given the well-documented relationship of 13C values of leaf tissues to water-use eciency19,40 the carbon isotopic composition of MC guano (26.5 to 21‰) suggests variation within the C3 pathway that may ultimately be related to changes in water availability. Based on these observations, we test a hypothesis for a hydrological connection between 13C and 15N values of guano by examining the correlation between each proxy in the Mgurici Cave guano record. Excluding two outliers, the resulting statistical analysis indicates that the 15N and 13C values in the MC record between AD 1800 and 2012 show a negative correlation (p-value t t 0.001; R2 t t 0.62; n t t 105; see Supplementary Fig. S2a). is suggests some dependence of the N-cycle of the bats foraging area on water availability, as the latter can be interpreted as the primary control on 13C values of C3 vegetation. e relationship between 15N and water availability is in contrast to other studies32, 33, 41, however, is consistent with results obtained from modern guano25 and precipita tion in NW Romania. Although both 15N and 13C values of guano reect hydrological conditions, it is likely that they are recording dierent seasonal inuences on water availability. While 13C values of foliage are related to water stress during photosynthesis (spring/summer), 15N values of guano are related to the winter precipitation inuence on leaching. erefore, correlation between 13C values and 15N values is ultimately the result of the winter precipitation (control of N-cycle) contributing to the degree of water stress in the spring/summer (control of 13C). Consequently, if there is an inuence of the NAO on precipitation in ECE, the nitrogen isotopic composition of guano should retain this signal more accurately than 13C values. In accordance, hereaer we focus our interpretations of 15N values of guano on reconstructing DJF precipitation. One of the most striking features of our 15N reconstruction is the abrupt decrease (~4‰) at the end of 1970’s (Fig. 2a) representing a shi of the NAO to a strong positive phase aer the mid-1970s. is swing corresponds to regional climatic eects such as milder and wetter winters in northern Europe42, a reduced discharge of the Danube River43, and decreasing winter precipitation over Romania44. is shi at the end of 1970’s is clearly observed in the sea level pressure (SLP) and precipitation patterns (Fig. 2 ). e dierence map in the SLP eld between 1940–1970 and 1980–2010 is indicative of a period characterized by an increased frequency of positive NAO phases aer the 1970s (Fig. 2b), which is associated with a strong reduction in winter precipitation over the southern part of Europe (Fig. 2c). e resulting precipitation anomaly that occurs between northern and southern Europe during the winter months is also recognized in instrumental records across these regions1. is regional decrease in winter precipitation that occurs at the end of the 1970’s is demarcated by the most signicant decrease in 15N values of MC guano. Given the direct link between precipitation and the current phase of the NAO, we interpret the 15N values to largely reect a hydrologic component of the regional climate with a signal that can be related to the NAO. Due to the absence of 15N values for certain years it is dicult to condently utilize a statistical analysis to compare the record directly to the NAO index. However, there is a correlation (p-value t t 0.002; R2 t t 0.43) between the rst derivatives of time series of the NAO index and of the 15N values of MC guano (AD 1981–2012; interval of near annual ages of guano; see Supplementary Fig. S3). Additionally, since AD 1800, lower (higher) 15N values, which are indicative of drier (wetter) conditions, occur preponderantly during positive (negative) phases of the NAO (Fig. 3 ). e occurrence of more negative phases of the NAO (AD 1940–1975) corresponds with progressively wetter conditions expressed in the 15N record. Likewise, trends towards drier conditions inter preted from 15N values appear near contemporaneous with a higher frequency of NAO positive phases (AD 1848–1852; AD 1875–1930; and AD 1975–2012). Our interpretation of 15N values of MC guano as a NAO proxy (Fig. 3a) is supported by comparison to other precipitation proxies that are more directly inuenced by the NAO. Lower 15N values from MC correspond well with drier conditions indicated by a DJF reconstructed precipitation record for ECE12 (Fig. 3b ), a long-term precipitation measurement in southern France45 (Marseille; Fig. 3c), and nearby Budapest and Baia


