Diatoms and Other Siliceous Indicators Track the Ontogeny of a Bofedal (Wetland) Ecosystem in the Peruvian Andes

Botany

Diatoms and other siliceous indicators track the ontogeny of a bofedal (wetland) ecosystem in the Peruvian Andes

Journal: Botany

Manuscript ID cjb-2020-0196.R1

Manuscript Type: Article

Date Submitted by the 20-Feb-2021 Author:

Complete List of Authors: King, Connor; Queen’s University, Department of Biology Michelutti, Neal; Queen’s University, Department of Biology Meyer-Jacob, Carsten; Queen’s University, Department of Biology Bindler, Richard; Umeå University, Department of Ecology and EnvironmentalDraft Sciences Tapia, Pedro; INAIGEM Grooms, Christopher; Queen’s University, Department of Biology Smol, John; Queen's University

Tropical Andes, Cushion bogs, High-altitude peat, Distichia muscoides, Keyword: Cordillera Vilcanota

Is the invited manuscript for consideration in a Special Not applicable (regular submission) Issue? :

Diatoms and other siliceous indicators track the ontogeny of a bofedal (wetland) ecosystem in the Peruvian Andes

Connor King1, Neal Michelutti1*, Carsten Meyer-Jacob1, Richard Bindler2, Pedro Tapia3, Christopher Grooms1, John P. Smol1

1Paleoecological Environment Assessment and Research Laboratory (PEARL), Department of Biology, 116 Barrie Street, Queen’s University, Kingston, ON K7L 3N6, Canada

2Department of Ecology and Environmental Sciences, Umeå University, 901 87 Umeå, Sweden (email: [email protected])

3INAIGEM – Dirección de Investigación en Ecosistemas de Montañas, Huaraz, Peru e-mail: [email protected] Draft *Corresponding Author: email: [email protected]; phone: 613.533.6159; fax: 613.533.6617

Abstract

Recent warming in the Andes is affecting the region’s water resources including glaciers and lakes, which supply water to tens of millions of people downstream. High altitude wetlands, known locally as bofedales, are an understudied Andean ecosystem despite their key role in carbon sequestration, maintaining biodiversity, and regulating water flow. Here, we analyze subfossil diatom assemblages and other siliceous bioindicators preserved in a peat core collected from a bofedal in Peru’s Cordillera Vilcanota. Basal radiocarbon ages show the bofedal likely formed during a wet period of the Little Ice Age (1520-1680 CE), as inferred from nearby ice core data. The subfossil diatom record is marked by several dynamic assemblage shifts documenting a hydrosere succession from an open-water system to mature peatland. The diatoms appear to be responding largely to changes in hydrology that occur within the natural development of the bofedal, but also to pH and possibly nutrient enrichment from grazing animals. The rapid peat accretion recorded post-1950 at this site is consistent with recent peat growth ratesDraft elsewhere in the Andes. Given the many threats to Peruvian bofedales including climate change, overgrazing, peat extraction, and mining, these baseline data will be critical to assessing future change in these important ecosystems.

Key Words: Tropical Andes, Cushion bogs, High-altitude peat, Distichia muscoides, Cordillera Vilcanota, X-ray fluorescence spectroscopy, Climate change

Introduction

Temperature increases in the tropical Andes are occurring at a rate nearly double the global average (Vuille et al. 2003) and are already resulting in marked environmental changes, including rapidly receding glaciers (Salzmann et al. 2013; Thompson et al. 2013), changes to agricultural practices (Halloy et al. 2005), and shifts in species ranges (Seimon et al. 2007; Schmidt et al. 2008). Anthropogenic climate change will have unpredictable effects on Andean ecosystems, particularly on plant communities whose habitat is restricted to the highest elevations and therefore may be under threat of mountaintop extirpation. Andean wetlands, regionally known as bofedales (singular bofedal), are of particular concern because many exist at the altitudinal and hydrological limits for plant life (Squeo 2006). Bofedales often form downstream from glaciers where topographical and hydrological conditions favour water pooling. This vegetation provides rich forage in an

otherwise barren environment, supporting a variety of camelids, avifauna, and larger predators. For millennia, indigenous communities have been directly dependent upon bofedales to graze their livestock including llamas, alpacas and now cows, which remain the basis of the local economy. In addition, bofedales provide various ecological services that promote biodiversity and act as water buffers preventing floods and increasing base flow during the dry season (Maldonado Fonkén, 2015). In Peru, the societal and ecological importance of bofedales has been recognized via their identification as “fragile ecosystems” under Peruvian General Environmental Law (Law No. 28611, Article 99; Maldonado Fonkén 2010) and they are considered areas for conservation or protection under Peruvian Ecological-Economic Zoning Regulations (DS Nº 087-2004-PCM, Article 9, PCM 2004). However, effective management of bofedales will require a greater understanding of their relationship with climate, specifically how they respond to rising temperatures, altered precipitation regimes and dwindling glacial runoff. In addition, Andean bofedales are increasingly threatened by overgrazing, peat cutting, mining and drainage (Benavidez 2014; MaldonadoDraft Fonkén 2015; Sánchez et al. 2017). A common characteristic of bofedales is the underlying presence of peat, which accumulates when production of the vegetation exceeds decomposition. Peatlands are dynamic ecosystems and undergo a series of successional changes, known as hydroseres, driven largely by changes in hydrology and vegetation. A common hydroseral succession is the transition from an open water-to-fen-to-bog environment, although variability exits along this trajectory (Charman 2002). Peatlands are useful natural archives because the organic material that accumulates over time contains physical, chemical, and biological indicators that reflect changing environmental conditions over long-term timescales (Engel et al. 2014; Hribljan et al. 2015; van Bellen et al 2016). Paleoecological studies of peat deposits play an important role in conservation research (McCarroll et al. 2016) as they inform about the development of the peatland itself, as well as past climate and other environmental changes (Gaiser and Rühland 2010; Carballeira and Pontevedra-Pombal 2020). For example, diatom algae (Bacillariophyceae) preserved in peat deposits have been used throughout the world to track changes in hydrology, water chemistry, landscape disturbances, and climate variability (Rühland et al. 2000; Hargan et al. 2015). Diatom studies in Andean wetlands have typically focused on floristic descriptions (Maidana and Seeligmann, 2006; Seeligmann et al. 2008) with a few studies assessing seasonal and spatial patterns (Salazar-Torres and Huszar 2012). Here, we analyze fossil

