https://orcid.org/0000-0001-8026-4679
Figures
Abstract
The southern Central Andes–or Puna–now contains specialized plant communities adapted to life in extreme environments. During the middle Eocene (~40 Ma), the Cordillera at these latitudes was barely uplifted and global climates were much warmer than today. No fossil plant remains have been discovered so far from this age in the Puna region to attest to past scenarios. Yet, we assume that the vegetation cover must have been very different from what it looks today. To test this hypothesis, we study a spore-pollen record from the mid Eocene Casa Grande Formation (Jujuy, northwestern Argentina). Although sampling is preliminary, we found ~70 morphotypes of spores, pollen grains and other palynomorphs, many of which were produced by taxa with tropical or subtropical modern distributions (e.g., Arecaceae, Ulmaceae Phyllostylon, Malvaceae Bombacoideae). Our reconstructed scenario implies the existence of a vegetated pond surrounded by trees, vines, and palms. We also report the northernmost records of a few unequivocal Gondwanan taxa (e.g., Nothofagus, Microcachrys), about 5,000 km north from their Patagonian-Antarctic hotspot. With few exceptions, the discovered taxa–both Neotropical and Gondwanan–became extinct from the region following the severe effects of the Andean uplift and the climate deterioration during the Neogene. We found no evidence for enhanced aridity nor cool conditions in the southern Central Andes at mid Eocene times. Instead, the overall assemblage represents a frost-free and humid to seasonally-dry ecosystem that prevailed near a lacustrine environment, in agreement with previous paleoenvironmental studies. Our reconstruction adds a further biotic component to the previously reported record of mammals.
Citation: Tapia MJ, Farrell EE, Mautino LR, del Papa C, Barreda VD, Palazzesi L (2023) A snapshot of mid Eocene landscapes in the southern Central Andes: Spore-pollen records from the Casa Grande Formation (Jujuy, Argentina). PLoS ONE 18(4): e0277389. https://doi.org/10.1371/journal.pone.0277389
Editor: Gongle Shi, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, CHINA
Received: October 25, 2022; Accepted: March 1, 2023; Published: April 5, 2023
Copyright: © 2023 Tapia et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Data are available within the manuscript and its Supporting Information files. The fossil specimens analyzed and illustrated in the present study are housed in the public repository of the University of Jujuy (Argentina), Palynological Laboratory, under the code PAL JUA (P) Cz/Plg. N° 001a-g(Eo).
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
The Puna-Altiplano encompasses a high elevation montane grassland in the Central Andes, extending from southern Peru, through Bolivia into northern Chile and Argentina [1, 2]. The landscape is a high plateau ranging from 3,700 m to 4,500 m above sea level, with snow-covered peaks and saline lakes. The climate ranges from temperate to cold and arid; average temperature ranges between 0°C and 15°C while precipitation ranges between 200 and 300 mm per year [3]. These climatic conditions associated with important disturbances like droughts and frosts have restricted the development of life but have favored the establishment of species able to cope with these conditions. For example, the vegetation is characterized by tall tussocks of bunchgrass, and shrubs such as Parastrephia lepydophilla (Asteraceae) as well as other cushion plants and sparse lichens and mosses [4]. Fauna, on the other hand, include vicuña (Lama vicugna), guanaco (Lama guanicoe), chinchilla (Chinchilla chinchilla), vizcacha (Lagidium viscacia), the Andean cat (Felis jacobita) and the large flightless bird Darwin’s rhea (Rhea pennata), among others [5–7].
