Variation in δ15N of fog-dependent Tillandsia ecosystems reflect water availability across climate gradients in the hyperarid Atacama Desert

Global and Planetary Change 183 (2019) 103029

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Research article

Variation in δ15N of fog-dependent Tillandsia ecosystems reflect water availability across climate gradients in the hyperarid Atacama Desert

T

Andrea Jaeschkea, , Christoph Böhmb, Felix F. Merklingerc, Stefano M. Bernasconid, Mark Reyersb, Stephanie Kuscha, Janet Rethemeyera ⁎

a

Institute of Geology and Mineralogy, University of Cologne, Germany Institute for Geophysics and Meteorology, University of Cologne, Germany c Nees Institute for Biodiversity of Plants, University of Bonn, Germany d Geological Institute, ETH Zürich, Switzerland b

ARTICLE INFO

ABSTRACT

Keywords: Atacama Desert Hyperaridity Tillandsia landbeckii Stratocumulus cloud Fog Nitrogen isotopes WRF model

The Atacama Desert is considered one of the driest places on Earth, where the availability of water plays a crucial role in determining the presence of plants. The sparse vegetation is limited to the coastal mountains, where abundant fog provides the main source of water and nutrients for unique Tillandsia landbeckii ecosystems. The apparent retreat of this fog-dependent vegetation over the past decades, however, may relate to changing climatic conditions, in particular increasing aridity. In this study, we used the nitrogen isotopic composition (δ15N) of plant organic matter as a measure of water availability and atmospheric nitrogen input in present and past Tillandsia dune fields. We compiled an extensive data set on δ15N values of living plants and corresponding site factors (latitude, elevation, cloud cover and precipitation) along a coastal transect. We present radiocarbon-based ages of relict T. landbeckii layers preserved in sand dunes that evolved episodically over the past 2500 years. Site-averaged δ15N values range from +2‰ to −16‰, with variations of up to 4‰ observed within one site that can be related to changes in elevation. The spread in δ15N values is surprising and considerably larger than previously reported for T. landbeckii. In contrast, δ15N values of Huidobria fruticosa and Ophryosporus spp. leaves collected mostly below and above the fog zone vary between +4‰ and + 17‰, largely in agreement with global observations from water-limited systems. Comparison with satellite-based meteorological data and modelling results revealed significant correlations between δ15N values of T. landbeckii and total cloud cover (r = −0.90; p < .01), cloud height (r = −0.93; p < .001) and precipitation (r = −0.98; p < .001) along the investigated transect. The gradient in δ15N values further coincides with surface ocean nutrient concentrations in austral summer when ocean primary production is highest suggesting a potential marine source for the large spread in δ15N values. Reconstruction of past changes in fog water supply based on fossil T. landbeckii remains indicate a distinct dry episode that is consistent with a known period of extreme long-lasting droughts during late Medieval times.

1. Introduction

rainfall can occur during El Niño years (Rundel et al., 1991; Houston, 2006; Schulz et al., 2011). In contrast, fog frequently occurs as a result of the regular formation of thick stratocumulus (Sc) cloud banks below 1000 m over the Pacific Ocean (Cereceda et al., 2008; Garreaud et al., 2008; Lobos Roco et al., 2018). Where the Sc cloud intercepts the steep topography of the coastal Cordillera, it gives rise to a persistent fog zone, locally known as camanchaca (Rundel et al., 1991; Pinto et al., 2006; Cereceda et al., 2008). Fog is the most important source of moisture, which allows the development of unique plant communities (termed lomas) of surprisingly high biodiversity in northern Chile and southern Peru (Johnston, 1929; Rundel et al., 1991; Pinto et al., 2006). Isolated patches of

The Atacama Desert in northern Chile is believed to be one of the driest places on Earth (e.g. Dunai et al., 2005). Prevailing hyperarid conditions strongly limit plant growth and survival, resulting in vast areas with absolutely no vegetation in the core area of the Atacama (Rundel and Dillon, 1998). The general climatic regime is determined by its position at the subtropical high pressure belt, the cold northward flowing Humboldt current, and by the rain shadow effect of the Andes resulting in a mild, nearly uniform coastal climate (Houston and Hartley, 2003; Garreaud et al., 2008; Cereceda et al., 2008). Annual precipitation is extremely low but short irregular periods of heavy ⁎

Corresponding author. E-mail address: [email protected] (A. Jaeschke).

https://doi.org/10.1016/j.gloplacha.2019.103029 Received 21 May 2019; Received in revised form 29 August 2019; Accepted 5 September 2019 Available online 06 September 2019 0921-8181/ © 2019 Elsevier B.V. All rights reserved.

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Fig. 1. (a) Map of the study area within the Atacama Desert in northern Chile showing the locations of the different Tillandsia loma systems along the coastal Cordillera (1: Quebrada rio Lluta; 2: Quebrada Vitor; 3: Quebrada Camarones; 4: Cerro Guanacos; 5: Cerro Oyarbide; 6: Cerro Pajonales; 7: Cerro Peninsula; 8: Cerro Chipana; 9: Quebrada rio Loa; according to Pinto et al., 2006) and (b-d) photographs from fieldwork in 2017. Typical occurrence of monospecific Tillandsia landbeckii stands (b) on SW-facing slopes of small hills and (c) small sand dunes at Cerro Oyarbide (5); (d) flowering T. landbeckii stand at Quebrada rio Loa (9).

