Climatic variability as a principal driver of primary production in the southernmost subalpine Rocky Mountain lake

ABSTRACT

Mountain lakes are sensitive indicators of anthropogenically driven global change, with lake sediment records documenting increased primary production during the twentieth century. Atmospheric nutrient deposition and warming have been attributed to changes in other Western mountain lakes, however, the intensity of these drivers varies. We analyzed a sediment core representing a 270-year record from Santa Fe Lake, New Mexico, to constrain the southern margin of Rocky Mountain lakes and quantify patterns of change in lake biogeochemistry, production, and diatoms since 1750. Lake sediments were dated using ²¹⁰Pb and analyzed for carbon (C), nitrogen (N), stable isotopes (δ¹³C, δ¹⁵N), diatoms, and phototrophic pigments. The abundance of cyanobacteria, purple sulfur-reducing bacteria, and diatom pigments were elevated during the stable conditions of the Little Ice Age; these phototrophic groups declined in the late 1800s and reached a minimum by 1950. From 1950 to 2020, sediments recorded an increased abundance of cryptophyte, diatom, and chlorophyte groups. The C and N (percentage dry mass) increased after 1950, whereas δ¹⁵N and δ¹³C values declined. Changes since the mid-twentieth century are contemporaneous with warming trends in the Southwest and modest deposition of atmospheric N. Our findings highlight the geographic variability of mountain lake responses to changing environmental conditions.

Highlights

• Fossil phototrophic and diatom pigments revealed elevated primary production resulting from increases in cyanobacteria, purple sulfur bacteria, and diatoms during the stable conditions of the Little Ice Age.

• Primary production declined from the end of the Little Ice Age into the mid-twentieth century.

• The warming climate after ca. 1950 and, to a lesser extent regional N deposition, drove primary productivity to a historic maximum due to increased chlorophyte and cryptophyte groups.

• Unlike other Rocky Mountain lakes, regional human activities had little effect on the phototrophic composition and productivity of Santa Fe Lake.

KEYWORDS:

• Rocky Mountains
• subalpine lake
• mountain lakes
• climate
• fossil pigments
• stable isotopes
• diatoms
• nitrogen deposition
• Little Ice Age

Introduction

Anthropogenic drivers of global change, such as fossil fuel and fertilizer use, greenhouse gas emissions, nonnative species introductions, and widespread land use modifications, have brought about considerable changes to ecosystems worldwide. Exponential increases in both the human-caused drivers and responses of ecosystems have been termed the “Great Acceleration” (Steffen et al. 2015) due to the unprecedented rates of social and ecological transformation after ca. 1950. Mountain lake catchments in North America are often protected from direct modifications associated with hydrological or land use changes due to their remote locations. As a result, climate variability and atmospheric deposition have been suggested as principal controls of ecological change in alpine and subalpine lakes, although relatively few direct comparisons of human and climate controls exist (Catalan et al. 2013; Moser et al. 2019).

Many mountain lakes have been altered by atmospheric inputs of nutrients, elevated climatic variability, lengthening of the ice-free season, and increased air and water temperatures beginning in the twentieth century (Baron et al. 2000; Saros et al. 2011; Slemmons and Saros 2012; Jeppesen et al. 2014; Williamson et al. 2016). Nearly all mountain lakes have additionally been stocked with nonnative fish (Leavitt et al. 1994). This suite of changes has altered nitrogen-to-phosphorus ratios (Elser et al. 2009) and stimulated increases in primary productivity in historically oligotrophic lakes, particularly in lakes in Colorado, Wyoming, Montana, Utah, and Washington (Saros et al. 2003; Hundey et al. 2014; Sheibley et al. 2014; Spaulding et al. 2015; Oleksy et al. 2020). Lake sensitivity to anthropogenic disturbances depends on complex interactions between external and internal lake processes that vary in space and time (Schindler 2001; Burpee et al. 2022). Consequently, whereas some mountain lakes exhibit unprecedented elevated production resulting from increased nutrient deposition, climate warming, or fish stocking (Leavitt et al. 1994; Wolfe, Baron, and Cornett 2001; Oleksy et al. 2020), others have shown more modest historical changes (Hundey et al. 2014; Spaulding et al. 2015). Little is known of the effects of climate and humans in mountain lakes at more southern locations in the Rocky Mountain Range (e.g., Schindler 2001). Because forcing by global changes will be modified through site-specific variation within lakes (morphometry, community composition, biogeochemistry) and external features (catchment characteristics, geographic location, land use), a better understanding of the geographic variability of lake responses to natural and anthropogenic agents is needed to develop effective plans for lake protection or mitigation (Hood, Williams, and Caine 2003; Adrian et al. 2009; Burpee et al. 2022).

Analysis of biological and biogeochemical components of lake sediments can reveal past ecological states and quantify trajectories of ecosystem change in mountain lake ecosystems (Leavitt and Hodgson 2001; Catalan et al. 2006; Adrian et al. 2009; Smol 2010). Paleolimnological studies of mountain lakes in Western North America have demonstrated the sensitivity of high-elevation sites to atmospheric deposition of nitrogen (N) (Wolfe, Baron, and Cornett 2001; Saros et al. 2011) and phosphorus ((P) (Brahney et al. 2014), climate and climate change (Hundey et al. 2014; Spaulding et al. 2015; Williams et al. 2016; Oleksy et al. 2020), terrestrial aquatic linkages (Bunting et al. 2010), and fisheries management (Leavitt et al. 1994; Schindler 2001).

We explored 270 years of geochemical and biological signals in the sediment record of Santa Fe Lake, the southernmost mountain lake in the Rocky Mountains. Prior studies from remote lakes in Montana, Wyoming, and Utah revealed muted changes in biogeochemical cycles and algal production during the transition from the end of the Little Ice Age (LIA, C.E. 1750–1880) into the twentieth century, followed by a marked increase in primary production and organic matter content (percentage dry mass) coincident with increases in regional and global anthropogenic activities (Slemmons and Saros 2012; Hundey et al. 2014; Burpee et al. 2022). Unlike lakes in mountain areas proximal to intensive agriculture and urbanization (e.g., Southern Sierra Nevada, Colorado Front Range), northern New Mexico has less agricultural, industrial, or urban development, resulting in lower atmospheric deposition of N and P (Diemer, Crawford, and Patrick 2012). Santa Fe Lake is historically fishless, removing the consideration of changes in nutrient cycling arising from food web modifications (Leavitt et al. 1994). We hypothesized that regional climate variability likely plays the predominant role in regulating lake production and biogeochemistry with little or no influence from atmospheric N or P deposition.