The harsh climatic conditions prevailing in the Puna are mostly attributed to the Neogene uplift of the Andean Cordillera, which blocks the easterly humid winds, casting a shadow of dryness on the leeward [8–10]. However, the reconstructed climates from the Paleogene are remarkably different from those of today; during the Paleocene and early Eocene, sedimentological information (e.g., clay minerals and paleosols) from the Salta Group, in Northwestern Argentina, indicate humid-subtropical to tropical climates, although episodes of seasonality have been identified [11–14]. This paleoclimate supported a diverse biota with fish, crocodiles, lizards and mammals [15]. Also, spores and pollen grains demonstrated the existence of landscapes dominated by humid forests and lacustrine environments, with local arid conditions [16–21]. The onset of the Andean Cordillera uplift in the mid Eocene at these latitudes (22°S–26°S) [22, 23] have driven important environmental (e.g., [24]), and climatic shifts [25], although little is known about its impact on biotas (e.g., [26]). The available sedimentological information points to the existence of a depositional environment characterized by plains with localized ponds or shallow lakes and meandering fluvial systems with clay-rich floodplains [27]. Large herbivores as browsers (Leontiniidae) and some scavengers (Dasypodidae) along with small grazers, fruit and insect feeders (Prepidolopidae) have occurred across these landscapes [15, 28, 29]. Yet, little is known about the composition and structure of the plant cover, which is the primary support of habitats where these and other herbivores may have lived, fed on, and found shelter. Here, we present terrestrially-derived palynomorphs (largely pollen and spores) from deposits of the Casa Grande Formation (Figs 1 and 2), middle Eocene (approx. 40 Myr), exposed in northwestern Argentina. The Casa Grande Formation largely includes reddish oxidized sediments, where palynomorphs are substantially less abundant. Yet we were able to recover a productive layer with microscopic remains produced by a wide range of organisms (i.e., plants, fungi, insects).
(A) Map of South America indicating the region covered by the present study. (B) Map of northern Chile, southern Bolivia and northwestern Argentina, indicating the sample site (Casa Grande Fm, Jujuy Province). Maps were taken from USGS National Map Viewer (public domain).
Note the overall appearance of the terrestrial deposits cropping out in Jujuy (Casa Grande Fm.).
Geological and chronostratigraphic context
The Casa Grande Formation [30] includes red to reddish brown siltstones and sandstones (Fig 2) with a mean thickness of 800 m [31], and crops out along the Tres Cruces–Mina Aguilar area, in the Jujuy province, northwestern Argentina (Fig 1). This unit represents the onset deposition in the foreland basin [27, 31] contemporaneous with the initial construction of the Andean topography [23]. Montero-López et al. [27] proposed a subdivision of this sedimentary unit into the Casa Grande 1 and Casa Grande 2 sequences on the basis of a new and more detailed mapping analysis (Fig 3). The Casa Grande 1 sequence was previously assigned to the Lumbrera Formation of the Salta Group (e.g., [31, 32]). However, Montero-López et al. [27] recognized a sharp stratigraphic contact between the underlying dark reddish brown, highly cemented mudstones of the early Eocene Lumbrera Formation and the overlying reddish, gypsum-rich sandy siltstones of the Casa Grande 1 sequence. The ~160 m- thick Casa Grande 1 sequence, which preserves the palynomorphs we present and illustrate in this contribution, includes dark reddish orange fine-grained sediments, interbedded with green to dark gray claystones, carbonate and fine-grained sandstones (Fig 4). The depositional environment for this sequence is interpreted to be transitional between a vegetated mudflat with ponds and shallow lakes, and isolated channel belts. Until now, no radiometric ages have been published for the Casa Grande 1 sequence, although absolute age for the upper Lumbrera Formation–equivalent unit–provided an absolute U/Pb zircon depositional age of 39.9 ± 0.4 Ma (Eocene) [33]. Furthermore, fossil mammalian remains discovered from the Casa Grande 1 also support the Eocene age (e.g., [28, 34]).
Note the stratigraphic relationship between the Casa Grande I Fm. and other units used for comparison in the present analysis (Tunal Fm./Olmedo Fm., Mealla Fm., Maíz Gordo Fm., and Lumbrera Fm.).
Note the location of the palynologically-rich level located in the upper part of the section.