predominantly Tillandsia landbeckii plants supported by fog typically occur on the inner coastal landforms at altitudes between 900 and 1300 m above sea level (m a.s.l.) (Pinto et al., 2006; Westbeld et al., 2009; González et al., 2011; Latorre et al., 2011). These unique, functionally rootless plants (also known as airplants) of the Bromeliaceae family grow unattached to sandy or rocky surfaces and rely exclusively on water and nutrients supplied by fog (Rundel and Dillon, 1998; Pinto et al., 2006; González et al., 2011). They are ecological specialists, well adapted to the extremely arid environment by physiological and morphological adaptations such as Crassulacean Acid Metabolism (CAM) for photosynthetic carbon assimilation and narrow leaves with waterabsorbing trichomes (Rundel et al., 1997). This enables these plants to survive even longer periods without fog, however, continuous dehydration will eventually lead to plant dieback. On the other hand, too much moisture is believed to hinder plant growth (e.g. Benzing and Renfrow, 1971; Benzing et al., 1978; Martin, 1994). The isotopic composition of nitrogen (δ15N) in soil and plant organic matter can be used as a measure of water availability along precipitation gradients and provides valuable information on nitrogen input and subsequent transformation within a defined ecosystem (Handley et al., 1999; Díaz et al., 2016). On a global scale, a negative correlation between foliar δ15N and mean annual precipitation across different terrestrial ecosystems is observed indicating that climate is the major driver of the nitrogen cycle (Handley et al., 1999; Amundson et al., 2003; Craine et al., 2009). In general, positive δ15N values are typical for water-limited systems, whereas negative δ15N values are characteristic for areas with increased precipitation (Heaton, 1987; Schulze et al., 1998; Handley et al., 1999; Amundson et al., 2003; Swap et al., 2004). This global relationship between precipitation and δ15N values of mostly C3 plants, however, does

not include sites where annual precipitation is very low. Studies from the hyperarid Namib and Atacama deserts revealed an apparent reversal of the global trend at low precipitation levels (< 200 mm, Soderberg, 2010; < 50 mm, Díaz et al., 2016) pointing to different drivers below a certain threshold. In the Namib Desert, the reversed trend in foliar δ15N values (C3/CAM plants) and precipitation was proposed to be related to the presence of frequent coastal fog providing additional input of 15Ndepleted nitrogen species (Soderberg, 2010). Fog may also play a significant role in nitrogen supply and cycling for the unique Tillandsia ecosystems along coastal northern Chile (González et al., 2011; Latorre et al., 2011). The initial study of Latorre et al. (2011) suggested that the relatively large spread in δ15N values (−2‰ to +4‰) observed in living Tillandsia plants most likely reflected variations in fog moisture. Since the 1970s, a general retreat of the fog-dependent ecosystems has been observed (Rundel et al., 1997; Pinto et al., 2006; Schulz et al., 2011). The dieback is assumed to be related to changes in climatic conditions, in particular increasing aridity. This could be attributed to an intensification of the Southeast Pacific Anticyclone and associated weather extremes during recent decades (Falvey and Garreaud, 2009; Schulz et al., 2011; Cai et al., 2012; Scheff and Frierson, 2012). In addition to the general decrease in rainfall frequency, a strong reduction of cloud cover in the northernmost region may largely affect plant growth by further limiting water supply and favouring desiccation due to intense direct solar radiation (Schulz et al., 2011). For a better understanding of this vulnerable ecosystem currently enduring at the dry limit, a more detailed evaluation of the present-day distribution of T. landbeckii in relation to climate variables is crucial. In this study, we further evaluate the potential of δ15N values in T. landbeckii as a proxy for present and past fog water availability as 2

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suggested by Latorre et al. (2011). We present a geographically and quantitatively extended δ15N-based data set on both living and dead T. landbeckii specimen collected along a 300 km coastal transect in northern Chile and evaluate the relationship with corresponding site factors such as latitude, elevation, Sc cloud properties as well as mean annual precipitation (MAP). We further investigate whether relict T. landbeckii layers buried in sand dunes preserve a record of environmental change during the late Holocene. Our new approach combining stable isotope, remote-sensing and modelling data will allow a more comprehensive description and understanding of these unique ecosystems and their links to atmospheric and oceanic processes in the subtropical eastern Pacific.

mountains at elevations of 900–1200 m a.s.l. between Arica and the Rio Loa Canyon (ca. 18.5°S–21.5°S) in March 2017 (Table 1). T. landbeckii is the predominant species of these lomas, but occasionally, T. virescens, T. capillaris and T. marconae coexist, in particular towards the northern range of occurrence close to the border with Peru. The communities are located at distances to the coast ranging from 3 km at Cerro Chipana to about 27 km at Quebrada Rio Loa (Fig. 1; Table 1). They form either dense units or sparse and isolated stands on W and SW facing slopes directly exposed to fog. We collected multiple specimen from each Tillandsia population to cover a range in elevation (total n = 72; Table S1). While the steep topography at Cerro Oyarbide and Cerro Chipana allowed us to sample across elevation ranges of about 130–180 m, north of Iquique only small patches of Tillandsia stands were found in a narrow range of elevations (Table S1). During the time of sampling, the population at Cerro Peninsula was practically dead but we were able to collect one living specimen. At Quebrada Vitor and Quebrada Rio Loa, only sparse small cushions of living plants were observed. At Quebrada Camarones and Cerro Pajonales, we also excavated two small sand dunes down to the underlying salt crust and sampled discrete layers composed of fossil Tillandsia plant remains. In addition, we sampled leaves of the sparse C3 vegetation present in the broader area including Huidobria fruticosa (Loasaceae) and Ophryosporus spp. (O. cf. anomalus, O. triangularis and O. paradoxus, Asteraceae; Table 2; Fig. S2). These plants occurred mostly below and above the fog zone either close to the coast or in deep canyons (termed quebradas), possibly in contact with groundwater. Upon return to the laboratory in Cologne, plant material was first rinsed with deionized water to remove surficial mineral dust and particles and then dried in a convection oven at 40 °C. Leaves and stems of each plant sample were ground and homogenized for elemental and stable isotope analysis.

2. Materials and methods 2.1. Study area and sampling strategy The Atacama Desert extends west of the central Andes between 15°S and 30°S across southern Peru and northern Chile (Houston and Hartley, 2003). The coastal Cordillera in northern Chile with elevations of approximately 1000–1600 m a.s.l. separates the narrow coastal plain from the broad Central Valley. The study area is located in the coastal range area of the Chilean Atacama Desert (Fig. 1). The climate is generally mild with uniform annual air temperature of 18.9 °C in Arica and 18.4 °C in Iquique, respectively (Schulz et al., 2011). Annual precipitation is extremely low (Arica: 1.6 mm, Iquique: 0.9 mm; Schulz et al., 2011) and rainfall is largely restricted to austral winter (Houston, 2006; Schulz et al., 2011). Summer precipitation becomes more dominant in the northern Andean zone accounting for ca. 30% of annual rainfall at Arica (Houston, 2006; Schulz et al., 2011). Fog occurs frequently along the coastal Cordillera when the massive marine Sc cloud deck that covers a large portion of the subtropical southeast Pacific approaches the coastal cliff. Advection of marine Sc air masses facilitate fog formation in the morning and evening/night, while changes in air circulation during the afternoon produces thermal stratification that dissipates fog (Muñoz et al., 2016; Lobos Roco et al., 2018). The maximum spatial extent of fog as exemplified in Fig. 2 typically occurs during the winter months from June to August (Cereceda et al., 2008; Muñoz et al., 2016). We surveyed nine of the largest currently known Tillandsia loma systems (Pinto et al., 2006; Latorre et al., 2011) located in the coastal