4 Mare meteorological stations45 (Fig. 3d,e). All three are located over regions strongly inuenced by NAO (see the blue shaded band in Fig. 1a). Frequently there is contemporaneous overlap between a negative NAO index and wetter conditions indicated by precipitation records and the 15N values from MC guano (Fig. 3h ). is agrees with an interpretation of a wetter NW Romania during the negative phase of the NAO. us, the state of the N-cycle that is preserved in 15N values of MC guano appears to be inuenced by DJF precipitation, which in turn is modulated in ECE by the NAO. A few of the general trends in hydroclimate that are expressed by the NAO index, meteorological records, and the nitrogen isotopic composition of MC guano can also be found in other Romanian and southern Europe paleo-records spanning the period AD 1850 to present. 15N values from the MC core trend towards wet conditions until AD 1800, uctuates between 1800 and 1975, aer which the climate abruptly became drier until present. Broadly, the 15N values from Zidit and Mgurici guano frequently show similar trends. e two records are well-correlated aer AD 1900, when both feature a gradual trend towards drier conditions interrupted by a wetter interval between AD 1940 and 1975 (Fig. 3g,h). 15N values from Zidit, Mgurici, and 13C values in a Sphagnum core from the Tul Muced46 (Rodnei Mountains, N. Romania; see Supplementary Fig. S1), all reect a drying trend aer ~AD 1975 (Fig. 3f–h). However, the MC record appears to correspond more consistently with the NAO index, suggesting that the inuence of the NAO is more prevalent in NW Romania than in other regions of the Carpathians. Given that the signal of the NAO instrumental record is reected in the 15N values since AD 1850, we extend our interpretation of this proxy to infer past phases of the NAO prior to the instrumental record. Indeed, using the ECE DJF precipitation reconstruction12 and measurements45 (Marseille) as additional evidence, 15N values suggest that the positive phase of the winter NAO dominated the circulation between AD 1650 and 1800. Over this 150-year interval, there were ve prominent periods of at least 2 years each during which the negative phase was dominant (Fig. 3h). Our core reveals a major depositional hiatus, when guano accumulation ceased and a silty-clay layer was deposited between ~AD 1713 and 1715 (Fig. 3h). is period corroborates well with one of the highest reconstructed value of DJF precipitation across ECE12, suggesting unusually wet winter seasons. Concurrent, historical hydroclimate records elsewhere in Europe47 document an increased in ooding frequency at this time. Interestingly, a testate amoeba record from Tul Muced ombrotrophic bog located ~100 km NE of our cave documents a decline in water table depth over this period46. Furthermore, the sharp decrease of the 13C values of Sphagnum at the same location (Fig. 3f ) was interpreted to indicate prevalence of drier conditions44. ese site-specic contrasting precipitation patterns are not surprising since the winter NAO signal is stronger in the intra-Carpathian region8. Following the guano hiatus, the 15N time series suggests that beginning at ~AD 1720, a gradual transition to recurring positive phases of the NAO occurred, with the atmosphere remaining locked into this mode until Figure 2. (a) 15N of MC guano from 1850 to 2012 (see text for details). (b) e dierence in the Sea Level Pressure between 1940 and 1970 (pre-shi) and the period 1980–2010 (post-shi) based on data from NCEP/ NCAR Reanalysis55. (c) As in (b) but for winter precipitation derived from CRU TS3.24.01 data set54. e gures were produced using (a) pro Fit 7.0 ( and (b,c ) Matlab 2014b (http://de.mathworks. com/products/new_products/release2014b.html), respectively. e digital version was generated using Adobe Illustrator CC17 (