Material and methods
Palynological samples were collected from seven stratigraphic levels of the Casa Grande 1 sequence from a 165 m-thick section of red to reddish gypsum-rich sandy siltstones and green-gray mudstones, exposed in the Casa Grande valley (Figs 1–4). Permits to access and collect sedimentary samples were given by indigenous communities from the region (i.e., Casa Grande, Vizcarra and El Portillo). Palynomorphs are best preserved in unoxidized, fine-grained, primarily dark-colored (gray to black) sediments; the Casa Grande 1 sequence lacks suitable lithologies to preserve organic material, and hence any productive palynological level is very valuable for reconstructing past floras and environments. Seven samples were processed and sieved using standard palynological techniques [35, 36]), of which only one, from a lacustrine bed, yielded palynomorphs; the residue was permanently mounted in six palynological replicates using UV-curable acrylates gel [37]. The slides are housed in the palynological collection of Jujuy under the code PAL JUA (P) Cz/Plg. N° 001a-g(Eo). Photomicrographs were taken with a Leica ICC50W camera; the coordinates of the illustrated specimens refer to a Leica DM500 microscope. Pollen terminology follows Punt et al. [38]. Fossil spores and pollen grains were identified to species level and diagnosed to modern families, subfamilies, tribes or genera whenever possible (Table 1). We counted 546 palynomorphs (S1 Table). We used R software program, version 2.2.0 [39] for estimating similarities among the spore-pollen assemblages from the Casa Grande 1 sequence and those previously reported from other Paleogene localities cropping out in northwestern Argentina [i.e., Tunal/Olmedo Formation (early Paleocene [19–21]); Mealla Formation (late Paleocene [17]); Maíz Gordo Formation (Paleocene/Eocene [18]); Lumbrera Formation (Early Eocene [16])] based on presence/absence data (S2 Table) because most of the published works lack pollen counts (S3 Table). The Hierarchical Clustering (‘hclust’ function) was run using a distance matrix (‘dist’ function, ‘method: binary) from the R package ‘stats’ version 4.0.2. The number of samples and spore-pollen species recovered for each of the sedimentary sections used for comparisons vary ([16–21], S3 Table) and hence results should be interpreted accordingly: Tunal Fm (14 samples, 42 palynomorphs); Olmedo Formation (~11samples, 32 palynomorphs); Mealla Formation (4 samples, 36 palynomorphs); Maíz Gordo Formation (4 samples, 37 palynomorphs); Lumbrera Formation (12 samples, 19 palynomorphs).
(A) Todisporites minor (PAL JUA (P) Cz/Plg. N° 001c(Eo)+10 μm: 21.9–150.9). (B) Deltoidospora minor (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 10–135). (C) Leiotriletes sp. (PAL JUA (P) Cz/Plg. N° 001c(Eo)+10 μm: 9–138.9). (D) Polypodiaceoisporites cf. P. retirugatus (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 21.5–131). (E) Reboulisporites fuegiensis (PAL JUA (P) Cz/Plg. N° 001e(Eo)+25 μm: 3.5–139.4). (F) Zlivisporis sp. (PAL JUA (P) Cz/Plg. N° 001f(Eo)+25 μm: 16–151). (G) Podocarpidites sp. (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 3–153.5). (H) Microcachryidites antarcticus (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 3.9–130.5). (I) Equisetosporites notensis (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 4.5–154.6). (J) Smilacipites cf. S. herbaceoides (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 16.9–135.5). (K) Arecipites minutiscabratus (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 23–152.2). (L) Liliacidites vermireticulatus (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 24.2–126.9). (M) Liliacidites mirus (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 15–139). (N) Echimonocolpites sp. (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 5.2–128.9). (O) Nothofagidites anisoechinatus (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 13–128). (P) Nothofagidites saraensis (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 15.5–152.6). (Q) Retitrescolpites adultus (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 14–150.4). (R)Tricolpites asperamarginis (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 13.8–128.8). (S) Tricolpites membranus (PAL JUA (P) Cz/Plg. N° 001f(Eo)+10 μm: 14.9–152). (T) Tricolpites sp. (PAL JUA (P) Cz/Plg. N° 001c(Eo)+10 μm: 17–143. Scale bars: 10 μm (except in A, I, J, and N: 5 μm). Each morphotype name is followed by slide number and coordinates of Leica DM500 microscope held at the Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina.
(A) Beaupreadites sp. (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 7.5–142). (B) Siltaria dilcheri (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 17–151.2). (C) Foveotricolporites sp. (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 15.5–141.5). (D) Margocolporites tenuireticulatus (PAL JUA (P) Cz/Plg. N° 001a(Eo)+10 μm: 23–141). (E) Ailanthipites sp. (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 19–149). (F) Bombacacidites sp. (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 8–153.2). (G) Rhoipites baculatus (PAL JUA (P) Cz/Plg. N° 001c(Eo)+10 μm: 24–149.9). (H) Rhoipites guianensis (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 10–152). (I) Heterocolpites rotundus (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 9.5–152.5). (J) Baumannipollis sp. (PAL JUA (P) Cz/Plg. N° 001c(Eo)+25 μm: 21.3–138). (K) Graminidites sp. (PAL JUA (P) Cz/Plg. N° 001c(Eo)+10 μm: 15–145.9). (L) Pandaniidites sp. (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 13.9–130.2). (M) Corsinipollenites menendezii (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 2.5–137). (N) Psilatriporites desilvae (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 16.7–155). (O) Verrustephanosporites simplex (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 14,8–142,7). (P) Psilaperiporites circinatus (PAL JUA (P) Cz/Plg. N° 001f(Eo)+10 μm: 10.1–132.2). (Q) Periporopollenites sp. (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 7–151). (R) Periporopollenites polyoratus (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 9.5–152). (S) Gomphrenipollis sp. 1 (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 7–141). (T) Gomphrenipollis sp. 2 (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 4–130.5). Scale bars: 10 μm (except in L, N and R: 5 μm). Each morphotype name is followed by slide number and coordinates of Leica DM500 microscope held at the Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina.