2.2. Elemental and stable isotope analysis Total organic carbon (TOC) and total nitrogen (TN) content of 2–3 mg decarbonized bulk plant material (mixture of both leaves and stems) were determined using an elemental analyzer (Vario MICRO cube, Elementar, Germany). Bulk plant carbon (δ13C) and nitrogen (δ15N) values were measured on a Thermo Fischer Scientific Flash Elemental Analyzer (EA) (1112 Series) interfaced with a Conflo IV to a Delta V Plus Isotope Ratio Mass

Fig. 2. GOES-16 image on (a) 31 July 2018 and (b) 12 March 2018 showing the Stratocumulus (Sc) clouds over the Pacific forming thick fog as they reach the coastal cliff (indicated by black arrows). 3

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Table 1 Location of major Tillandsia lomas systems in northern Chile reported in this study. No.a

Tillandsia lomas systemb

Sample locality

Latitude °S

Longitude °W

Elevation (m asl)

Distance inland (km)

1 2 3 4 5 6 7 8 9

Quebrada rio Lluta Quebrada Vitor Quebrada Camarones Cerro Guanacos Cerro Oyarbide Cerro Pajonales Cerro Peninsula Cerro Chipana Quebrada rio Loa

PCRUC QVIT QCAM CGUA COYA CPAJ CPEN CCHI QLOA

−18.48 −18.88 −19.07 −20.34 −20.53 −20.73 −21.18 −21.30 −21.41

−70.08 −70.12 −70.11 −70.03 −70.03 −69.97 −70.01 −70.03 −69.81

1000 1043 1100 1067 1157 1014 942 987 1028

23.6 22.4 20.8 12.7 15.7 23.3 10.0 4.5 27.5

a b

Site numbers refer to Fig. 1. After Pinto et al. (2006).

Spectrometer (IRMS). Isotope ratios were calculated and normalized using a number of in-house standards (i.e. peptone, atropine, nicotinamide) calibrated with IAEA-N1 (δ15N = +0.45‰), IAEA-N2 (δ15N = +20.41‰) and IAEA-N3 (δ15N = +4.72‰) reference material for nitrogen, and NBS22 (δ13C = −30.03‰) and IAEA CH-6 (δ13C = −10.46‰) for carbon. All analytical results are reported in δ notation, in per mil relative to the Vienna Pee Dee Belemnite (VPDB) for carbon and AIR for nitrogen. Reproducibility based on triplicate measurements was generally better than 0.2‰.

cloud mask pixels from the individual satellite overpasses, we defined a common 0.05° × 0.05° longitude by latitude grid. To determine the TCC for each grid cell, we divided the number of enclosed pixels marked “confident cloudy” or “probably cloudy” by the total number of enclosed pixels. Temporal averages of TCC offshore were calculated for a 15-year period (2003 to 2017) for the area between 71 and 70.5°W and 18–24°S. For each Tillandsia location on land, the value from the nearest grid cell was considered for comparison (Fig. 3). The diurnal cycle of the TCC recorded by the Terra and Aqua satellites during different times of the day is shown in Fig. S1 (ocean) and Fig. S2 (land). Offshore cloud heights were determined using the Multi-angle Imaging SpectroRadiometer (MISR) on the Terra satellite (Table S2). The cloud base height is retrieved from the MISR Level 2TC Cloud Product (MIL2TCSP; Diner, 2012), which provides cloud top heights, applying the MISR cloud base height (MIBase) algorithm of Böhm et al. (2019). MIBase is able to provide retrievals on a 0.25° × 0.25° longitude by latitude grid if the cloud scene meets some preconditions, such as the occurrence of cloud gaps. Among other processing steps, the 15th percentile was applied to the distribution of cloud top heights within a grid cell to retrieve the cloud base height. Furthermore, we retrieved the cloud top height analogous by changing this percentile to the 95th percentile. This way, the retrieval represents the maximum cloud top height rather than a mean cloud top height within each grid cell. Retrievals of cloud base heights and cloud top heights were averaged for a 17-year period (2001 to 2017) for the area between 71 and 70.5°W and 18–24°S.

2.3. Radiocarbon analysis Plant tissue (ca 30–70 mg) was prepared by standard alkali-acid extraction (AAA) followed by combustion and graphitization using an EAAGE system according to the protocol of Rethemeyer et al. (2019). Radiocarbon analysis was performed at the accelerator mass spectrometry (AMS) facility at the University of Cologne (CologneAMS), Germany. All radiocarbon ages were converted to calendar years before 1950 (cal years BP) using CALIB7.10 (Stuiver and Reimer, 1993) with the southern hemisphere SHCAL13 calibration curve (Hogg et al., 2013). 2.4. Remote sensing Total cloud cover (TCC) was derived from the Moderate Resolution Imaging Spectroradiometer (MODIS) Level 2 Cloud Mask product (35_L2; Ackerman et al., 2015). MODIS is installed on both Terra and Aqua satellites with overpass times of around 10:30 and 22:30 local time, and around 13:30 and 01:30 local time, respectively. The product provides a cloud mask at a 1 km horizontal resolution which distinguishes between “confident cloudy”, “probably cloudy”, “probably clear” and “confident clear”. To standardize the geolocation of the

2.5. Modelled precipitation data MAP is derived from a long-term simulation with the Weather Research and Forecasting (WRF) regional climate model v3.9 (Skamarock et al., 2018). The simulation covers the period 1982 to

Table 2 Location, elemental and stable isotope composition of selected C3 plant species reported in this study. Plant type/sample IDa

Lat °S

Long °W

Elevation (m asl)

Distance (km)

δ13C (‰)

δ15N (‰)

TOC (%)