Study site

Santa Fe Lake (35.78878° N, −105.7781° W) is a small (surface area = 1.9 ha), shallow (6.5 m), transparent (Secchi depth ca. 6.5 m) subalpine lake (3,530 m.a.s.l.) situated in a small catchment (15.9 ha) located in the Pecos Wilderness area 28 km northeast of Santa Fe, New Mexico, USA (Figure 1). Santa Fe Lake lies in the headwaters of the Santa Fe River watershed and is the southernmost subalpine lake in the Rocky Mountains. We relied on previously published physical and chemical characteristics to describe lake features (Davis and Joseph 2007; Lynch et al. 1988; Table 1). Santa Fe Lake has a shallow (<1 m deep) and narrow littoral zone (extending 1–5 m from shore) that drops into deeper waters. Light penetrates to the bottom of the lake during the open water season (Table 1). Precambrian granite underlies the basin, causing Santa Fe Lake to have dilute waters with low acid-neutralizing capacity (Lynch et al. 1988). Water quality assessments conducted in 2007 classified Santa Fe Lake as oligo-mesotrophic according to Carlson’s (1977) indices for Secchi depth, chlorophyll a (Chl a), total phosphorus, total nitrogen, and algal community composition (Table 1).

Table 1. Santa Fe Lake site information.

Characteristic	Value	Source
Santa Fe Lake location	35.78884° N, −105.77804° W	Google Earth Pro, Davis and Joseph (2007)
Elevation (m)	3,530	Google Earth Pro, Lynch et al. (1988), Davis and Joseph (2007)
Max depth (m)	6.5	Davis and Joseph (2007)
Surface area (ha)	1.9	Lynch et al. (1988)
Basin area (ha)	15.9	Lynch et al. (1988)
Secchi disk depth (m)	6.5	Davis and Joseph (2007)
Dissolved oxygen^a (mg/L)	7.3	Davis and Joseph (2007)
Dissolved oxygen, bottom (mg/L)	1.2	Davis and Joseph (2007)
Temperature^a (°C)	16.35	Davis and Joseph (2007)
Temperature, bottom (°C)	14.43	Davis and Joseph (2007)
pH	7.7	Davis and Joseph (2007)
Conductivity (μS/cm)	22	Davis and Joseph (2007)
Turbidity (NTUs)	0.62	Davis and Joseph (2007)
Chlorophyll a (μg/L)	3.26	Davis and Joseph (2007)
Total phosphorus (mg/L)	<0.01	Davis and Joseph (2007)
Total nitrogen (mg/L)	0.35	Davis and Joseph (2007)
Limiting nutrient^a	Nitrogen	Davis and Joseph (2007)

Note. Lake physical–chemical characteristics are taken from reports generated by Davis and Joseph (2007) and from Lynch et al. (1988) during the open water season. The 2007 Davis and Joseph report is the product of a single sampling effort in the summer of 2007 and, as such, mean and standard deviation values are not available.

^aDissolved oxygen and temperature are mean values from the epilimnion (upper one-third of water column) and the hypolimnion (lower one-third of water column).

Figure 1. Map of study region (top left), local study area including (a) Santa Fe Lake (35.78878, −105.7781,3,530 m above sea level (a.s.l.)), (b) the city of Santa Fe, NM (35.68698, -105.93780, 2132 m a.s.l.), and (c) the NADP NM07 site at Bandelier National Monument (35.77917, -106.25492, 1,997 m a.s.l., bottom right), and aerial imagery of Santa Fe Lake (top right). Base map from Esri and its licensors, copyright 2023.

Methods

Field collection

A 49-cm sediment core was collected from the deepest part of Santa Fe Lake using a modified gravity corer on 21 September 2020 (Glew 1991). The core was extruded on-site in 0.5-cm increments from 0 to 40 cm and 1-cm increments for the bottom 9 cm. Samples were stored in the dark on dry ice during transport to Colorado State University.

Sediment preparation

Sediments were stored at −80°C before analyses at the EcoCore Laboratory at Colorado State University. Samples were weighed to acquire their wet mass and then freeze-dried until a constant mass was achieved, typically by 72 hours. Freeze-dried sediments were homogenized and subdivided into portions for ²¹⁰Pb activity, stable isotope analyses, elemental C and N, diatom species composition, and fossil pigments.

Lake core chronology

Freeze-dried, homogenized sediment samples were dated using ²¹⁰Pb alpha spectroscopy at the U.S. Geological Survey’s St. Petersburg Coastal and Marine Science Center. Chronologies were determined from fifteen 250-mg sediment samples dispersed throughout the core, with more samples analyzed in the top and bottom 2 cm of the core. Sediments were dated by analysis of ²¹⁰Pb activity and application of the constant rate of supply model (Appleby and Oldfield 1978). The tidypaleo package in R developed by Dunnington et al. (2022) was used to estimate calendar dates for the sediment core (Figure 2). This package allows for the interpolation of dates within known ages/depths and extrapolation using a linear fit of ages/depths (Dunnington et al. 2022).

Biogeochemical analyses

Carbon and N stable isotope values (δ¹⁵N, δ¹³C) and elemental composition of whole dried sediments were analyzed at the Institute of Environmental Change and Society, University of Regina, Saskatchewan, Canada. Approximately 30 mg of un-acidified sediment was analyzed using a ThermoQuest DeltaPLUS XL mass spectrometer equipped with a continuous flow unit (Con Flo II) and an automated Carlo Erba elemental analyzer as an inlet device following standard procedures (Bunting et al. 2010). Isotopic compositions of δ¹⁵N and δ¹³C were expressed in the conventional notation: units of per mil deviation from atmospheric N₂ and an organic C reference calibrated against an authentic Pee Dee Belemnite standard. Sample reproducibility exceeded 0.25 and 0.10 per mil for δ¹⁵N and δ¹³C determinations, respectively (Figure 3).