4 diatom assemblages preserved in a bofedal peat core from the Cordillera Vilcanota in southeastern Peru (Fig. 1). Although peat cores have been used to reconstruct long-term environmental change elsewhere in the Andes (Skrzypek et al. 2011; Engel et al. 2014; Hribljan et al. 2015; Benfield et al. 2021), few have focused on paleoecology. In addition to diatoms, we also document the relative abundances of other siliceous microfossils, namely chrysophycean stomatocysts (Duff et al. 1995; Wilkinson et al. 2001), disassociated plates of testate amoeba (Douglas and Smol 1987; 1988), and phytoliths (Piperno 2001). Chrysophytes, although traditionally viewed as being planktonic algae common in oligotrophic waters, are also known to be periphytic and often associated with mosses in shallow waterbodies (Douglas and Smol 1995). As such, they may respond sensitively to changes in vegetation and moisture levels expected with peatland succession. Testate amoebae are often the most common protists living in peat habitats (Heal 1962), and in past studies have been shown to closely track bog development (van Bellen et al. 2016; Zhang et al. 2020). Phytoliths are siliceous deposits that form in plant tissue and because they are released upon death and decompositionDraft (Piperno 2006), their abundances may be related to levels of peat decomposition; but other factors such as fire and aerial transport can also alter their concentrations in peat cores (Mullholland and Rapp 1992; Rühland et al. 2000). Collectively, these siliceous microfossils may provide valuable paleoecological evidence, independent of diatoms, on peatland changes over time. To characterize the peat core stratigraphy and help interpret shifts in the biological communities, we also measured the loss-on-ignition (LOI) to estimate organic content, as well as a suite of major and trace elements using X-ray fluorescence spectroscopy (XRF), which can provide information on, for example, changes in peat decomposition or redox conditions (Biester et al. 2004; López et al. 2006). We demonstrate that diatoms and other siliceous indicators sensitively track successional changes in the study of this bofedal since its inception, providing some perspective on how future climate changes may affect bofedales throughout the Andes. This research provides novel data on long-term changes of a bofedal from Peru’s Cordillera Vilcanota. Together with paleoenvironmental records from nearby ice cores (Thompson et al. 2013) and lake sediment cores (Michelutti et al. 2019, 2020), these data provide a more holistic account of long-term environmental change from this region.

Methods

Study Site Description The Cordillera Vilcanota (~14° S; 71° W) is an important “water tower” in southeastern Peru and is home to the Quelccaya Ice Cap (QIC), the world’s largest tropical glacier. Several studies have shown marked environmental changes in this mountain range in response to warming of recent decades. Most notably is the retreat of the region’s iconic glaciers and ice caps, which have shrunk by ∼30% in area and ∼45% in volume since 1985 (Salzmann et al. 2013). The region near the study bofedal contains archaeological ruins and remains including pottery sherds, arrowheads, and mortuary monuments that date from the Formative Period in the Cuzco region (2500 BCE – 200 CE) to the Colonial era (1532 – 1800s CE). In nearby Laguna Sibinacocha (Fig. 1), submerged ruins thought to indicate sacred architecture have been reported (Michelutti et al. 2019). Climate in the Cordillera Vilcanota is determined by a complex interplay of mesoscale and synoptic processes. Precipitation during the austral summer is enabled by the Bolivian High, a semi-permanent zone of high pressure located at 17° S, 70° W. The Bolivian High creates easterlies that advect moistureDraft from the Amazon basin and carry it towards the Andes. However, most water vapour is transported by surface winds that develop in response to permanent zones of low pressure in continental South America and high pressure in the south Pacific and Atlantic (Garreaud, 2009). Both sea surface temperature (SST) in the Atlantic and the El Niño-Southern Oscillation (ENSO) also exert climatic control, particularly in the eastern tropical Andes. During El Niño (La Niña) years, temperatures are warmer (cooler) and the climate is drier (wetter) (Vuille et al. 2000). This is mainly due to changes in upper-level wind patterns that inhibit westerly transport of moisture (Vuille et al. 2000). Variations in ENSO thus play an important role in modulating regional climate in the Cordillera Vilcanota. Recently, new evidence has arisen that strengthening of meridional flow over the Amazon basin offsets the influence of ENSO, highlighting the complexity of climatic controls in this region (Segura et al. 2020). Annual variations in mean temperature are minor, with only a few degrees Celsius separating temperatures from summer to winter seasons; however, diurnal temperatures can vary by as much as 18 °C. Seasonality is defined largely by precipitation with a rainy period from October to March and a dry period from April to September. Instrumental data in the Cordillera Vilcanota are sparse. The Peruvian National Weather Service (Servicio Nacional de Meteorología y Hidrología (SENAMHI) has two nearby stations with data extending back to the mid-1960s. The Ccatcca station (3729 m asl), located ∼60 km west-northwest of the study site, recorded mean minimum and maximum

6 daily temperatures of 1.3 and 15.3 °C, respectively, and mean annual precipitation of 608 mm from 1965–2014. The Pomacanchi station (3200 m asl), located ∼60 km west-southwest of the study site, recorded mean minimum and maximum daily temperatures of 2.8 and 17.2 °C, respectively, and mean annual precipitation of 851 mm from 1985–2014 (Michelutti et al. 2020). From 1965–2014 the Ccatcca station recorded an increase of 0.23 °C (r2 = 0.001, P < 0.001) in maximum daily temperatures and 1.08 °C (r2 = 0.01, P < 0.001) in minimum daily temperatures. The Pomacanchi station recorded increases of 0.37 °C (r2 = 0.004, P < 0.001) in maximum daily temperatures and 0.80 °C (r2 = 0.014, P < 0.01) in minimum daily temperatures from 1985–2014. Precipitation at both stations show significant increases over time, with Ccatcca showing an increase of 139 mm from 1965–2014 and Pomacanchi showing an increase of 457 mm from 1965–2014 (Michelutti et al. 2020).