5 AD 1790. During this 70-year interval, signicant negative phases of the pattern appeared only three times (AD 1760, 1775, and 1785), all coincident with wettest winters recorded at the Marseille weather station (Fig. 3c,h). From AD 1800 to 1820, we identied an abrupt transition to more positive nitrogen isotopic values, which suggest increased regional moisture delivery mostly over the winter period. As inferred from our guano 15N values, this begins a period of ~20 years of mild and wet winters in the ECE relative to the earlier interval, which ends ~AD 1840 when precipitation started to decrease. e onset of this period of positive winter NAO phase is coeval with a marked phase of ice ablation in the St. Livre Cave (SW Switzerland), thought to represent almost three decades of warm and dry winters48. It also agrees well (but opposite sign) with a composite speleothem annual growth-rate record in NW Scotland, reective of positive winter NAO states49. It is apparent from the discussion above that the changes in the phases of the NAO may partly explain the climate variability over the last part of the LIA.‘…Ž—•‹‘•A nitrogen isotopic proxy record of guano provides new information regarding the eect of DJF hydroclimate system on the N-cycle and the inuence of the winter NAO on the ECE. e evidence of a NAO signal contained within the MC guano 15N series is the temporal strong correlation of the winter precipitation amount in the instrumental record. is study demonstrates that future guano research should consider not only precipitation, but also larger scale climatic systems when utilizing the nitrogen isotopic composition of guano. e use of nitrogen isotopic composition of bat guano it is possible to add to, and improve the historical record of the NAO. As such, our results suggest that the 15N values of guano can be utilized to reconstruct past phases of the NAO beyond the instrumental record and demonstrates that the 15N values of guano can oer a proxy of the NAO in regions where instrumental or historical records are limited.‡–Š‘†•n—ƒ‘…‘”‹‰ƒ†•ƒ’Ž‹‰ In October 2012, a Russian peat corer was used to extract a 287 cm core from a guano pile located in the Circular Room of MC (Fig. 1 in Johnston et al .50). e coring site was adjacent (within 1 m) to the one investigated by Johnston et al .50. Both cores have similar stratigraphy, however, the lower 29 cm of the rst one recovered only clay, whereas ours penetrated a 4-cm thick clay layer at 237 cm revealing an additional 46 cm of guano beneath it. Except for the clay layer, the entire core length was sampled for isotopic analyses and radiocarbon measurements. Figure 3. Comparison of guano 15N with other hydroclimate proxy records between AD 1650 and 2012: (a) Winter (DJF) NAO index56; DJF precipitation data series from ECE12 (b), Marseille45 (c), Budapest45 (d), and Baia Mare45 (e), 13C of Sphagnum from Tul Muced46 (f), 15N values of guano from Zidit Cave26 (g), and Mgurici Cave (h; this study). e black smoothed lines in a–e represent the 3-year running mean.


6 ƒ†‹‘…ƒ”„‘†ƒ–‹‰ƒ†ƒ‰‡†‡’–Š‘†‡Ž• Twenty aliquots of bulk bat guano from various depths of the Mgurici core were submitted for radiocarbon dating by accelerator mass spectrometry (AMS) at the Poznan Radiocarbon Laboratory (Poland) and returned ages in stratigraphic order. Sample MG-15 was contaminated with young organic matter and thus discarded. Since guano is mainly composed of chitin (95%), which makes it an excellent material for AMS age determinations51, no sample preparation was needed. e age-depth models (see Supplementary Fig. S4) are based on a linear interpolation between each14C age in the upper 50 cm of the core, whereas for the rest of the sequence a type 4 smooth spline was applied. Both models were generated using Clam code52. e reasoning for employing a linear age-depth model for the upper 50 cm is because continuous observations since 1965 conrmed that the size of the bat colony has not changed, and therefore, it is expected that the guano accumulation remained constant. e default calibration curve utilized by Clam is the northern hemisphere terrestrial curve IntCal13.14C (cc t t 1) from Reimer et al .53. e samples in the top 50 cm of the core are characterized by high radiocarbon activity (130.06 t t 0.4 and 132.46 t t 0.34 pMC) resulting in modern ages (1979–1980 and 1977–1978 cal. years). Guano began to accumulate