Diatom microfossil analyses

Diatom processing and analyses followed the methods of Pite et al. (2009). Permanent slides and cleaned material are archived in the University of Colorado INSTAAR Diatom Database (Accession Nos. 17500-17578). Diatom composition was documented using the voucher flora approach and diatom remains were identified to species (Figure 4; Bishop et al. 2017; Tyree et al. 2020; Shampain et al. 2023). Identification and autecological characterization followed Spaulding et al. (2021).

Algal pigments

Carotenoids, chlorophylls, and their derivatives were quantified at the Institute of Environmental Change and Society following standard procedures (Leavitt and Hodgson 2001). Briefly, ~ 50 mg of freeze-dried sediment was extracted in an acetone–methanol–water mixture (80–15–5, by volume) for 24 hours, filtered through a 0.2-µm pore membrane filter, and dried under N₂ gas. Before quantification, pigment residues were reconstituted in a known volume of standard injection solution and analyzed on an Agilent 1100 high-performance liquid chromatography system equipped with a photodiode array detector. Individual pigments were distinguished based on chromatographic position and light absorbance characteristics relative to authentic pigment standards from DHI and local isolates (Leavitt and Hodgson 2001). All pigment concentrations are presented as nanomoles pigment per gram total C, a metric that is linearly correlated to annual phototroph standing stock in whole lake calibrations (Leavitt and Findlay 1994).

A total of thirteen pigments were identified in the sediment core, although this study focused on the seven most common and taxonomically diagnostic compounds (Shampain et al. 2023; Figure 5, Table 2). These pigments included biomarkers from cryptophytes (alloxanthin), mainly diatoms (diatoxanthin), chlorophytes and cyanobacteria (lutein-zeaxanthin; isomers not resolved), total cyanobacteria (echinenone), Nostocales cyanobacteria (canthaxanthin), chlorophytes alone (pheophytin b), and purple sulfur bacteria (okenone; Figure 5). Pheophytin a, a chemically stable derivative of labile ubiquitous Chl a, was used as a proxy for total primary producer abundance. The ratio of Chl a to pheophytin a (preservation index) was used as a proxy for changes in down-core pigment preservation (Leavitt and Hodgson 2001).

Table 2. Model summary of generalized additive models (GAMs) for the detection of trends in all geochemical biomarkers, atmospheric deposition data, and phototrophic pigments in a sediment core representing a 270-year record from Santa Fe Lake, New Mexico. For each predictor, effective degrees of freedom (EDF), F-statistic, p-value, and adjusted R², and periods of significant change are shown.

Analyte	Effective degrees of freedom	F	p Value	Adjusted R^2	Period of change (−)	Period of change (+)
δ^13C	8.59	3.3	.00219	0.95	1962–2020
δ^15N	2.36	7.36	.00103	0.69	1945–2020
C (percentage dry mass)	16.1	140	<2e-16	0.96	1865–1884	1837–1851 1969–1988 1998–2020
N (percentage dry mass)	19.58	148	<2e-16	0.97		1968–1983 1999–2020
C:N	20.6	145.3	<2e-16	0.97	1962–1977 2000–2020
Total N	1.925	2.085	.0993	0.1
NH4-N	1.0	9.626	.00366	0.185	1983–2020
NO3-N	2.35	11.1	9.34e-05	0.406		2001–2017
SO4	1.639	68.06	<2e-16	0.75	1982–2020
Pheophytin a (total phototrophic abundance)	2.69	5.7	.00966	0.39		1968–2002
Pheophytin b (chlorophytes)	3.82	7.482	.00064	0.25		1966–2020
Lutein and zeaxanthin (chlorophytes and cyanobacteria)	1.0	42.48	<2e-16	0.383		1749–2020
Alloxanthin (cryptophytes)	5.64	13.38	<2e-16	0.70	1802–1810 1893–1911	1922–1931 1975–2014
Echinenone (cyanobacteria)	1.0	26.93	1.54e-06	0.30	1749–2020
Canthaxanthin (cyanobacteria)	3.94	12.84	<2e-16	0.51	1855–1919
Diatoxanthin (diatoms)	20.43	24.82	<2e-16	0.82	1749−1754 1775–1784 1898–1908 1994–2020	1920–1934 1973–1984
Okenone (photosynthetic bacteria)	6.06	27.74	<2e-16	0.70	1882–1931	1968–2020

Climate and atmospheric deposition data

Broad-scale climatic patterns were derived from a suite of available datasets. Average annual air temperatures were taken from temperature reconstructions derived from tree ring analyses of Wahl and Smerdon (2012) for the region bounded by 30° to 55° N and 95° to 130° W encompassing Western North America (Wahl et al. 2014). For finer resolution, average temperature and precipitation data at the 4 km grid cell level available from 1895 to 2020 were downloaded from the PRISM database (PRISM Climate Group, Oregon State University, https://prism.oregonstate.edu/explorer/, accessed 11/30/23; Figure 6). Precipitation records were omitted from analyses due to poor synchrony between the overlapping period of paleoclimatological precipitation records from El Malpais, New Mexico (Stahle et al. 2009), located approximately 250 km southwest of Santa Fe Lake, and PRISM data from 1895 to present. Instead, we interpreted precipitation trends from the Palmer Modified Drought Index (PMDI). Periods of dry and wet conditions were derived from estimates of PMDI from the Living Blended Drought Atlas v2 (Gille et al. 2017) at the 5 km grid cell level (https://www1.ncdc.noaa.gov/pub/data/paleo/drought/LBDP-v2/lbda-v2_pmdi_kddm_template.txt; accessed 11/30/23; Figure 6). Wet atmospheric deposition data (total N, NH₄, NO₃, and SO₄; 1983–present) were obtained from the National Atmospheric Deposition Program (NADP), National Trends Network site at Bandelier National Monument, New Mexico (NM07; (https://nadp.slh.wisc.edu/sites/ntn-NM07/; accessed 11/20/23). Site NM07 is located at 1,997 m.a.s.l. and approximately 45 km west of Santa Fe Lake (Figure 1 and Figure 6). This is the closest NADP site to Santa Fe Lake and represents a regional estimate of wet atmospheric deposition.