Core Collection and Chronology In August 2018, a Russian peatDraft corer (7.6 cm diameter, 1 m length) was used to collect a profile from the main study site at an elevation of 5090 m asl (S 13° 48' 42.9", W 71° 06' 15.0"; Fig. 1). The study bofedal was dominated by Distichia muscoides, a widespread, semiaquatic plant that grows in dense cushions. Distichia peatlands serve similar ecological functions to Sphagnum-dominated peatlands common in the Northern Hemisphere; however, Distichia is a member of the Juncaceae family and is a vascular plant, whereas Sphagnum is a non-vascular bryophyte. Two successive 1-m drives, ~15 cm apart, were required to obtain the entire 130 cm profile. Glacial clay from 96–130 cm indicated the entire history of peat accumulation at the site was collected. The cores were sectioned into 2- cm intervals in the field, using a sharp blade that was cleaned between intervals. Samples were stored in Whirl-pak® bags in cool and dark conditions until being transferred to the PEARL lab at Queen’s University. A second peat core (S 13° 48' 58.3", W 71° 04' 35.1") from a nearby bofedal ~3 km away and ~210 m downslope (4880 m asl) of the main study site was also collected (Fig. 1). We refer to this site as the “lower bofedal” given its lower altitude relative to the “main site”. The lower bofedal core was 90 cm in length, of which the bottom ~16 cm was glacial clay indicating the entire growth history at the site was recovered. The lower bofedal core was only analyzed for 210Pb and 14C radioisotopes for dating comparisons to the main study profile. Both the main and lower bofedal cores were dated by applying a constant-rate-of- supply model to excess 210Pb activities using the ScienTissiME dating software

(ScheerSoftware Solutions, Barry’s Bay, ON, Canada; Fig. 2). Peat samples were counted at Queen’s University on a digital high-purity germanium spectrometer (DSPEC, Ortec®) with a well-type gamma detector consisting of a germanium crystal with lithium diffused electrodes. Intervals beyond the range of 210Pb dating were dated using Accelerator Mass Spectrometry (AMS) radiocarbon (14C) macrophyte remains (where available) and bulk sediments. In the main study core, material from seven depth intervals were sent to the A.E. Lalonde AMS Laboratory at University of Ottawa for AMS 14C (Table 1). Four of those intervals contained paired samples of both bulk peat and picked Distichia leaves (non-root material) to assess the influence of modern carbon being introduced to older intervals via root penetration. In the lower bofedal core, bulk peat samples from two intervals were dated by 14C. Age-depth models (exclusive of the 210Pb data) were developed using the Clam v.2.3.4 package (Blaauw 2010) in R (R Core Team 2013), the SHCal13 radiocarbon age calibration curve (Hogg et al. 2013), and SH1-2 for post-bomb radiocarbon dates (Hua et al. 2013).

Diatom Sample Preparation and EnumerationDraft Siliceous microfossil preparation followed techniques outlined by Wilson et al. (1996). Approximately 0.03 grams of peat were measured from 45 samples (every 2-cm interval) and placed in a glass scintillation vial. Organic material was digested using 15 mL of a 50:50 molar mixture of sulphuric and nitric acid was added to the vials, which were then placed in a ~80°C water bath and stirred every 20 minutes for two hours. The slurries were repeatedly aspirated and rinsed with deionized water until a neutral pH was achieved. Aliquots of the slurry were pipetted onto coverslips and after drying, were permanently mounted onto slides using Naphrax®. Diatom valves and other siliceous indicators were enumerated using a Leica® DMRB light microscope fitted with differential interference optics at 1000X magnification. Efforts were made to count a minimum of 300 valves per interval (every 2 cm), but where diatoms valves were sparse, a minimum of at least 150 valves was enumerated. Intervals where 150 valves could not be counted were excluded from analysis. Diatoms were identified to the species level where possible using several sources including Krammer and Lange-Bertalot (1986) and Kulikovsky et al. (2010). The ratio of diatoms to other siliceous indicators was calculated using methods outlined by Smol (1985).