in the Circular Room at ~AD 881, shortly before the beginning of the Medieval Warm Period (MWP: ~AD 950–1300). One hiatus is inferred from the age depth model between AD 1237–1651, an interval that corresponds to the rst half of the LIA. e raw14C data are included in Supplementary Dataset 2, and the results of modeling in Supplementary Dataset 3).bŽ‡‡–ƒŽƒ†•–ƒ„Ž‡‹•‘–‘’‡ƒƒŽ›•‡• Contiguous 1-cm bulk guano sub-samples were recovered for isotopic analyses along with a modern sample collected in 2012 to anchor the isotope chronology. Chitin is the dominant organic compound in MC guano, therefore, we considered compound specic extraction to be unnecessary. Due to the cave climate (see Supplementary Information) it is highly unlikely that any soluble guano-derived N-compound will survive and potentially impact the nitrogen isotopic composition. All samples were prepared for 15N and 13C analysis following the procedures described in Forray et al .25 and Cleary et al .26. Out of these samples, 1–2 mg aliquots were weighed and placed in tin cups and then measured for 15N, 13C, %N, %C, and C:N. Analysis was completed using a Costech Elemental Analyzer coupled to a Delta V Isotope Ratio Mass Spectrometer hosted in the Stable Isotope Laboratory (School of Geosciences, University of South Florida). A glutamic acid (internal standard; 15N: 6.28‰; 13C: 16.50‰; %N: 9.54%; %C: 41.37%) and a protein standard B2155 ( 15N: 5.94‰; 13C: 26.98‰; %N: 13.32%; %C: 46.5%) were used during analysis. Certied reference materials, B2155 and IAEA-N1, were used to calibrate the 15N value for the internal standard. B2155 and IAEA-C7 were used to calibrate 13C value of the glutamic acid. Estimation of the precision of analysis (15N: 0.08‰; 13C: 0.04‰) was based on replicate internal standards during each run (Supplementary Dataset 1).–ƒ–‹•–‹…ƒŽ‡–Š‘†• Correlation analysis between 15N values (mean t t 10.4‰; std. dev. t t 1.5) and 13C values (mean t t 24.5‰; std. dev. t t 0.7) (n t t 105) was completed using SPSS. is statistical test is appropriate as both data sets were extracted from the MC core with the same sampling and temporal resolution. Resulting p value andR2 (p-value t t 0.001; R2 t t 0.62) from the 2-tailed test indicate statistical correlation. MATLAB was used to convert unevenly sampled data to evenly sampled 15N values, whereas EXCEL was used to compute the rst derivatives (in 1-year time steps). is step allowed for the examination of year-to-year changes in values. 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8 t 53.t eimer, P. J. et al IntCal13 and Marine 13 adiocarbon Age Calibration Curves 0-50,000 Years cal BP. adiocarbon 55, 1869–1887, (2013).t 54.t Harris, I., Jones, P. D., Osborn, T. J. & Lister, D. H. Updated high-resolution grids of monthly climatic observations – the CU TS3.10 Dataset. Int. J. Climatol. 34, 623–642, (2014).t 55.t alnay, E. et al e NCEP/NCA 40-year reanalysis project. Bull. Am. Meteorol. Soc. 77, 437–471,;2 (1996).t 56.t Jones, P. D., Jnsson, T. & Wheeler, D. Extension to the North Atlantic Oscillation using early instrumental pressure observations from Gibraltar and South-West Iceland. Int. J. Climatol. 17, 1433–1450,;2-P (1997).…‘™Ž‡†‰‡‡–•We thank Dr. T. Tma (TT) and A. Giurgiu who helped during coring and initial sampling activities. We acknowledge the E-OBS dataset from the EU-FP6 project ENSEMBLES ( and the data providers in the ECA&D project ( is research was funded by the Romanian CNCS grant PN-II-ID-PCE 2011-3-0588 to BPO.—–Š‘”‘–”‹„—–‹‘•B.P.O. designed the project and B.P.O., T.T., and J.G.W. recovered the cave guano core. B.P.O., F.L.F., and T.T. sampled the core and D.M.C. ran the stable isotope analyses and constructed the age-depth model. M.I. analyzed present-day climate data and derived precipitation sources. D.M.C. analyzed the data and wrote the main manuscript text along with B.P.O. and J.G.W., and further contribution from M.I. and F.L.F.††‹–‹‘ƒŽfˆ‘”ƒ–‹‘Supplementary information accompanies this paper at Competing Interests : e authors declare that they have no competing interests. Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional aliations. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. e images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit e Author(s) 2017