Statistical analyses

All statistical analyses were performed in RStudio R version 4.2.2. (R Studio 2022). Generalized additive models (GAMs; Hastie and Tibshirani 1987; Wood 2017) were employed to estimate trends response variables and identify significant periods of change in phototrophic pigments, biogeochemical data, and atmospheric deposition values (Table 2, Figures 3, 5 and 6). Models were fit using the gamm() function (Wood 2004) in the mgcv package (Wood 2017) and were parameterized following the technical recommendations of Elser et al. (2009) and methods of Oleksy et al. (2020). Hierarchical clustering analyses were created using the TidyPaleo R package and employed rioja analyses and were used to inform significant periods of change shared amongst the phototrophic and biogeochemical analytes (Figure 7; Dunnington et al. 2022; Juggins 2023). Fossil diatom data were omitted from the hierarchical analysis because of sampling irregularity in the mid-sections of the core.

Figure 2. Chronology for the Santa Fe Lake, New Mexico, sediment core representing a 270-year record. (a) Natural log of ²¹⁰Pb activity within the Santa Fe Lake sediment core, (b) Estimated age by depth for Santa Fe Lake sediments based on fifteen sediment samples dispersed throughout the core, with groupings in the first and final 2 cm of the core. Standard error bars and regions of extrapolation (dashed lines) are indicated.

Figure 3. Summary of temporal trends in biogeochemical signals from Santa Fe Lake, New Mexico, in a sediment core representing a 270-year record. The δ¹⁵N, δ¹³C, N (% dry mass), C (% dry mass), and C:N are plotted against the year. Values were fitted with a generalized additive model (GAM)-smoothing trend and 95% confidence interval. (a) δ¹⁵N of bulk sediments; (b) δ¹³C of bulk sediments; (c) nitrogen content as a percentage of dry mass; (d) carbon content as a percentage of dry mass; and (e) C:N ratio.

Figure 4. Santa Fe Lake, New Mexico, fossil diatom community data in a sediment core representing a 270-year record. (a) Relative abundance of common (≥ 2% of relative abundance) diatom species identified in the Santa Fe Lake Core, grouped by niche. (b) The proportion of planktonic, tychoplanktonic, and benthic taxa throughout the Santa Fe Lake Core.

Results

Chronology

The analyses of ²¹⁰Pb activities provided a reliable sediment chronology for Santa Fe Lake (Figure 2). Overall, ²¹⁰Pb activities declined in a monotonic fashion. The core was dated to ca. 1810 and extrapolated to ca. 1750 using the assumption of linear mass accumulation before the 1800s. Mass accumulation rates were similar through much of the core (0.039 ± 0.01 g/cm²/yr) other than a transient decline in deposition during ca. 1825 to ca. 1900.

Figure 5. Temporal trends in major algal functional groups inferred by pigment analyses. Generalized additive model (GAM)-smoothing trends fitted are depicted with 95% confidence intervals for all major algal pigments in the Santa Fe Lake, New Mexico, time series. Pheophytin a (a) is a proxy for total phototrophic abundance. Alloxanthin (b) is a proxy for total cryptophytes. Pheophytin b (c) is a proxy for total chlorophyte biomass. Lutein-zeaxanthin (d) is a proxy for chlorophytes and cyanobacteria. Echinenone (e) and canthaxanthin (f), and are proxies for cyanobacteria (total, and Nostocales, respectively). Diatoxanthin (g) is a proxy for total diatom biomass. Okenone (h) is a proxy for a purple sulfur-reducing photosynthetic bacteria.

Biogeochemistry

There was a decline in δ¹⁵N from 1750 to the present, with some variation over time. Values ranged from 1.9 to 1.1 per mil between ca. 1750 and ca. 1945 (Figure 3). The δ¹⁵N values then declined significantly from 1.2 per mil to the lowest value of −0.4 per mil in 2019 (Table 2, Figure 3). Bulk sediment δ¹³C enriched from −26.3 to −24.8 per mil from ca. 1775 to 1920. Steady depletion began post-1920, with a significant rate of depletion during ca. 1960 to 2020, where values decreased from −25.6 to 28.1 per mil (Table 2, Figure 3). Percentage C was relatively stable from ca. 1750 to 1830 with a mean value of 13.3 percent ± 0.1 (Figure 3). There was a small but significant increase in percentage dry mass of C during ca. 1837 to 1851 from 13.8 to 15.0 percent before a decline from 14.6 to 12.9 percent during ca. 1865  to 1884 (Table 2, Figure 3). Between ca. 1975 and 2020, C content increased from 12.4 to 23.6 percent (Figure 3). Sedimentary N content (percentage dry mass) remained stable from ca. 1750 to ca. 1900, with a mean value of 1.2 percent ± 0.01 that then declined slightly (ca. 0.2 percent) between ca. 1897 and ca. 1942 before significantly increasing during ca. 1968 to 1983 and 1999 to 2020 from 1.3 to 2.9 percent. The C:N ratio of Santa Fe Lake sediments was relatively stable around 12 throughout 1750 to 2000, before decreasing to 9 between 1950 and ca. 2000 (Table 2, Figure 3).

Diatom microfossils

The analysis of inorganic silica of diatom cells (Figure 5) indicated that species composition of the assemblage varied in accordance with changes in diatom abundance inferred from fossil pigments (see section “Algal Pigments - Diatoms”). Specifically, the relative abundance of the predominant taxon Staurosira construens var. venter (Ehrenb.) (Hamilton et al. 1992) was elevated both before ca. 1875 and more recently after ca. 1975. The timing of changes in Staurosirella pinnata (Ehrenb.) (D. M. Williams and Round 1987) was like that of S. construens var. venter, whereas other common taxa revealed few pronounced trends (Figure 4a). Siliceous cysts of scaled chrysophytes were also abundant in the core, particularly in older and more recent deposits. Tychoplanktonic species were overall in greatest relative abundance within the core and comprised 60 percent of the identified species, followed by benthic (21 percent) and then planktonic species (18 percent, Figure 4b). Tychoplanktonic taxa remained elevated throughout the record, whereas planktonic-associated taxa were in greater relative abundance pre-1900, and benthic-associated taxa increased post-2000 (Figure 4b).