Loss-on-Ignition and X-ray Fluorescence Spectroscopy

Organic matter content was estimated by loss-on-ignition at 550°C for four hours using ~0.2 g of freeze-dried, ground, and homogenized sample material (Dean, 1974). Inorganic element concentrations in the peat samples were determined on ~0.5 g of peat material by wavelength dispersive X-ray fluorescence using a Bruker S8 Tiger spectrometer equipped with a Rh anticathode X-ray tube. The calibration was developed for a plant/peat matrix (for specific details see Hansson et al. 2015) based on modification of a sediment-soil calibration from Rydberg (2014). The XRF analyses yield data on 20 major and trace elements; accuracy was within 8% for all elements, except Pb (14%), and precision with 6%. Mn and Fe are redox sensitive elements, with higher mobility in reduced form under anoxic conditions that can migrate along redox gradients, and Mn/Fe ratios were thus used as an indicator of changes in redox conditions where higher ratios indicate more oxygenated conditions (López et al. 2006). Concentrations of halogens such as Br can indicate peat decomposition processes because of their strong association with organic matter and enrichment following peat decomposition (Biester et al. 2004). Draft Data Analysis To determine diatom assemblage zones of significance, a constrained incremental sum of squares (CONISS) was performed (Grimm, 1987). First, diatom assemblage data were converted to relative abundances. Taxa that did not exceed more than 2% relative abundance in two intervals were excluded from analysis. Data were loaded into R and a CONISS analysis was carried out using the rioja package (Juggins 2017). Using the same package, a broken stick analysis was then performed to determine the number of significant zones. The diatom profile, showing those taxa with relative abundances > 5% in at least one interval, were plotted using the program C2 version 1.5.1 (Juggins 2007). The significant zones determined by the CONISS analysis were overlaid on the stratigraphy and the ratios of diatoms to other siliceous indicators including phytoliths, chrysophyte cysts, and protozoan plates, were plotted alongside the diatom assemblages.

Results

Core Chronology – In the main study core, unsupported 210Pb activity declined from approximately 290 Bq kg-1 before reaching supported levels at ~7 cm (Fig. 2). The surface value in the peat is about three times lower than surface values recorded in nearby lake

sediment cores (Michelutti et al. 2020). There is no peak in 137Cs (which has been detected in nearby lake sediments (Michelutti et al. 2019)), and thus this anthropogenic radionuclide cannot be used to independently corroborate the modeled 210Pb dates. Although the unsupported 210Pb activity shows a steady decline to background, the chronology should be interpreted with caution due to such low activity levels. In the lower bofedal core, the peak unsupported 210Pb activity is approximately the same as in the main study core; however, the top interval records an unsupported 210Pb activity near background values (Fig. 2). The numerous 14C dates indicate the main study profile is much younger than an extrapolation of the CRS-derived 210Pb dates would suggest (Table 1). The same is true for the lower bofedal core (Table 1). The dating of younger peat sequences using 210Pb or 14C can be complicated by the potential mobility of atmospherically derived Pb as well as potential differential uptake, redistribution, and recycling of carbon in peat (Biester et al. 2007; Hansson et al. 2014); however, the fact that the trend in the fraction of modern carbon (F14C; Table 1) follows the post bomb radiocarbon curve as well as the agreement among the numerous 14C ages lends support that radiocarbonDraft dating provides an accurate chronology for our main profile. It is for this reason that we rely solely on 14C ages in developing the peat core chronologies. For the main profile, the 14C age-depth model indicates a most likely basal age between ~130 to 280 cal. yr. BP (best fit age: ~215 cal yr BP; Fig. 3), although given the range of possible dates for the minerogenic peat at the clay-peat transition (up to 501 cal. yr. BP; Table 1; Fig. 3), this should be interpreted with caution. In the main profile, minimal differences in 14C ages between paired samples of Distichia leaves and bulk sediment indicate that anomalously young ages due to modern roots penetrating downward is not an issue (Table 1). Radiocarbon dating of the lower bofedal core reveals a similar, although slightly older, age-depth profile to the main profile with a basal age between 507 and 549 cal. yr. BP (Table 1, Fig. 3).

Physical and geochemical peat characteristics – Variability in the geochemical data generally follows the chief lithologies identified within the main profile, including a basal clay interval from 130-96 cm depth, followed by a peat interval from 96-0 cm (Fig. 4). The grey basal clay is characterised by a low organic matter content (LOI <24%). With the initiation of peat accumulation and the transition from the basal clay, organic matter content increased and varied between 86 and 99% throughout the peat record, except for a more minerogenic layer around 63 cm (LOI: 67%). This layer also showed an increase in Br, with concentrations of up to 26 ppm. Simultaneous with a change in peat colour from dark-brown

10 to yellow-brown around the 30 cm depth, Mn/Fe ratios increased from <0.1 to >1 towards the top of the peat profile (~8 cm depth) (Fig. 4). Despite the dating uncertainties, radiocarbon dates indicate a large change in peat accretion rates for the main profile (Figs. 3, 4). Independent of the exact basal peat age, peat accretion rates appear to have increased substantially during the development of the uppermost ~60 cm of the profile for which radiocarbon dating indicates modern carbon ages (post-1950 CE). Whether assuming a basal peat age of 501 cal. yr BP, i.e., the oldest possible age indicated by radiocarbon dates, or a basal age of 215 cal. yr BP, i.e., the best fit age of the established 14C age-depth model, peat accretion would have ranged between ~0.1 and 0.2 cm/yr from the base of the peat to 60 cm depth, while post-1950 CE accretion rates were about an order of magnitude higher. Radiocarbon dates for the lower bofedal suggest similar peat accretion dynamics, with an accelerated modern peat accumulation (Fig. 3).

Diatom Assemblages – The main peat profile records several rapid diatom assemblage shifts. Benthic taxa, excluding a few tychoplanktonicDraft Aulacoseira taxa, dominated the assemblage throughout the peat profile (Fig. 5; ESM Table 1). We restrict our discussion to the dominant taxa, defined here by any species constituting at least 5% relative abundance at any one interval. This criterion was met by 26 taxa (Fig. 6). The CONISS analysis identified six significant assemblage zones in the core (Fig. 5), described below.

Zone 1 (90 – 64 cm; ~157 to 16 cal. yr. BP) Dominant taxa include Staurosira construens Ehrenberg, Staurosirella pinnata (Ehrenberg) D.M.Williams & Round, and to a lesser extent Encyonema norvegicum (Grunow) Mayer, Encyonopsis falaisensis (Grunow) Krammer, and Encyonema silesiacum (Bleisch) D.G.Mann. The ratio of diatoms:cysts and diatoms:phytoliths are relatively high and remain fairly stable during this zone, while the diatoms:plates ratios decrease steadily before rising again at ~70 cm depth (Fig. 5).