TN (%)

C/N

Huidobria fruticosa SFB225 SFB211-19 SFB540 SFB537 SFB040

−19.33 −19.55 −20.95 −22.06 −24.29

−69.51 −70.19 −69.15 −70.16 −70.30

2445 35 1810 561 1795

79 1.5 106 3 24

−21.5 −23.2 −21.1 −25.7 −25.4

6.6 8.2 3.9 12.3 4.5

33.6 36.3 35.7 36.2 37.8

2.1 3.1 2.7 1.9 2.5

19 14 15 22 18

Ophryosporus spp. SFB080b SFB538c SFB501c SFB382-4c SFB375-1d

−21.41 −21.30 −22.43 −27.92 −29.93

−69.81 −70.03 −70.22 −70.85 −71.34

1028 1007 658 232 15

3.6 3.8 26.4 0 5

−23.5 −27.1 −23.2 −27.5 −28.6

6.5 7.5 6.1 17.0 9.8

45.1 41.9 45.5 44.3 46.0

2.2 1.9 2.7 2.3 2.3

24 26 19 23 23

a b c d

Voucher specimen of the plant samples are deposited at the herbarium BONN in Germany. O. cf. anomalus. O. triangularis. O. paradoxus. 4

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Fig. 3. Total cloud cover (a) day and (b) night averaged over a 15-year period from 2003 to 2017 using the Moderate Resolution Imaging Spectroradiometer (MODIS). Location of Tillandsia populations are indicated as black circles.

plants show higher nitrogen contents of 2–3% (Table 2), which may relate to the preferential uptake of mineral soil nitrogen species. C/N ratios of Huidobria fruticosa and Ophryosporus spp. range between 14 and 26 (Table 2) and are much lower compared to those of Tillandsia.

2017 using actual atmospheric conditions from the ERA-Interim reanalysis dataset (Dee et al., 2011). A horizontal resolution of 10 km is obtained using a double one-way nesting, and the model domain covers the area from approximately 26.0–16.5°S and 74.0–67°W. A detailed description of the model setup, including details to the used parameterisations, is given in Reyers et al. (2019, this issue). For each Tillandsia location on land, the value from the nearest grid cell was considered for comparison (Fig. 4). Simulated daily accumulated precipitation is freely available (Reyers, 2019).

3.2. Carbon (δ13C) isotope data The δ13C values of living Tillandsia plants range from −12.6‰ to −14.3‰ (Table 3). The δ13C values are in the typical range of CAM plants reported for the Atacama Desert (Ehleringer et al., 1998) and also confirm earlier findings of Latorre et al. (2011). Although the range of δ13C values from different sites is relatively small (1.6‰), a general trend towards more enriched values farther inland is observed (r = 0.6; p = .09; n = 8; Fig. S3) and may reflect the increasing aridity with increasing distance to the coast. δ13C values range from −21.5‰ to −25.7‰ in Huidobria fruticosa and from −23.2‰ to −28.6‰ in Ophryosporus spp. (Table 2). The average δ13C value of −24.7‰ is slightly higher than the global average of −27‰ for C3 plants, consistent with a higher water use efficiency displayed by desert C3 plants (Ehleringer et al., 1998; Quade et al., 2007). While the more negative values can be related to higher humidity either in the fog zone or close to the ocean, positive δ13C values are consistent with most arid conditions above the fog zone.

2.6. Environmental reference data The environmental data used in this study, i.e., sea surface water mean annual temperature as well as dissolved inorganic nutrients (nitrate, phosphate, silicate) concentrations were extracted from the World Ocean Atlas (WOA13) data set (Garcia et al., 2013; Locarnini et al., 2013). We used southern hemisphere seasons as defined by the WOA09, i.e., summer: January–March, autumn: April–June, winter: July–September, spring: October–December. 3. Results 3.1. Elemental data

3.3. Nitrogen (δ15N) isotope data

Site-averaged TOC values of Tillandsia plants are generally high ranging from 29% to 45% (Table 3). Low TN values of 0.3–0.7% show little variation between the sites except for the northernmost population (Quebrada rio Lluta) with a higher TN content of 1.4%, which may relate to high nitrogen input from fog (González et al., 2011). C/N ratios vary between 36 and 119 (Table 3) and are in the lower range of those previously reported for Tillandsia. The values may reflect the seasonal variation in nutrient ratios that are generally lowest in autumn (González et al., 2011). This is in agreement with the time of our sampling campaign in March. TOC values of the relict Tillandsia plants range between 30.4% and 38.7% at Quebrada Camarones and 41–43% at Cerro Pajonales (Table S1). TN values at both sites are low (0.2–0.4%) and C/N values are also in a similar range. Average TOC values of Huidobria fruticosa and Ophryosporus spp. plant material are 35.9% and 44.6%, respectively (Table 2). These

The site-averaged δ15N values of living Tillandsia plants range from +2‰ at Cerro Peninsula to −16‰ at the northernmost site Quebrada rio Lluta (Table 3). This spread of δ15N values is considerably larger than previously reported (Evans and Ehleringer, 1994; Latorre et al., 2011). The difference in δ15N values at each site is about 4.5‰ at Cerro Chipana (Fig. 6; Table S1). δ15N values of dead plants are in general more enriched in 15N compared to living specimen at the same site accounting for 3–4‰ (Fig. 7; Table S1). The δ15N values of relict Tillandsia plants at Quebrada Camarones range from −3‰ at the base to −9‰ at the dune crest (Table 4). A Cerro Pajonales, δ15N values of the fossil plant remains range from −2‰ at the base to −4‰ at the top of the small dune (Table 4). The δ15N values of Huidobria fruticosa and Ophryosporus spp. vary between 4‰ and 17‰ (Table 2) with a mean of 8‰ and are in extreme 5

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contrast to those of T. landbeckii. The exclusively positive δ15N values of these C3 plants are in the range of values reported for the coastal Atacama and in agreement with values known from water-limited systems (Evans and Ehleringer, 1994; Díaz et al., 2016). 3.4.