Figure 6. Historical trends with 95% confidence intervals in environmental conditions and atmospheric deposition at Santa Fe Lake, New Mexico. (a) Palmer Modified Drought Index (PMDI) reconstructions at the 5km grid cell derived from the Living Blended Drought Atlas (Gille et al. 2017). (b) Variance in temperature from mean annual temperature. Temperature data derived from The Western North America 500-Year Annual Temperature Reconstruction (Wahl and Smerdon 2012) were used for the 1749-1894 period. PRISM average annual temperature data https://prism.oregonstate.edu/explorer/, at the grid-cell level (standard PRISM 4 km), were used for the period from 1895-2020, averages were calculated from each dataset respectively. Total N, NO₃- N, NH₄ - N (c) and SO₄ (d) deposition trends between 1982 and 2020 from the National Trends Network, Bandelier National Monument location (site NM007) maintained by the National Park Service and the National Atmospheric Deposition Program.

Algal pigments

Total phototrophic abundance

Total phototrophic abundance (as chemically stable pheophytin a) exhibited a mean concentration of 70.5 ± 2.9 nmol g⁻¹ organic carbon (OC) during ca. 1750 to 1800 and then declined during ca. 1800 to 1850 to reach its lowest level (~25 nmol g⁻¹ OC) in the early 1920s (Table 2, Figure 5). Beginning in the mid-1950s, phototrophic abundance increased steadily, resulting in an average concentration of 95.0 ± 6.0 nmol g⁻¹ OC in modern sediments (ca. 2007–2020) that exceeded all historic levels (Figure 5).

Chlorophytes and cryptophytes

High primary production during the past seventy years was largely due to chlorophytes (as lutein-zeaxanthin, pheophytin b) and cryptophytes (alloxanthin; Figure 5). Before ca. 1950, chlorophyte abundance had been relatively stable (pheophytin b) or declining slightly (lutein-zeaxanthin) until the early twentieth century (Table 2); however, pheophytin b levels increased to a mean of 182.0 ± 13.8 nmol g⁻¹ OC during 1950 to 2020 (Table 2, Figure 5). Similarly, the combined abundance of chlorophytes (lutein) and cyanobacteria (zeaxanthin) oscillated during the 1800s and early 1900s before increasing linearly to surface deposits, particularly after ca. 1925 (Figure 5). Values ranged from 60 to 185 nmol g⁻¹ OC. Cryptophytes (as alloxanthin) declined slightly but significantly from 1880 to 1915 before nearly tripling to 32 nmol g⁻¹ OC by 2020 (Table 2, Figure 5). Overall, the pattern of increases in chlorophytes and cryptophytes was like those observed for percentage C and percentage N content (Figures 2 and 5).

Diatom pigments

Diatoms (as diatoxanthin) were variable throughout the past 270 years (Table 2, Figure 5). The greatest concentrations of diatoxanthin (99.5 nmol g⁻¹ OC) occurred in the oldest layers of the sediment core ca. 1750 (Table 2, Figure 5). Fossil concentrations declined rapidly to 50 nmol g⁻¹ OC between 1800 and 1850 before declining further to a minimum of 19.3 nmol g⁻¹ OC ca. 1920. Diatom abundance increased to a peak of 77.5 nmol g⁻¹ OC ca. 1995 before declining again in the uppermost sediments (Figure 5).

Cyanobacteria and purple sulfur bacteria

Echinenone, a carotenoid representative of total cyanobacteria, declined irregularly throughout the fossil record from ca. 1750 to ca. 2020 (Table 2, Figure 5). Values ranged from 1.8 to 18.6 nmol g⁻¹ OC, with modern values exhibiting low concentrations. Concentrations of canthaxanthin, a biomarker of the potentially nitrogen-fixing family Nostocales, were stable during ca. 1750 to ca. 1825, before declining sharply until ca. 1950. Canthaxanthin rebounded to moderate levels in the most recent surface sediments (Table 2, Figure 5). Modern levels of canthaxanthin remained below historic maxima and averaged 5.5 ± 0.3 nmol g⁻¹ OC (Table 2, Figure 5). Concentrations of echinenone and canthaxanthin were an order of magnitude lower than those of chlorophyte biomarkers (lutein-zeaxanthin, pheophytin b), suggesting that chlorophytes, rather than cyanobacteria, dominated the phototrophic assemblages (Figure 5).

Okenone is a pigment representative of purple photosynthetic sulfur bacteria whose presence indicates an environment where illuminated and anoxic habitats overlap (Leavitt and Hodgson 2001). This pigment was most abundant early in the record from ca. 1750 to 1850, averaging 11.2 ± 0.7 nmol g⁻¹ OC, and then declined to 0.4 nmol g⁻¹ OC near 1950 (Table 2). From ca. 1965 to 2020, okenone concentrations increased to an average of 3.6 ± 0.5 nmol g⁻¹ OC (Table 2, Figure 5). Overall, okenone concentrations were much lower than those recorded in profoundly anoxic habitats (e.g., meromictic lakes; Leavitt and Hodgson 2001)

Temperature, drought, and atmospheric deposition trends

Temperatures have increased in northern New Mexico, with an average annual rate of increase of 0.02°C since ca. 1895 (PRISM 2023). This pattern aligns with temperature trends for the North American continent, which exhibits a steady increase over the interval encompassed by the core (Figure 6a). Post-1950 there was a marked tendency for more frequent and severe droughts (Figure 6b). Analyses of total N deposition revealed no change in nitrogen influx between 1983 and 2020, with deposition ranging from 0.7 to 1.9 kg·ha⁻¹·yr⁻¹ with an average value of 1.3 kg·ha⁻¹·yr⁻¹. Ammonia (NH₄-N) increased significantly between 1983 and 2020; values ranged from 0.24 to 0.84 kg·ha⁻¹·yr⁻¹ with an average of 0.55 kg·ha⁻¹·yr⁻¹ (Table 2, Figure 6c). Wet nitrate (NO₃-N) deposition declined significantly from 2001 to 2017, decreasing from 0.90 to 0.40 kg·ha⁻¹·yr⁻¹ (Table 2, Figure 6c). NO₃-N deposition ranged from 0.40 to 1.13 kg·ha⁻¹·yr⁻¹ from 1982 to 2020 with a mean value of 0.69 kg·ha⁻¹·yr⁻¹ (Figure 7c). Wet deposition of SO₄ significantly declined from 1983 to 2018, with a range of 1.0 to 5 kg·ha⁻¹·yr⁻¹ and a mean deposition of 2.3 kg·ha⁻¹·yr⁻¹ (Table 2, Figure 6d).