Zone 2 (64 – 32 cm; 16 to -44 cal. yr. BP) Zone 2 is demarcated by an abrupt decline of S. construens, which occurs contemporaneously with an increase in the relative abundances of E. norvegicum, S. pinnata, and E. silesiacum. There is a small peak in E. falaisensis between 50–52 cm depth. From 50 cm to 42 cm there is an increase in Ulnaria ulna (Nitzsch) Compère that also coincides with an increase in E. silesiacum. These increases occur concurrently with relative decreases of E.

norvegicum and S. pinnata. The ratios of diatoms:cysts, diatoms:plates, and diatoms:phytoliths are variable, but all show declines towards the end of this zone (Fig. 5).

Zone 3 (32-28 cm; -44 to -45 cal. yr. BP) Zone 3 is marked by an abrupt diatom assemblage shift with Sellaphora sp. [cf. subnympharum] increasing rapidly from zero values to a relative abundance of 64%, the highest value reached for any taxon in the record. At the 28-30 cm interval E. norvegicum shows an increase to ~20% relative abundance. The diatom:cyst ratio shows a slight peak and subsequent decline, and the diatoms:phytoliths show a steady decline (Fig. 5).

Zone 4 (28 – 22 cm; -45 to -46 cal yr BP) Zone 4 is demarcated by abrupt declines in the previously dominant Sellaphora sp. [cf. subnympharum] and E. norvegicum. Nitzschia paleacea Grunow in Van Heurck, Hantzschia amphioxys (Ehrenberg) Grunow, Pinnularia sp. [cf. kuetzingii], S. construens and S. pinnata are common during this intervalDraft but none exceed 20% relative abundance. Ratios of diatoms:cysts and diatoms:phytoliths, and to a lesser extend diatoms:plates all decrease during this zone (Fig. 5).

Zone 5 (22 – 14 cm; -46 to -51 cal yr BP) Hantzschia amphioxys dominates Zone 5, exceeding 60% relative abundance in some intervals. N. paleacea and Pinnularia sp [cf. kuetzingii] are also present but at <20% relative abundance. The diatoms:cysts ratios show a slight increase whereas the diatoms:plates and diatoms:phytoliths ratios each show a small rise and decline (Fig. 5).

Zone 6 (14 cm – surface; -51 to -68 cal. yr. BP) At the 16–14 cm interval, Pinnularia sp. [cf. kuetzingii] begins to increase as N. paleacea and H. amphioxys decline, demarking Zone 6. At the 12-14 cm interval, Eunotia arculus Lange-Bertalot & Nörpel becomes a dominant taxon for the first time in the history of the profile. From 10 to 2 cm depth, the combined relative abundance of Pinnularia sp. [cf. kuetzingii] and E. arculus exceed 50%. At 4 cm, Kobayasiella subtillissima (Cleve) Lange- Bertalot begins to increase and becomes the dominant taxon at the surface for the first time in the profile (Fig. 5).

Discussion

Peat formation and growth – In the main study core, the best-fit age-depth model based on radiocarbon dating indicates the initiation of highly organic peat (>86% organic matter) at the main study site ca. 200 cal yr. BP/1750 CE, although there is large uncertainty associated with the basal date and peat growth might have started as early as ~500 cal yr. BP/1450. CE (Fig. 3). The main drivers of peatland initiation are complex and vary globally. In mid and high latitudes, peat initiation is significantly predicted by rising growing season temperatures; however, in tropical South America peat formation is not significantly predicted by any paleoclimatic variable (Morris et al. 2018). At our study site, the nearby Quelccaya ice core records provide a paleoclimate context for the initiation of peat. A distinct Little Ice Age (LIA) period from ca. 1520 to 1880 CE is inferred by low values of δ18O in the ice core, which are thought to reflect air temperatures over long-term timescales. Net accumulation values, which represent a regional signal of precipitation variability, show record highs in the early LIA (1520-1680 CE) and record lows in the late LIA (1681-1880 CE). Given that bofedalDraft vegetation and peat accumulation are supported by stable groundwater flows and perennial saturation (Cooper et al. 2015), we conclude that the main bofedal study site most likely formed during the record high precipitation levels inferred during the early portion of the LIA (1520-1680 CE) in this region (Thompson et al. 2013). This wet period raised water levels by several meters in nearby Laguna Sibinacocha (Fig. 1), as evidenced by submerged archaeological remains within the lake (Michelutti et al. 2019). The relatively young age and high altitude (5090 m asl) of the main bofedal site is consistent with the relationship between peatland age and elevation documented in the northern Andes. Benfield et al. (2021) synthesized basal ages from 22 peatlands throughout the northern Andes and found a linear relationship (r2 = 0.65) between peatland initiation and elevation, with the youngest sites at the highest elevations. For example, the oldest peatland in the study formed ca. 17,200 cal yr BP at 3490 m asl, and the youngest formed ca. 1950 CE at 4881 m asl. At the main coring site, peat accretion accelerated after ca. 1950 CE. This may be driven, in part, by enhanced meltwater from the nearby (~2 km) glacier that drains into the study bofedal (Fig. 1). Recent warming in the Cordillera Vilcanota has led to massive reductions in the cryosphere including the Quelccaya Ice Cap, which has retreated to limits unprecedented within the last 6,000 years (Thompson et al. 2013). Also, glacial margins at the north end of nearby Laguna Sibinacocha (Fig. 1a) have receded at an average rate of 13.1