(A) Biporipsilonites krempii (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 2–142.5). (B) Inapertisporitese edigeri (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 6–145.5). (C) Multicellites crassisporus (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 20.8–129.2). (D) Quilonia cf. Q. allepeyensi (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 4.1–126.7). (E) Polycellaesporonites bellus (PAL JUA (P) Cz/Plg. N° 001e(Eo)+10 μm: 7–141.5). (F) Scolecosporites modicus (PAL JUA (P) Cz/Plg. N° 001b(Eo)+10 μm: 7.5–153.4). (G) Scales of Lepidopteran wings (PAL JUA (P) Cz/Plg. N° 001e(Eo)+25 μm: 11–143.9). (H) Scales of Lepidopteran wings (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 19.8–141.5). (I) Scolecodont-like palynomorph (PAL JUA (P) Cz/Plg. N° 001e(Eo)+25 μm: 2–153.9). (J) Hydrozetes adult leg (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 16.5–144.5). (K) Filinia-type resting eggs (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 23.2–155). (L) Compact type sclerocyte (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 22.5–152). (M) Pediastrum boryanum (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 4–149.5). (N) Mougeotia sp. (PAL JUA (P) Cz/Plg. N° 001a(Eo)+10 μm: 6–145). (O) Planctonites stellarius (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 18–145). (P) Stigmozygodites ministigmosus (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 8.8–138). (Q) Spirogyra sp. 6 Martínez et al. 2008 (PAL JUA (P) Cz/Plg. N° 001d(Eo)+10 μm: 23.9–134.9). (R) Scenedesmus sp. (PAL JUA (P) Cz/Plg. N° 001e(Eo)+25 μm: 3.5–147.5). (S) Indeterminate dinoflagellate cyst 1 (PAL JUA (P) Cz/Plg. N° 001d(Eo)+25 μm: 21.7–141.8). (T) Indeterminate dinoflagellate cyst 2 (PAL JUA (P) Cz/Plg. N° 001c(Eo)+25 μm: 15–146.6). Scale bars: 10 μm (except A and H: 5 μm and 25 μm, respectively). Each morphotype name is followed by slide number and coordinates of Leica DM500 microscope held at the Museo Argentino de Ciencias Naturales, Buenos Aires, Argentina.
Results and discussion
The palynological assemblage recovered from the Casa Grande 1 sequence is relatively well preserved and relatively diverse. It includes spores, pollen grains, algae, among other fossil remains (fungi and zoological remains). We identified 43 spore and pollen species (Table 1, Figs 5–7), including 2 bryophytes, 4 pteridophytes, 3 gymnosperms, and 34 angiosperms. From these, we found the nearest living relatives (families, subfamilies, tribes or genera) of 37 species (2 ferns, 2 bryophytes, 3 gymnosperms, and 30 angiosperms); the remaining sporomorphs have doubtful or uncertain botanical affinity. From the 43 recognized taxa, 38 has been reported for the first time at Casa Grande 1 Fm., compared to the older Paleogene sediments cropping out nearby (i.e., Olmedo, Tunal, Mealla, Maíz Gordo, Lumbrera). These records, combined with those recorded earlier in northwestern Argentina, provide a total of 55 confidently assigned plant families for most of the early Paleogene (Paleocene-mid Eocene).