Figure 7. Hierarchical cluster analyses of biogeochemical and algal pigment data from a sediment core representing a 270-year record from Santa Fe Lake, New Mexico. The red lines represent significant breaks in the hierarchical model structure, which define the three phases of change discussed. Constrained cluster analysis was produced using CONISS (Juggins 2023).

Hierarchical cluster analysis

Analysis of geochemical and pigment proxies using constrained cluster analysis revealed three main periods of lake conditions (Figure 7). The main split in the core occurred ca. 1975, separating more recently deposited sediments from deeper deposits. A secondary division isolated sediments deposited before ca. 1810 from those deposited during the interval 1810 to ca. 1975. A relatively minor transition occurred ca. 1920, separating older and more recent sections of the middle interval (Figure 7).

Discussion

Hierarchical cluster analysis and GAM analyses of significant periods of change revealed several distinct temporal phases related to changes in geochemistry, primary production, and phototrophic community composition in Santa Fe Lake during the past 270 years (Figures 3–5). Phase 1 (ca. 1750–1810) is the oldest interval of the time series and begins during the LIA when a relatively stable and cold climate favored cyanobacteria (echinenone, canthaxanthin), purple sulfur bacteria (okenone), and diatoms (diatoxanthin) over chlorophytes and cryptophytes. Phase 2 (ca. 1810–1975) defined a period of prolonged decline of most primary producers to historic minima during the mid-twentieth century, after which air temperatures increased in tandem with greater variability in precipitation extremes (PRISM, 2023; Figure 6a,b). During phase 3 (after ca. 1975), total phototrophic abundance increased (as pheophytin a), as populations of chlorophytes (pheophytin b, lutein-zeaxanthin), cryptophytes (alloxanthin), and diatoms all expanded, albeit with slightly different timing (Figure 5). These groups appeared to benefit from atmospheric warming in the latter half of the twentieth century alongside increasing atmospheric nitrogen deposition. These environmental changes resulted in C and N isotope variations consistent with elevated primary production (Bunting et al. 2016) declines in C:N ratios toward more algal-like values and elevated deposition of organic matter (as C and N). In general, historical patterns of lake change were dissimilar to local histories of many anthropogenic processes (e.g., land use change, fire events), suggesting that the production and community composition of Santa Fe Lake were mediated mainly by climatic factors.

Phase 1. The Little Ice Age (ca. 1750–1810)

During the first approximately sixty-five years of the core record, the relatively stable climatic conditions of the LIA may have facilitated elevated algal biomass in Santa Fe Lake (Figure 5). During this period, biogeochemical parameters (percentage N, percentage C, C:N ratio) were low and consistent suggesting a stable oligotrophic system (Figure 3). The phototrophic communities at a near historical maximum during this period included cyanobacteria (echinenone, canthaxanthin), purple sulfur bacteria (okenone), and diatoms (diatoxanthin). Recent research demonstrates that cyanobacteria can proliferate in cold conditions across a variety of lake systems (Reinl et al. 2023), particularly in arid polar and alpine habitats with low levels of dissolved organic matter (DOM) in the water column. These conditions favor taxa that can withstand elevated ultraviolet radiation (UVR) (Leavitt et al. 1997; Hodgson et al. 2004). During this early period in Santa Fe Lake, planktonic chlorophyte and cryptophyte groups could have been suppressed by photo-oxidative damage, whereas benthic or tychoplanktonic taxa could have been less affected. During this phase, okenone was also present at elevated abundances (Figure 5). Purple sulfur bacteria are obligate anaerobes that require light to penetrate sulfide-rich anoxic habitats, such as profundal sediments (Leavitt and Hodgson 2001; Stomp et al. 2007). Consistent with the high abundance of total phototrophs (pheophytin a), these bacteria need a relatively high influx of organic matter to sediments to allow the development of complete anoxia in surficial illuminated sediments.

Phase 2. End of the Little Ice Age and climate instability (ca. 1810–1975)

The second phase of the Santa Fe core record began with the end of the LIA (approximately 1850) and continued into the middle of the twentieth century. This period was marked by an increase in the amplitude of the PMDI, with frequent shifts between drought and precipitation over both cold and warm periods (Figure 6). Some of the most extreme single-year, 3-year, and 7-year flow events of the past 700 years occurred in the Santa Fe River basin since 1950 (Margolis et al. 2011). At the same time, 81 percent of the wettest reconstructed 40-year and 7-year high flow periods began in 1914 and continued into phase 3, with extremely wet periods in 1920 and 1980. The concentrations of most pigment biomarkers declined throughout this time of climatic variance (Figure 5). Of note, concentrations of okenone from purple sulfur photosynthetic bacteria declined significantly from ca. 1880 to 1930 and remained at low levels until the 1960s (Figure 5). The decline in okenone may reflect lower water column primary production and organic matter (OM) deposition resulting in reduced sedimentary anoxia. It may also reflect a decline in light penetration to the benthos from sediment inputs stimulated by variability in precipitation. Given that the proportion of benthic diatoms increased slightly during this phase (Figure 4b), we infer that the loss of sulfur bacteria is most consistent with the effects of declining primary production, which is further supported by low values of total phototrophic abundance (pheophytin a) during this period (Figure 5).