m/yr since 2005 CE (Seimon et al. 2017). While we can only speculate about the underlying mechanism, the high post-1950 CE peat accretion rates estimated for our study site are similar to those reported for other high-elevation peatlands in the South American Andes (Earle et al. 2003; Benavides et al. 2013; Cooper et al. 2015; Benfield et al. 2021). LOI and XRF data illustrate the onset of peat accumulation and the general ontogeny of the bofedal at the study site, with a distinct transition from basal clay to peat, which is decreasingly decomposed and highly organic towards the surface. Slightly lower organic matter contents between 68 and 54 cm depth co-occur with higher concentrations of Br and are likely the results of an increased degree of peat decomposition during this interval because preferentially organically bound elements such as Br tend to enrich following peat decomposition (Biester et al. 2004). The colour change and increase in Mn/Fe ratios at 30 cm depth indicate a shift from permanently anoxic to at least temporarily oxygenated conditions in the peat profile, and likely signify the height of the lower water table during the dry season. Draft Diatoms – The benthic fragilarioids that dominate the early portion of the peat record (Zone 1), namely S. construens and S. pinnata, are also often the first taxa to typically colonize lakes immediately following deglaciation (Wilson et al. 2012). Their pioneering nature is due to their ability to outcompete other diatoms in unfavourable conditions such as cool temperatures, low nutrients, and turbid waters (Lotter and Bigler 2000, Finkelstein and Gajewski 2008). Although common in alkaline waters, they can be found in circumneutral and slightly acidic waters from the Arctic (Smol et al. 2005) to the Andes (Michelutti et al. 2020; Fritz et al. 2004; Tapia et al. 2006). In lakes adjacent to the bofedal study site, paleolimnological data show that these fragilarioids are the most abundant taxa over the past several hundred years in both shallow and deep sites (Michelutti et al. 2020). Similar benthic fragilarioids were documented with peat initiation in Siberia (Russia) and were interpreted as indicating a shallow, open-water environment (Rühland et al. 2000). Likewise, S. construens and S. pinnata were found to be the main taxa in Sphagnum-dominated peatlands of the boreal shield and Hudson Plains (Canada) with high water tables (Hargan et al. 2015). Their dominance in the earliest portion of this record likely reflects shallow, open-water conditions characteristic of an emerging peat environment. The presence of acidophilic Eunotia taxa, such as E. exigua and E. arculus, in the bottommost intervals, albeit in low (<10%) relative abundances, suggests initial conditions may have been slightly acidic.

The transition to Zone 2 is demarcated by a decline in S. construens, with concomitant increases in epiphytic Encyonema taxa, including E. norvegicum, E. silesiacum, E. neogracile, and E. hebridicum. These taxa are common in high elevation lakes from the Ecuadorean Andes (Benito et al. 2019) as well as peatlands, moss seeps, and ponds in Arctic and alpine regions (Potapova 2014; Hargan et al. 2015). Their increase suggests a transition to a macrophyte-dominant environment relative to a shallow, open-water system. A similar transition from benthic fragilarioids to epiphytic taxa was documented in the early developmental stage of a Siberian peatland (Rühland et al. 2000). Peat accretion rate values begin to rise in the upper part of Zone 2, which is consistent with the inference of greater macrophyte production and peat formation (Fig. 4). The presence of Ulnaria ulna in Zone 2 (16 to -44 cal. yr. BP) is noteworthy because this taxon is known to be tolerant of saprobic water pollution (Hofmann et al. 2011; Lobo et al. 2002) and has been recorded in urban wetlands in Bogotá (Castro-Roa and Pinilla- Agudelo 2014) and eutrophic streams in Poland (Noga et al. 2016). Its presence might be tracking the first occurrence of grazingDraft animals that were likely to have been present as the bofedal vegetation became further developed. However, this taxon does not reach appreciable abundances elsewhere in the peat profile and it has also been documented as part of the periphyton assemblage associated with macrophytes (Montoya-Moreno and Aguirre-Ramírez 2013). Thus, it may simply be reflecting the increase in vegetation, as inferred by the presence of epiphytic taxa. Zones 3-5 are characterized by a series of rapid diatom assemblage shifts that, according to our age-depth model, would have occurred over less than one decade. In the Chilean altiplano, similarly rapid post-1950 peat accumulation rates were thought to reflect the young age and lack of steady-state conditions within the peatland, possibly due to strong seasonality of precipitation that could result in stochastic intervals of higher rates of net peat accumulation (Earle et al. 2003). In our main profile, the modelled time periods for Zones 3-5 are short due to the high accretion rates and we acknowledge that our age-depth estimates, although not implausible, should be interpreted with some caution. Zone 3 is characterized by a rapid increase of a taxon we refer to as Sellaphora sp. [cf. subnympharum]. Unfortunately, given the taxonomic uncertainty, there is little we can infer from this taxon, which reaches the highest relative abundance of any diatom species on record and then declines almost as abruptly. Clearly, though, the assemblage shift in Zone 3 marks the onset of a series of rapid, short-lived shifts in the dominant taxa. As discussed below, the assemblage changes beginning at this time may be tracking the continued