14

C-based chronology

The dune profiles at Cerro Pajonales and Quebrada Camarones contain 4–7 discrete layers of T. landbeckii remains and reveal a clear trend of increasing age with increasing depth from the dune crest (Fig. S4; Table 4). Layers P1-5 and P1-6 at Quebrada Camarones were more or less interwoven and also reveal similar ages (Fig. S4; Table 4). The 14 C age of the basal layer indicates that dune growth started at 2560 cal years BP at Quebrada Camarones. At Cerro Pajonales, dune growth started about 919 cal years BP ago (Table 4). Dead T. landbeckii remains collected at a dune surface at Quebrada Rio Loa revealed a median 14C age of 182 cal years BP (Table 4). 4. Discussion 4.1. Modern distribution of δ15N values in fog-dependent Tillandsia ecosystems The vast spread in δ15N values from −17‰ to +2‰ observed in living T. landbeckii specimen is unusual and has to the best of our knowledge not been reported so far in any terrestrial plants (Fig. 5; Table S1). At large spatial scales, foliar δ15N values seem to reflect water availability of an ecosystem. Global surveys of terrestrial vegetation showed decreasing δ15N values with increasing mean annual rainfall (Handley et al., 1999; Amundson et al., 2003; Swap et al., 2004; Craine et al., 2009). According to these global studies, foliar δ15N values of −8‰ relate to areas with annual rainfall > 2000 mm. In our study area, precipitation is extremely low (< 2 mm/yr; Fig. 4) and is not believed to differ notably along the investigated transect (Schulz et al., 2011). In contrast, fog has been shown to influence hydrology and nutrient cycling of coastal desert ecosystems in Chile and South Africa (Weathers et al., 2000; Soderberg, 2010; González et al., 2011; Eckardt et al., 2013). A study from the hyperarid Namib Desert indicated an apparent reversal of the global trend in foliar δ15N below a certain precipitation threshold at sites close to the coast, where fog frequently occurs (Soderberg, 2010). Thus, the availability of fog water, which is often exceeding water input provided by precipitation, seems to control the occurrence of sparse vegetation adapted to extremely low resources such as T. landbeckii in northern Chile (Rundel et al., 1991; Weathers et al., 2000; Pinto et al., 2006; Westbeld et al., 2009; González et al., 2011). The strong reliance of T. landbeckii on atmospheric nitrogen sources via fog water deposition may have led to the evolution of a high N use efficiency as suggested by high C/N ratios (Table 3; González et al., 2011). These are in strong contrast to C/N values of C3 plants with access to soil-derived nutrients (Table 2; Díaz et al., 2016).

Fig. 4. (a) Estimates of mean annual precipitation (MAP) derived from the Weather Research and Forecasting (WRF) model (Reyers et al., 2019; Reyers, 2019) and (b) MAP at the specific Tillandsia locations along the coastal Cordillera (grey circles). Black diamonds indicate MAP recorded over a 30-year period (1971–2000) at Arica and Iquique, respectively (Schulz et al., 2011).

Table 3 Site-averaged stable isotope and elemental composition of living Tillandsia landbeckii dune ecosystems. No.a

Sample locality

Latitude °S

Elevation (m asl)

Distance inland (km)

δ15N (‰)

δ13C (‰)

TOC (%)

TN (%)

C/N

1 2 3 4 5 6 7 8 9

PCRUC QVIT QCAM CGUA COYA CPAJ CPEN CCHI QLOA

−18.48 −18.88 −19.07 −20.34 −20.53 −20.73 −21.18 −21.30 −21.41

1000 1043 1100 1067 1157 1014 942 987 1028

23.6 22.4 20.8 12.7 15.7 23.3 10.0 4.5 27.5

−16.1 −9.1 −7.7 −5.0 −1.6 0.8 2.1 0.1 1.0

−13.0 −13.4 −13.1 −13.3 −14.3 −12.6 −13.2 −13.9 −12.9

45 38 29 38 41 39 33 39 37

1.4 0.5 0.3 0.4 0.4 0.5 0.5 0.6 0.7

36 97 104 119 106 97 83 79 64

a

Site numbers refer to Fig. 1.

6

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Table 4 Radiocarbon ages and δ15N values for buried T. landbeckii layers at Quebrada Camarones and Cerro Pajonales and dead specimen at Quebrada Rio Loa. Radiocarbon Lab ID (COL #)a

δ15N (‰ vs AIR)

Fraction modern (F14C)

14

Quebrada Camarones (QCAM: −19.066278, −70.090361; 1133 m a.s.l.) 4878.1.1 QC1–7 1 4877.1.1 QC1–6 8 4876.1.1 QC1–5 15 4875.1.1 QC1–4 27 4874.1.1 QC1–3 40 4873.1.1 QC1–2 50 4728.1.1 QC1–1 65

−8.9 −7.4 −4.7 −5.8 −6.6 −6.7 −3.0

0.953 0.916 0.921 0.896 0.860 0.784 0.732

± ± ± ± ± ± ±

0.004 0.004 0.004 0.004 0.004 0.004 0.003

385 ± 34 709 ± 36 661 ± 35 885 ± 37 1212 ± 35 1960 ± 38 2511 ± 32

322–489 559–671 550–654 677–802 978–1178 1781–1933 2379–2716

Cerro Pajonales (CPAJ: −20.733278, −69.971111; 967 m a.s.l.) 5004.1.1 CP1–1 25 5005.1.1 CP1–2 42 5006.1.1 CP1–3 55 4726.1.1 CP1–4 85

−4.3 −3.9 −1.9 −1.6

0.969 0.957 0.897 0.878

± ± ± ±

0.007 0.004 0.004 0.003

250 ± 57 351 ± 37 876 ± 38 1049 ± 31

133–331 302–470 674–801 804–962

Quebrada Rio Loa (QLOA: −21.409806, −69.810917; 1051 m a.s.l.) 5343.1.1 QLOA-1 0

2.3

0.976 ± 0.004

197 ± 34

134–292

Sample ID

Depth dune (cm)

C age (yrs BP)

Calibrated

14

C age (cal yrs. BP)b

a

COL (Cologne AMS, University of Cologne, Germany). Radiocarbon ages were calibrated using Calib 7.10 (Stuiver and Reimer, 1993) and the southern hemisphere SHCAL13 calibration dataset (Hogg et al., 2013). 2sigma probability ranges are reported. b

Fig. 6. Elevational changes in δ15N values of living T. landbeckii at Cerro Chipana (black dots) and Cerro Oyarbide (grey triangles).