Typically, droughts reduce water influx from the surrounding watershed, resulting in decreases in terrestrial dissolved organic matter, silica, and nutrient inputs to lakes while increasing water transparency, ultraviolet radiation penetration, salinity, and acidity (Hodgson, Ward, and Dahm 2013; Williamson et al. 2016). In contrast, precipitation extremes can increase physical turbidity by flushing sediment from the surrounding watershed. In concert, these opposing processes can result in shifts in whole-lake metabolism (Sadro and Melack 2012) and a predominance in generalist taxa including S. construens venter, S. pinnata, and P. brevistriata (Stanish, Nemergut, and McKnight 2011). These species were found in Santa Fe Lake sediments and are known to thrive in cool arctic and alpine lakes globally (Figure 4a).

Phase 3. Continued warming and anthropogenic impacts (ca. 1975–2020)

The third phase of the Santa Fe Lake historical record was defined by increasing regional temperatures, further increases in climatic variability, increases in wet atmospheric ammonia deposition, and only modestly elevated anthropogenic disturbances (Figure 6). Warming in northern New Mexico increased, with an increase in annual mean temperatures of 1.1°C since 1950 (PRISM 2023). During this most recent phase, variability in dry and wet conditions continued. However, unlike the patterns in phase 2, primary production increased rapidly to near-historical maxima during phase 3 (Figures 3 and 5).

Long-term atmospheric warming can enhance lake production by increasing terrestrial soil development and nutrient export, water residence times, and length of the lake ice–free season (Adrian et al. 2009; Dugan 2021). In Santa Fe Lake, warmer air temperatures were marked by an increased abundance of chlorophytes, cryptophytes, and overall phototrophic biomass (Figures 5 and 6). Chlorophytes respond positively to warming in both paleolimnology studies and field experiments (Kuefner et al. 2021; Oleksy, Baron, and Beck 2021), whereas pelagic cryptophytes increase when lake water warming is combined with elevated DOM concentrations (Lami, Guilizzoni, and Marchetto 2000; Buchaca and Catalan 2007). In Santa Fe Lake, alloxanthin from cryptophytes increased alongside elevated sediment C and N content after the 1960s, consistent with increased DOM influx in the most recent decades (Figure 7). Though increased C:N ratios after ca. 1975 imply a shift from more terrestrially derived OM (C:N ~20) to that of aquatic origin (C:N < 12), research from more northern Rocky Mountain sites suggests that DOM derived from alpine meadows may also exhibit C:N ratios like those of algae (Bunting et al. 2010). Further analysis of the composition and provenance of sedimentary OM (e.g., cellulose, lignin-phenols) would help better resolve how changes in elemental geochemistry record variation in primary production and influx of terrestrial DOM (Meyers and Ishiwatari 1993).

The sharp depletion in sedimentary δ¹³C values during phase 3 is consistent with the effects of elevated primary production in Santa Fe Lake during the past fifty years (Figures 3 and 5). Overall historical changes in δ¹³C were inversely correlated with biomarkers of total primary production (i.e., pheophytin a), with particularly rapid transitions after ca. 1975 when sedimentary δ¹³C declined from −25 to −28 per mil. In other lakes, this pattern reflects an increase in the use of respired CO₂ (−25 to −30 per mil) rather than atmospheric CO₂ (0 to −5 per mil) or carbonate-derived dissolved inorganic carbon (DIC; −5 to −10 per mil) for nutrient-stimulated photosynthesis (Finlay and Kendall 2007). Though the general depletion of δ¹³C also aligns with changes in atmospheric δ¹³C-CO₂ a phenomenon known as the “Suess effect” (Verburg 2007), the near-exponential increases in C, N, and overall algal biomass since ca. 1975 support an interpretation of increased primary production and fixation of respired CO₂.

Although increases in DOM and lake warming may contribute to elevated lake production over the last 50 years, the last half of the twentieth century also marks an interval of potential human effects on global and regional biogeochemical cycles. Although Santa Fe Lake and its catchment were not directly modified by forestry, hydrology, soil disturbance, or fish stocking, atmospheric deposition of N and P may have influenced biological responses during phase 3. Throughout the past 270 years, δ¹⁵N values declined from ~2.0 per mil in the deepest sediments to ~0.6 per mil by the mid-twentieth century, with a more marked depletion to −0.4 per mil in surface sediments. The δ¹⁵N profile from Santa Fe Lake is like many other lakes reported by Holtgrieve et al. (2011), including two Colorado lakes within 320 km of our study lake. Though initial and final stable N isotope values differed somewhat across the twenty-six lakes in the Northern Hemisphere, all displayed declines in δ¹⁵N during the mid-1900s. Holtgrieve et al. (2011) explained the coherent depletion of δ¹⁵N as signaling the acceleration of N emissions from industrial N fixation for fertilizer use.

Though recent declines δ¹⁵N are present in Santa Fe Lake sediments, regional variation in deposition of different chemical species of N make it difficult to unambiguously assign the declines to atmospheric deposition. For example, there is presently substantial overlap in the range of δ¹⁵N values of both NO₃ and NH₄, as well as contrasting patterns of declining NOx emissions and increasing NH₃ emissions, which together affect N accumulation in sediments (Clark et al. 2021; Figure 3). Specifically, although the nearest atmospheric deposition measurements (from the NADP site at Bandelier National Monument) exhibit little change in overall wet N deposition from 1983 to present, there has been a significant increase in NH₄ deposition, whereas NO₃ deposition has declined (Figure 6c). This pattern mirrors a shift in species composition of N deposition across the United States, from principally NO₃ early in the historical record to mainly NH₄ in more recent wet atmospheric deposition. Overall, this pattern reflects a decline in nitrogen oxide emissions from combustion sources and an increase in ammonia emissions from livestock production (Li et al. 2016). Finally, differences in the elevation of monitoring and lake locations may have affected our ability to evaluate the effects of N deposition on Santa Fe Lake. The NADP site at Bandelier National Monument is located at 1,997 m.a.s.l., some 1,533 m lower than Santa Fe Lake (Figure 1). As a result, the deposition values may be higher at Santa Fe Lake due to increased precipitation at higher elevations. Although changes in the amount and chemical composition of N are known to influence phytoplankton in other mountain lakes (Wolfe, Baron, and Cornett 2001; Wolfe, van Gorp, and Baron 2003; Oleksy et al. 2020), we also note few increases in nitrophilic diatom species during the last seventy-five years (Wolfe, Baron, and Cornett 2001; Sheibley et al. 2014; Oleksy et al. 2020; Shampain et al. 2023), suggesting that the effects of N deposition were relatively minor. Instead, the majority (~80 percent) of the Santa Fe Lake diatom community was either tychoplanktonic or benthic. In shallow Santa Fe Lake, tychoplanktonic taxa may largely reside in the benthos, which can inhibit the response of the diatom community to N deposition as noted by Spaulding et al. (2015) in shallow alpine lakes in the Teton range.