accumulation of organic matter and the mature phase of bofedal ontogeny, characterized by thick histols, lower permeability and higher water retaining capacity than in the overlying material (Vining et al. 2019). This inference is supported by peak accretion rates during this period (Fig. 4). In Zone 4, Nitzschia paleacea is the dominant taxon, but it never attains >20% relative abundance. N. paleacea is a cosmopolitan species observed in lakes and rivers, but also in seeps and mosses that are more characteristic of this bofedal (Hamsher et al. 2016). N. paleacea is also a pollution-tolerant taxon capable of living in nutrient-enriched or high conductivity waters (Holmes and Taylor 2015). Its presence here could be a result of nutrient enrichment from grazing animals such as llamas and alpacas. Zone 4 also records minor increases (<10%) in S. construens and S. pinnata that may indicate a return to the more open- water conditions recorded in Zone 1. The dominance (>60% relative abundance) of the aerophilic Hantzschia amphioxys in Zone 5 indicates less standing water and drier conditions in the bofedal. H. amphioxys was common in high-elevation wetlands ofDraft Jujuy province in Argentina (Seeligman et al. 2008) and similarly recorded in high abundances during the mature phase (high-centered, polygonal bog) of a peatland in Siberia (Rühland et al. 2000). It was also commonly recorded in surface peat samples from the Boreal Shield and Hudson Plains of Canada and closely linked to water table depth and low moisture levels (Hargan et al. 2015). Zone 6 records three taxa that alternate in dominance, each reaching over 50% relative abundance. Although H. amphioxys is present, it declines by ~1/3 of its previous relative abundances. A taxon we refer to as Pinnularia sp. [cf. kuetzingii] (Fig. 6) dominates the early part of this zone. P. kuetzingii has been recorded in springs associated with higher conductivities (Lai et al. 2019; Denys and Oosterlynck 2015), but without taxonomic certainty it is difficult to make ecological inferences. The rise in E. arculus, which replaces Pinnularia sp. [cf. kuetzingii] as the dominant taxon, likely indicates a drop in pH, as this taxon is considered acidophilic (pH 5.5 – 7.0; Rakowska 2000; Clarke 2003). An inferred pH decline is supported by the near disappearance of H. amphioxys, which is typically rarer in acidic soils (Johansen 2010). The dominance of Kobayasiella subtilissima in the surface-most intervals (4 – 0 cm depth) may indicate a further decline in pH, as this taxon is considered acidobiontic (pH < 5.5; van Dam et al. 1981; Hargan et al 2015). In contrast to E. arculus, which is epiphytic, K. subtilissima is unattached and more likely to be found in bog hollow habitats (as opposed to hummocks) where pH and water table are important drivers (Hargan et al. 2015). The second most dominant taxon in the surface interval is E. exigua, which is

16 associated with acidic conditions, but also wetter sites in peatlands (Hargan et al. 2015). However, in situ pH measurements of pH 7.8 taken from an open pool of water beside the coring site do not reflect acidic conditions, which suggests that habitat (i.e., wetter conditions) may play a more important role than pH in explaining the co-occurrence K. subtilissima and E. exigua.

Additional siliceous indicators – The changing ratios of diatoms to chrysophyte cysts, protozoan plates and phytoliths appear to track successional changes in the bofedal, as inferred by the diatoms. Although there is some variability in the earliest portion of the record (Zones 1 and 2), especially in the diatoms:plates ratio, there is no clear directional trend until the later stages of Zone 2 when all three indicators show increases in relation to diatom valves. This response would be predicted with increased amounts of Distichia growth as periphytic chrysophytes and testate amoeba would become more competitive with greater macrophyte abundance. Likewise, an increase in phytoliths would be expected with larger quantities of decomposing vegetation.Draft Beginning in Zone 3, there is greater variability in the ratios of diatoms:cysts and diatoms:phytoliths, but not diatoms:plates. We are hesitant to overinterpret every minor ratio change, but in general chrysophyte cysts, protozoan plates, and phytoliths show increased numbers relative to diatom valves in Zones 3-6 compared to Zones 1 and 2. The timing of these increases occur with the beginning of greater peat accretion rates (Fig. 4) and a diatom- inferred mature phase of the bofedal. The exception is in the surface-most intervals where ratios indicate declines in numbers of chrysophyte cysts, protozoan plates, and phytoliths. These declines coincide with a diatom-inferred return to wetter conditions and may reflect the competitive advantage of diatoms in wetter or more open water environments.

Diatom provenance in the Quelccaya Ice Cap – Freshwater diatoms have been identified in ice cores from the nearby Quelccaya Ice Cap (Fritz et al. 2015; Weide et al. 2017). Diatoms in glacial ice can have the potential to inform about the long-range transport of compounds and source provenance (Gayle et al. 1998) as well as more fundamental questions related to the dispersal of microorganisms. However, the utility of diatoms in glacial ice as proxies of past environmental change is limited, in part by a lack of diatom studies from this immediate region. In the Quelccaya ice core samples, the most encountered diatoms were Pinnularia borealis, Hantzschia amphioxys and Aulacoseira species (Fritz et al. 2015; Weide et al. 2017). The ecological affinities of these taxa led the authors to conclude that likely sources

were from freshwater lakes and wetlands that surround the ice cap. The most common diatoms identified in the QIC are also the dominant taxa in our peat core (Figs. 5 and 6), supporting the inference of nearby wetlands as a likely source.

Conclusions

Subfossil diatom assemblages and other siliceous indicators preserved in the study core show a rapid hydrosere succession from an open-water environment to a mature peatland over the span of a few centuries. The principal drivers responsible for the documented diatom changes appear to primarily reflect changes in bofedal hydrology and, to a lesser extent, pH, and nutrient enrichment. The sensitivity of diatoms to past hydrological variability demonstrates their potential to track climate and environmental changes that can affect water supply to bofedales including temperature-driven changes in glacial runoff, shifts in precipitation that recharge hillslope groundwater, and changes in evapotranspiration (Cooper et al. 2019). The rapid peat accretion rate recordedDraft at our study site is not unusual for the Andes (Earle et al. 2003; Benavides et al. 2013; Hribljan et al. 2015; Benfield et al. 2021) and demonstrates the potential of bofedales to rapidly expand and potentially act as carbon sinks. Rapid peatland development and high accumulation rates may be expected at our study site given near-continuous above-freezing conditions and a steady water supply from the adjacent glacier. It is also well documented that Andean people managed bofedales by controlling the water supply especially during the dry season (Domic et al. 2018), and the presence of cut irrigation channels at nearby bofedales suggests local herders certainly promoted peatland development in this region; however, no obvious irrigation channels were observed at our main study site. Our study tracks the paleoecology of a Peruvian bofedal since its inception and provides important baseline data that can be used to assess future changes.