Fig. 5. δ15N values in different Tillandsia populations (living: grey boxes; dead: white box). Box plots show median (horizontal line inside the box), upper and lower quartiles (boxes), and maximum and minimum values (vertical lines), in addition to any outliers, i.e. values that exceed the fifth or ninety-fifths percentile (black circles).

A clear trend is also observed in δ15N values and latitude (Fig. 7; Table S3), overall reflecting slightly increasing moisture along the investigated transect (Fig. 4). Available data on fog water amount and fog δ15N values (Fig. 6) are sparse and associated with large errors (González et al., 2011; Latorre et al., 2011). This could be due to differences in fog intensity and frequency on a seasonal or even daily scale (Cereceda et al., 2008). However, our δ15N values derived from bulk plant tissue most likely average fog water supply over several years or even decades. Therefore, longer-term climate observation may help to explain the observed trend in δ15N values. In this study, we used satellite-based MODIS (Ackerman et al., 2015) and MISR products (Diner, 2012; Böhm et al., 2019) to assess cloud cover and cloud height, respectively, averaging 15–17 years of observations (Table S2; Figs. S1, S2). δ15N values of Tillandsia plants show significant correlations with the Sc cloud cover (night-morning) over the ocean (r = −0.94, p < .001) as well as over land at any specific Tillandsia site (r = −0.90, p < .01) most likely representing fog (Figs. 8a, 9c). Moreover, foliar δ15N values reveal a significant relationship with Sc cloud height (Fig. 8b). Therefore, the nitrogen isotopic composition in Tillandsia plants may be largely controlled by cloud properties, and by

The general link between fog water amount, site elevation and foliar δ15N values in T. landbeckii was first indicated by Latorre et al. (2011). Their study suggested that the position of the different Tillandsia stands within the marine Sc cloud is critical for moisture supply (Cereceda et al., 2008; Garreaud et al., 2008). In a first approach, we examined the proposed relationship between elevation and δ15N values in T. landbeckii at Cerro Oyarbide and Cerro Chipana, respectively, where the steep topography allowed sampling across a 130–180 m range in elevation (Table S1). Our results indicate changes of approximately 4.5‰ within one site that can be related to changes in altitude (Fig. 6). Lowest δ15N values detected at the highest elevation sites likely reflect the maximum water content at the top of the cloud deck (Cereceda et al., 2008; González et al., 2011; Latorre et al., 2011) in agreement with the prediction of Latorre et al. (2011). Our site-averaged δ15N values are also in the same range of δ15N values previously reported for fog water and T. landbeckii at the same or nearby sites, respectively (Fig. 7; Latorre et al., 2011). 7

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be less important for deeply rooted plants (Soderberg, 2010). Instead, the distribution of Huidobria fruticosa and Ophryosporus spp. may rather depend on rainfall and groundwater availability. Most studies of ground water with high nitrate concentrations such as in the Atacama found enriched δ15N values of up to 20‰ (Coplen et al., 2002). In addition, nitrate from sea-spray could represent a source of nitrogen for the C3 plants close to the coast (Table 2) as has been reported for C4 and CAM plants along the coast of Namibia (Heaton, 1987). To further explore potential marine nitrogen sources, we compared site-averaged δ15N values of T. landbeckii with available nutrient concentrations from the adjacent surface ocean across the same latitudinal transect (Garcia et al., 2013). Interestingly, we found a significant correlation between δ15N values and NO3− (possibly also NO2−) and PO43− concentration (Table S3) during austral summer (Jan-March) when primary production in the surface water is highest (Dale et al., 2018). Here, significant marine nitrogen input via cloud (fog) deposition (Weathers et al., 2000) during austral summer, that may have been altered chemically and isotopically when released from the ocean or by subsequent oxidation-reduction reactions in the atmosphere (Böhlke et al., 1997; Ewing et al., 2007) may help to explain the extremely 15Ndepleted values measured at the northernmost locations (Fig. S5). This however needs to be further investigated in future studies.

Fig. 7. Site-averaged δ15N values of living Tillandsia plants (black circles) and dead specimen (black crosses) along latitudinal transect together with previously published δ15N values of T. landbeckii (white triangles; average δ15N values of leave and stem material) and fog (grey diamonds) by Latorre et al. (2011). Error bars represent the spread in δ15N values at each site.

4.3. Past variations in fog availability based on relict T. landbeckii dunes In the previous sections, we showed that δ15N values in T. landbeckii is largely related to latitudinal changes in marine Sc cloud properties (i.e. cloud height and cloud cover) and precipitation (Fig. 9). We also showed that desiccated specimen carry nitrogen isotope signatures that are generally more 15N-enriched compared to their living counterparts. Therefore, we feel confident to use the δ15N composition preserved in relict Tillandsia dunes as a proxy for past changes in water availability, i.e. as fog, dew or rain. We investigated two relict dunes which are more abundant further inland, i.e. Quebrada Camarones and Cerro Pajonales (Fig. S4; Table 4). Distinct layers of fossil plant material buried in the dunes suggest multiple episodes of plant growth and extinction in the past. Radiocarbon ages indicate that these ecosystems established about 2500 years ago at Q. Camarones (Table 4). The basal age of this dune is in a similar range as reported for dunes at Q. Vitor and C. Pajonales (Latorre et al., 2011) indicating climate conditions favoured dune establishment during that time interval. Changes in δ15N values of about 6‰ recorded at this specific site indicate significant changes in fog water supply during the past 2500 years (Fig. 10b; Table 4). In contrast, dune growth at C. Pajonales started about 1000 years ago when other dunes of the same T. landbeckii system became extinct (Latorre et al., 2011). This suggests that local changes in water availability may regulate dune growth or extinction on a small spatial scale. Both records indicate dry conditions during a time interval between approximately 1200 and 800 cal years BP (Fig. 10). This coincides with a period in the past during which extreme long-lasting droughts were reported, i.e. the Medieval Climate Anomaly (MCA) (Mann et al., 2009; Graham et al., 2011). The MCA stands out as a period of reduced precipitation and cool SSTs (2–3 °C less than modern) in the tropical eastern Pacific, thus is comparable with modern La Niña-like conditions (Graham et al., 2011). This is indicated by a marine record off southern Peru, where the lithic content, a proxy for El Niño floods, showed minimum continental sediment input (Fig. 10a; Rein et al., 2004). As a consequence, lowering of the cloud base or less frequent/intense fog events along the Chilean coast may have caused the 15N-enriched values observed in our records. A trend towards wetter conditions and thus increased continental runoff (Fig. 10a) following the MCA is also seen in our dune records (Fig. 10bc). Interestingly, both dunes indicate a similar amplitude of change in δ15N (2–3‰) pointing to a synchronous response to changing climate conditions. Centennial-scale changes may relate to internal El Niño/ Southern Oscillation (ENSO) dynamics during the late Holocene (Moy