The fossil palynomorphs preserved in the terrestrial sediments of the Casa Grande 1 Formation come from a single sedimentary layer, yet they were transported from local to more distant sources by biotic (e.g., insects) or abiotic (e.g., wind, rivers) means. For example, we estimate that some of the non-pollen palynomorphs were preserved in situ or very close to the fossil site because they exhibit few adaptations to travel long distances. This is the case of palynomorphs assigned to algae such as Zygnemataceae (Mougeotia sp., Fig 7N; Spirogyra sp. 6, Fig 7Q; Stigmozygodites ministigmosus, Fig 7P), Scenedesmaceae (Scenedesmus sp., Fig 7R) and Hydrodictyaceae (Pediastrum biradiatum; P. boryanum, Fig 7M and P. duplex var. gracillimum), which strictly occur in freshwater ecosystems, as well the presence of fungal spores of Reduviasporonites suggests shallow aquatic habitats [40]. In addition, Filinia-type resting eggs (Fig 7K) are common in fresh-brackish ponds and lakes [41, 42]. Moreover, oribatid mites as Hydrozetes remains (Fig 7J) could also be restricted to freshwater habitats too (i.e., pools, ponds, raised bogs, lakes, slowly flowing waters, and submerse vegetation) [43]. Long distance transport of these palynomorphs (as coenobia or zygospores) has rarely been reported (e.g., [44, 45]). Additionally, the several fossil fungal spores recovered (e.g., Biporipsilonites krempii, Fig 7A; Inapertisporites edigeri, Fig 7B; Pluricellaesporites sheffyi (not illustrated); Multicellites crassisporus, Fig 7C; Scolecosporites modicus, Fig 7F; Polycellaesporonites bellus, Fig 7E) may have been produced at a short distance from the place where sporulation took place [41], hence indicating local occurrence. The presence of these sporomorphs at the fossil site, particularly those assigned to algae, indicate the occurrence of a shallow lake, or a pond, in agreement with previous sedimentological studies at the Casa Grande Formation [27]. Furthermore, other microscopic remains such as wing scales indicate the presence of moths or butterflies in the surroundings. Peaks in abundance of these fragments can be used by some authors to reconstruct insect outbreaks in ancient forests [46, 47]. Apart from that, scolecodont-like palynomorphs (Fig 7I) could be associated with mandibles or even body parts of a variety of freshwater arthropods (adults and larval stages) such as ants, copepods, oribatid mites, among others [48–50].
Other palynomorphs, such as spores of bryophytes and pteridophytes, may have also been produced by parent plants growing nearby. This is the case of bryophytes (Reboulisporites fuegiensis, Fig 5E; Zlivisporis sp., Fig 5F) and ferns [e.g., (Cyatheaceae/Dicksoniaceae, Deltoidospora minor, Fig 5B); (Osmundaceae; Todisporites minor, Fig 5A); (Pteridaceae, Polypodiaceoisporites cf. P. retirugatus, Fig 5D)]. We assume these spores have been transported by watercourses from relatively short distances. The presence of pollen grains assigned to aquatic plants such as water-plantains (Onagraceae, Corsinipollenites menendezii, Fig 6M) and duckweeds (Lemnoideae, Araceae; Pandaniidites sp., Fig 6L) also supports the occurrence of relatively quiet water bodies.
Other palynomorphs may have been produced within a short distance of the fossil site such as Osmundaceae (Todisporites minor, Fig 5A), Ricciaceae (Rebulisporites fuegiensis, Fig 5E), which most likely were transported to the pond from a more distant source either by insects or watercourses. Additionally, we suggest that the pollen grains of the Phytolaccaceae (Tricolpites membranus, Fig 5S), Fabaceae (Rhoipites baculatus, plate Fig 6G), Fabaceae Caesalpinioideae (Margocolporites tenuireticulatus, Fig 6D), the palm family Arecaceae (Arecipites minutiscabratus, Fig 5K; Verrumonocolpites sp.), Liliaceae (Liliaciditesmirus, Fig 5M), Ulmaceae Phyllostylon (Verrustephanosporites simplex, Fig 6O), Smilacaceae (Smilacipites cf. S. herbaceoides, Fig 5J), and Malvaceae Bombacoideae (Bombacacidites sp., Fig 6F) may have grown near the pond. Many of these (sub)families are well represented (S1 Table), including species with predominantly subtropical and seasonally dry modern distributions [51–53] and we suggest that they may have developed as patches near the pond, or as gallery forest along rivers (Fig 8). Other pollen species that became transported and preserved at the pond include the family Ephedraceae (Equisetosporites notensis, Fig 5I), commonly occurring throughout salt-stress and alkali-stress areas. Among non-pollen palynomorphs, fungi spores such as Multicellites crassisporus, Fig 7C; and Pluricellaesporites sheffyi (not illustrated) reinforce the hypothesis of humid conditions [40, 54].
The nearest living representatives of the discovered fossils indicate the presence of trees and shrubs nearby a vegetated pond with ferns and floating plants.