Acknowledgments

This study was funded by the Natural Sciences and Engineering Research Council of Canada (NSERC) by a grant to JPS. We thank Felix Benjamín Vicencio, Teodoro Huaney Torres, Leo Camones Gamarra, and César Loli Chinchay for fieldwork support. Preston Sowell kindly provided the digital image in Fig. 1. Matthew Duda assisted in diatom identification and provided helpful comments on the manuscript. We also acknowledge Sheri Fritz and another reviewer whose comments improved this manuscript.

Competing interests: The authors declare there are no competing interests.

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Figure captions

Figure 1. Location of the main bofedal profile (red circle) and lower bofedal profile (green circle) in relation to Laguna Sibinacocha and the Quelccaya Ice Cap (QIC) in the Cordillera Vilcanota of Peru (a). Photograph with a view to the west showing the bofedal where the main profile was extracted (b). The glacier (appears as white) visible to the west of the coring site in (a) is visible in the background of the photograph in (b). Digital image provided by Preston Sowell. Base image: Digital Globe/Maxar

Figure 2. Plots showing unsupported and supported 210Pb activity (as 214Pb) and associated age-depth models (right side panels) derived from the constant-rate of supply (CRS) model for the main study bofedal profile and the lower bofedal profile.

Figure 3: Radiocarbon-based age-depth models for the main study profile (upper panel) and lower bofedal profile (bottom panel) generated in Clam v.2.3.4 (Blaauw, 2010). The main study site profile model was developedDraft using a smooth-spline with a smoothing factor of 0.4, whereas the lower bofedal profile model was developed using a linear interpolation. The black lines indicate the best fit age–depth model, with the 95% confidence interval shown in gray shading. Note: Probability distributions of 14C ages were plotted at the same height for all samples to improve readability.

Figure 4. Loss-on-ignition-derived organic matter content and X-ray fluorescence-derived Mn/Fe ratios and bromine concentrations, as well as peat accretion rates based on the best fit ages of the radiocarbon age-depth model for the main study core. The core images to the far right show clear demarcations between the clay-peat transition at ~96 cm depth and the location of the lower water table at ~30 cm depth, indicated by the change in peat colour and increase in Mn/Fe.

Figure 5: Subfossil diatom assemblage from the study bofedal core. The y-axis is reported as depth because when plotted as age the CONISS zones become too compressed near the surface to clearly observe changes. Only species with relative abundances above 5% are shown. The ratios of diatoms to chrysophycean cysts, protozoan plates, and phytoliths are shown on the right side of the plot. The stratigraphy is divided into six zones using CONISS; significant zones were determined through broken stick analysis.

Figure 6. Common taxa found in the main study core. 1. Encyonema hebredicum; 2. Encyonema norvegicum; 3. Encyonema alpinum; 4. Encyonema silesiacum; 5. Encyonema neogracile; 6. Encyonopsis falaisensis; 7. Navicula angusta; 8. Gomphonema gracile; 9. Gomphonema parvulum; 10. Eunotia bilunaris; 11. Eunotia arculus; 12. Eunotia exigua; 13. Pinnularia sp. [cf. kuetzingii]; 14. Pinnularia borealis; 15. Pinnularia subcapita; 16. Nitzschia paleacea; 17. Hantzschia amphioxys; 18. Ulnaria ulna; 19. Kobayasiella subtilissima; 20. Navicula TBI 4; 21. Chamaepinnularia musicola; 22. Staurosirella pinnata; 23. Staurosira construens; 24. Pseudostaurosira brevistriata; 25 Testate amoeba (full); 26, 27. Protozoan plates; 28. Aulacoseira spp.

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Table 1: Radiocarbon data for all samples from the main study core and lower bofedal core. Calibrated ages are from Calib 7.10 (Stuiver et al. 2020) and CALIBomb (one-year smoothing).

Composite Calibrated Age Laboratory 14C yr. Core depth F14C (±1) Range (2; cal. yr. Material ID BP (cm) BP) 1.1283 ± -47.7 to -42.8, Main 1 14-16 UOC-10804 >Modern Distichia leaves 0.0064 -9.5 to -8.9

1.1516 ± -43.5 to -39.9, Main 1 16-18 UOC-11410 >Modern Distichia leaves 0.0032 -9.7 to -9.4

1.1540 ± -43.3 to -39.6, Main 1 16-18 UOC-11411 >Modern Bulk peat 0.0032 -9.8 to -9.4

1.3125 ± -30.1 to -27.4, Main 1 50-52 UOC-10805 >Modern Distichia leaves Draft0.0095 -13.5 to -13.2 1.2739 ± -32.1 to -30.2, Main 1 52-54 UOC-11412 >Modern Bulk peat 0.0036 -13.2 to -12.9

-6 to -4, 20-70, 85- 0.9915 ± Bulk peat, Main 1 74-76 UOC-12495 68 ± 23 86, 94-103, 113-139, 0.0028 visible organics 230-240

0.9741 ± -5 to 324, Main 2 96-98 UOC-10807 211 ± 29 Bulk peat 0.0084 414-430

0.9524 ± 324-414, Main 2 98-100 UOC-11413 392 ± 24 Bulk peat 0.0028 428-492

0.9562 ± Main 2 98-100 UOC-11414 360 ± 58 290-497 Distichia leaves 0.0069

Lower 1.1696 ± -42.3 to -38.1, 34-26 UOC-12496 >Modern Bulk peat bofedal 0.0034 -10.3 to -9.6

Lower 0.9339 ± 72-74 UOC-12497 549 ± 25 507-549 Bulk peat bofedal 0.0029

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