inference fog intensity, reflecting increasing water availability along a S-N gradient (Fig. 9; Table S3). This is also indicated by MAP estimates based on the WRF Model (Fig. 4; Reyers et al., 2019). Even though changes in MAP are very small along the investigated transect, a significant correlation (r = −0.98, p < .001) is observed with our siteaveraged δ15N values (Fig. 8c; Table S3). The relationship between cloud cover (fog) and precipitation with δ15N values observed in both living and dead T. landbeckii specimen suggests that conditions become increasingly water limited. In agreement with this observation, the dead population at Cerro Peninsula shows the most enriched δ15N values (Fig. 5). Also, differences in δ15N values between living and dead specimen of the same Tillandsia system that account for on average 1–4‰ (Fig. 7, Table S1) indicate that water limitation may have caused 15N enrichment, in consensus with global observations (Handley et al., 1999; Amundson et al., 2003; Swap et al., 2004; Craine et al., 2009). 4.2. Marine vs soil nitrogen sources The contrasting δ15N patterns between Tillandsia (−16‰ to +2‰; Table 3) and Huidobria fruticosa and Ophryosporus spp. (+4‰ to +20‰; Table 2) observed in our study area was unexpected and the absolute range in δ15N values of almost 40‰ indicate nitrogen cycling in the Atacama Desert is at the extremes (Fig. S6). This also suggests that the nitrogen cycle of Tillandsia is largely different from that of C3 plants, whose δ15N values integrate multiple processes (i.e. ammonification, nitrification, and denitrification) in the soil, each associated with distinct fractionation effects (Evans and Ehleringer, 1994; Handley et al., 1999; Amundson et al., 2003; Díaz et al., 2016). As discussed in the previous section, this difference could relate to fog nitrogen inputs and different δ15N dynamics (Soderberg, 2010). In coastal regions, the relative nutrient availability appears to be related to water availability, i.e. cloud, fog, sea spray (Weathers et al., 2000; Swap et al., 2004; González et al., 2011). The observed latitudinal trend in δ15N values in our study could thus be explained by a higher marine nutrient load transported and deposited via clouds (fog) and precipitation (Figs. 4, 9). This scenario agrees with a higher aerosol content of water droplets in coastal fog in southern Peru compared to Chile (Rundel et al., 1991). In contrast, fog as a significant source of water and nutrients is thought to 8

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Fig. 8. Cross plots showing the relationship between site-averaged δ15N values of living Tillandsia (a) cloud cover during night-morning over ocean (r = −0.94; p < .001) and land (r = −0.90; p < .01), (b) cloud height base/top (r = −0.93; p < .001), and (c) mean annual precipitation (MAP; r = −0.98; p < .001) derived from the Weather Research and Forecasting (WRF) model (Reyers et al., 2019; Reyers, 2019).

et al., 2002; Rein et al., 2004). Our Tillandsia-based paleo-moisture archives have a rather low resolution. However, both dunes indicate plant growth on centennial timescales starting at about 1000 years ago pointing to a change in fog or rainfall frequency before and after the MCA (Fig. 10b, c). Both records may largely reflect changes in water supply during periods of low and high ENSO frequency as suggested from lake and sediment records (Moy et al., 2002; Rein et al., 2004). Accordingly, distinct layers of T. landbeckii may relate to ENSO-driven precipitation extremes occurring over longer time intervals. During the past decades, a distinct cooling has been observed within the marine boundary layer (MBL) which is consistent with a cooling trend in SST off the coast of northern Chile (Falvey and Garreaud, 2009). An intensification of the South Pacific Anticyclone was proposed as a major driver for the observed regional cooling in a warming world (Falvey and Garreaud, 2009; Cai et al., 2012). As properties of the marine Sc are strongly influenced by SST, an effect on the distribution and frequency of fog can be expected (Lobos Roco et al., 2018). This implies changes in the height and thickness of the Sc cloud deck and thus the amount of water available at a specific site. Recent observations indicate lowering of the cloud layer of about 200 m in Antofagasta since the 1990s (Quintana and Berrios, 2007). If this trend continues in

the future, it may also impact the active Tillandsia systems further north that are currently located well within the fog zone (Fig. 9e). In addition, cloud cover and cloud thickness also have major impacts on the radiative properties of the clouds (Boucher et al., 2013). A constant decrease of total cloud cover over Arica has been observed over the past decades with −35% annual frequency (Schulz et al., 2011). This implies a reduction of area where the vegetation is protected by the cloud cover from the impact of intense direct solar radiation. Extended dry periods in combination with reduced cloudiness in the future will influence the water balance of the plants likely leading to extreme dehydration and possibly extinction. Our results derived from fossil Tillandsia systems indicate that multiple episodes of plant growth and dieback already occurred at least during the past 2500 years. 5. Conclusions In this study, we used a comprehensive modern data set of δ15N values in T. landbeckii as a measure of fog water availability along the coastal Cordillera in northern Chile. The occurrence and spatial distribution of the different Tillandsia systems can be readily explained by their position within the marine Sc cloud/fog zone and local 9