The contribution of atmospheric P derived from dust, as well as metals and acids from regional copper smelters and coal-burning power plants since the mid-twentieth century, also may have influenced Santa Fe Lake’s ecology. Significant dust mobilization in the Southwestern United States has occurred from cattle grazing, expansion of row crop agriculture, and river system modification (Neff et al. 2008). Because we did not see increases in the sedimentation rate in Santa Fe Lake indicative of dust deposition, we hypothesize that Santa Fe Lake’s position on the leeward side of the Southern Rocky Mountains may shield the lake from regional dust, creating a “deposition shadow” effect for atmospherically derived nutrients. In contrast, a sediment core extracted in the late 1980s from Santa Fe Lake found surface sediments enriched with Hg, Mn, and Pb, suggesting deposition of both atmospheric metals and, potentially, acids since 1920 (Lynch et al. 1988). Similarly, sustained acidic deposition would have altered diatom assemblages to favor acid-tolerant diatoms (National Research Council 1986), but we found no evidence of increased abundance of acidophilic taxa in phase 3 or earlier (Figure 4a). Taken together, these lines of evidence suggest that aggregate human activities were not the main factor regulating the production and algal composition of Santa Fe Lake since 1950.

Comparison with other Western mountain lakes

Other mountain lakes in the Western United States have shown marked increases in primary production in response to atmospheric warming and elevated N deposition. Research studies in lakes of the Sierra Nevada Mountains (Heard et al. 2014), Greater Yellowstone Ecosystem (Saros et al. 2012), Rocky Mountain National Park (Wolfe, Baron, and Cornett 2001; Wolfe, van Gorp, and Baron 2003; Oleksy et al. 2020), and Utah’s Uinta Mountains (Hundey et al. 2014) have all documented N enrichment and related biological changes in high-elevation lakes beginning in the mid-twentieth century. Across these systems, algal species assemblages have shifted to favor more pelagic and nitrophilic taxa, although changes in total phototrophic biomass have varied. Some lakes have experienced exponential increases in phototrophic biomass, such as in Rocky Mountain National Park in Colorado where an abundance of benthic chlorophytes and total primary producers increased two- to threefold in response to N deposition and warming after 1950 (Oleksy et al. 2020). Lakes more protected by topographic position and distance from N emission sources, including those within the Teton Range and Pacific Northwest, showed more muted responses to recent global changes (Sheibley et al. 2014; Spaulding et al. 2015). Santa Fe Lake falls in the category of muted responses. In Santa Fe Lake, C, N, δ¹³C, and δ¹⁵N proxies all changed after ca. 1975, but the timing and magnitude of phototrophic community response varied, with diatom community composition remaining stable, cyanobacteria declining, chlorophytes and cryptophytes increasing exponentially, and overall biomass increasing to a historical maximum.

Conclusions

Santa Fe Lake appears to represent a system mainly affected by climate change, only modestly by N deposition since 1950, and with less pronounced impacts than those observed in other mountain lakes. Anthropogenic activities, both direct and indirect, appear to have had a modest effect on primary production and biotic composition. Lakes such as Santa Fe are important examples of systems where despite significant regional and global changes, drivers have not been strong enough to elicit substantial biological reorganization since the middle of the twentieth century. Climate variability appears to be the main factor influencing Santa Fe Lake, such that there have been no points of critical transition in primary production or community composition over the past 270 years. Oleksy et al. (2020) suggested that high N deposition might have been the initial trigger for ecosystem change in Colorado Rocky Mountain lakes. In Santa Fe Lake, we noted subtle community shifts and significant changes in biogeochemistry alongside increasing air temperatures and more frequent and extreme periods of drought and precipitation. Changes in the climate appeared to favor chlorophytes and cryptophytes that benefit from warming and, possibly, organic matter inputs during the past century. We conclude that while regional N deposition after 1950 has likely supported elevated primary production and enhanced nutrient cycling, the effects of atmospheric N were limited such that Santa Fe Lake represents a “background” trajectory of anthropogenically induced global change, mainly in response to climate variability. We anticipate that lake production and biogeochemistry will continue to change as mountain lakes are predicted to continue warming at an average rate of 0.47°C per decade within the Southern Rocky Mountains (Roberts et al. 2017).

Highlights

• Fossil phototrophic and diatom pigments revealed elevated primary production resulting from increases in cyanobacteria, purple sulfur bacteria, and diatoms during the stable conditions of the Little Ice Age.

• Primary production declined from the end of the Little Ice Age into the mid-twentieth century.

• The warming climate after ca. 1950 and, to a lesser extent regional N deposition, drove primary productivity to a historic maximum due to increased chlorophyte and cryptophyte groups.

• Unlike other Rocky Mountain lakes, regional human activities had little effect on the phototrophic composition and productivity of Santa Fe Lake.

Data availability

Data are available at: https://doi.org/10.5066/P9P659GU

Acknowledgments

We thank Tim Weinmann and Caitlin Charlton, who helped collect the sediment core. We thank Deirdre Bateson for pigment analyses, Bjoern Wissel for stable isotope analyses, and Cheyenne Everhart and USGS St. Petersburg Coastal and Marine Science Center for ²¹⁰Pb analyses.

Disclosure statement

There are no competing interests to declare. Any use of trade, firm or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

Additional information

Funding

JSB, ABS, and SAS were supported by the USGS Climate Research and Development Program as part of the Western Mountain Initiative under grant EN05U4U; PRL was supported by the Canada Research Chair, Canada Foundation for Innovation, the Province of Saskatchewan, NSERC Canada, and the University of Regina.