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Fig. 9. Latitudinal transect of (a) site-averaged δ15N values of T. landbeckii, (b) mean annual precipitation (MAP) based on the WRF model (Reyers et al., 2019; Reyers, 2019), (c) total cloud cover during nightmorning (MODIS product) at each Tillandsia site, (d) mean annual sea surface temperature (Locarnini et al., 2013), (e) Stratocumulus cloud base (blue) and top (red) height along the coast of northern Chile (MISR product). Black circles indicate location of Tillandsia loma system 1–9; black bars indicate elevation range of T. landbeckii; grey area at the bottom is the coastal topographic profile (average height in between sampling sites along coast). Several deep canyons (quebradas) intercept the coastal topography allowing fog permeation inland. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

topography. Site-specific variations in δ15N values seem largely related to changes in altitude and thus water availability within the fog zone. Our site-averaged δ15N values also indicate a direct link to the marine Sc cloud, precipitation and likely fog along the coastal transect. The spread of δ15N values observed in our study was larger than expected given that climatic variables (i.e. precipitation, air temperature) are

relatively homogenous in the study area. The extremely 15N-depleted values in T. landbeckii were also in contrast to what is expected from water-limited systems globally but also from C3 plants such as Huidobria fruticosa and Ophryosporus spp. in our study area, pointing to different drivers for the nitrogen isotopic signature. The highly productive upwelling waters off northern Chile may serve as a source of nitrogen Fig. 10. Paleo-moisture archives from Peru and Chile for the last 2500 years. (a) marine record of El Niño flood sediments off Peru derived from lithic content (Rein et al., 2004). δ15N values of fossil T. landbeckii remains at (b) Quebrada Camarones and (c) Cerro Pajonales. Black symbols indicate δ15N values of modern specimen at the specific site. Grey bar indicates the extent of the Medieval Climate Anomaly, a known period of extreme droughts (Rein et al., 2004; Graham et al., 2011).

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species sustaining plant growth under generally nutrient-poor conditions. The suggested marine-terrestrial transfer of 15N-depleted nitrogen species via cloud deposition thus warrants further research. Particularly, a better knowledge about the specific nitrogen sources and processes influencing the nitrogen isotopic composition is needed. We gave first insights on past changes in fog water availability based on fossil Tillandsia plant remains buried in sand dunes. These revealed multiple episodes of plant growth and extinction during the past 2500 years that may relate to ENSO anomalies. Comparison of δ15N values in relict plants compared with their modern counterparts indicate drier conditions during late Medieval times, but also suggest higher fog water supply during the more recent past. Our data also support recent observations pointing to increased aridity in northern Chile during the past decades.

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Acknowledgements We thank Madalina Jäggi for help with isotope analysis, and Lana John, Ulrike Patt and Stefan Heinze for radiocarbon analysis. We also thank two anonymous reviewers for their constructive comments on the manuscript. This study was part of the CRC 1211 ‘Earth – Evolution at the dry limit’ subproject D04 supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) under Grant 268236062 – SFB 1211. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.gloplacha.2019.103029. References Ackerman, S., Menzel, P., Frey, R., Baum, B., 2015. MODIS atmosphere L2 cloud mask product. NASA MODIS adaptive processing system. Goddard Space Flight Centerhttps://doi.org/10.5067/MODIS/MOD35_L2.006. Amundson, R., Austin, A.T., Schuur, E.A.G., Yoo, K., Matzek, V., Kendall, C., Uebersax, A., Brenner, D., Baisden, W.T., 2003. Global patterns of the isotopic composition of soil and plant nitrogen. Glob. Biogeochem. Cycles 17 (1), 1031. Benzing, D.H., Renfrow, A., 1971. Significance of the patterns of CO2 exchange to the ecology and phylogeny of the Tillandsioideae (Bromeliaceae). Bull. Torrey Bot. Club 98, 322–327. https://doi.org/10.2307/2483971. Benzing, D.H., Seeman, J., Renfrow, A., 1978. The foliar epidermis in Tillandsioideae (Bromeliaceae) and its role in habitat selection. Am. J. Bot. 65, 359–365. https://doi. org/10.2307/2442278. Böhlke, J.K., Ericksen, G.E., Revesz, K., 1997. Stable isotope evidence for an atmospheric origin of desert nitrate deposits in northern Chile and southern California, U.S.A. Chem. Geol. 136, 135–152. Böhm, C., Sourdeval, O., Mülmenstädt, J., Quaas, J., Crewell, S., 2019. Cloud base height retrieval from multi-angle satellite data. Atmos. Meaurs. Tech. 12, 1841–1860. Boucher, O., Randall, D., Artaxo, P., Bretherton, C., Feingold, G., Forster, P., Kerminen, V. M., Kondo, Y., Liao, H., Lohmann, U., Rasch, P., Satheesh, S., Sherwood, S., Stevens, B., and Zhang, X., 2013. Clouds and Aerosols, in: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change, Stocker, T., Qin, D., Plattner, G.K., Tignor, M., Allen, S., Boschung, J., Nauels, A., Xia, Y., Bex, V., Midgley, P., chapter 7, 571–657, Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 2013. Cai, W., Lengaigne, M., Borlace, S., Collins, M., Cowan, T., McPhaden, M.J., Timmermann, A., Power, S., Brown, J., Menkes, C., Ngari, A., Vincent, E.M., Widlansky, M.J., 2012. More extreme swings of the South Paci c convergence zone due to greenhouse warming. Nature 488, 365–369. Cereceda, P., Larrain, H., Osses, P., Farías, M., Egaña, I., 2008. The spatial and temporal variability of fog and its relation to fog oases in the Atacama Desert, Chile. Atmos. Res. 87, 312–323. Coplen, T.B., Hopple, J.A., Böhlke, J.K., Peiser, H.S., Rieder, S.E., Krouse, H.R., Rosman, K.J.R., Ding, T., Vocke, R.D.J., Révész, K.M., Lamberty, A., Taylor, P., DeBièvre, P., 2002. Compilation of Minimum and Maximum Isotope Ratios of Selected Elements in Naturally Occurring Terrestrial Materials and Reagents. United States Geological Survey, Reston, pp. 98. Craine, J.M., Elmore, A.J., Aidar, M.P.M., Bustamante, M., Dawson, T.A., Hobbie, E.A., Kahmen, A., Mack, M.C., McLauchlan, K.K., Michelsen, A., Nardoto, G.B., Pardo, L., Peñuelas, J., Reich, P.B., Schuur, E.A.G., Stock, W.D., Templer, P.H., Virginia, R.A., Welker, J.M., Wright, I.J., 2009. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol. 183, 980–992. Dale, A.W., Bourbonnais, A., Altabet, M.A., Wallmann, K., Sommer, S., 2018. Isotopic fingerprints of benthic nitrogen cycling in the Peruvian oxygen minimum zone.

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