Pollen grains with clear long-distance adaptations such as those produced by southern beeches (Nothofagidites anisoechinatus and N. saraensis, Fig 5O–5P) and podocarps (Podocarpidites sp. and Microcachryidites antarcticus, Fig 5G and 5H) may have been blown in, probably from altitudinally zoned or edaphically restricted regions. The presence of these Gondwanan elements in tropical regions must not be surprising as today some of them (e.g., Podocarpus) coexist in the Southern Andean Yungas; a very humid narrow band of forest between the drier Gran Chaco region to the east and the dry, high altitude Puna region to the west. Some of the Gondwanan taxa that became regionally extinct in the Puna still prevail southwards in the humid and cool Andean region of Patagonia, such as the case of the southern beech genus Nothofagus. Additionally, the Tasmanian genus Microcachrys was detected in the Puna which is represented by low shrubs growing up to 1 m tall at high altitudes. It completely disappeared from South America, probably during the Miocene, after a major bloom of Gondwanan elements in Patagonia during the Oligocene [55].
A comparison with assemblages recovered from older units in northwestern Argentina (i.e., Tunal/Olmedo, Mealla, Maíz Gordo and Lumbrera formations) reveals that the assemblage from the Casa Grande 1 formation is quite different (Fig 9, S2 Table), particularly due to the reduced number of species in common. In fact, our cluster analysis (based on presence-absence data) shows a dramatically different hierarchical scheme with one major cluster including all Paleocene-early Eocene assemblages, all sister to the mid Eocene Casa Grande 1 Fm. as a single tip (Fig 9). Note that the stratigraphically closest Paleogene assemblages are clustered together, that is early Paleocene assemblages (Tunal/Olmedo Fm.) on one side and middle Paleocene (Mealla Fm.) and Paleocene/Eocene (Maíz Gordo Fm.) assemblages on the other. The slightly younger Lumbrera Formation stands next to those assemblages in our cluster analysis.
Hierarchical clustering showing the similarities among the spore-pollen records from the Casa Grande 1 sequence (this study) and those previously published from other nearby Paleogene sites based on presence/absence data (S2 Table). The number of samples and morphotypes of each site is given in Materials and Methods. The heterogeneity of either the fossil record and the sampling effort may influence the outcome of the hierarchical clustering, hence results should be interpreted accordingly.
The differences between our palynological assemblage and those previously studied from the Salta Basin–also supported by our cluster analysis–can be either because; 1) The number of species identified in our study from the Casa Grande 1 Fm. is dramatically different from those previously reported from older deposits (taxonomic bias hypothesis); 2) The environmental conditions prevailing during the accumulation of the palynomorph bearing level of the Casa Grande 1 Fm. favored the preservation of more spores and pollen types (taphonomic bias hypothesis); 3) The uplift of the Andean range (mid Eocene) may have driven shifts in the paleo-floras and, by extension, in the palynological assemblages (paleoecological hypothesis); 4) The increasing concentrations of atmospheric CO2 during the mid-Eocene climatic optimum probably triggered shifts in plant communities (paleoclimatic hypothesis); 5) The Casa Grande Fm. would be slightly younger than previously thought and therefore new and more modern floristic components were recorded (stratigraphical hypothesis). Among these, we reject hypothesis 1 because previous palynological works (e.g., [17–19, 56]) have been exhaustive, that is, they described and illustrated a large number of palynomorphs using a reasonable number of samples. In fact, the number of species identified for Casa Grande Fm. (43 species, this study) is very close to, for example, the 42 species identified for the Tunal Fm. (S2 Table). We tentatively reject hypothesis 2 because the reconstructed environmental conditions appear to have been terrestrial (i.e., ponds, swamps or shallow lakes) for all Paleogene sites from the region. We infer hypotheses 3 and 4 are the most likely largely because of the rise of typical arid-adapted elements (e.g., Poaceae and Ephedraceae), may have been driven, at least in part, by the effect of the initial stages of the Andean uplift. These families are common today in the southern Puna, and appear to have coexisted in the region since the accumulation of the Casa Grande Fm. (mid Eocene times) and onwards. On the other hand, the climatic optimum of the mid Eocene, promoted by an increasing concentration of atmospheric CO2, may have favored the rise of tropical elements; for example, we identified several species of palms and other tropical-affinity lineages (e.g., Malvaceae Bombacoideae, Smilacaceae). Finally, we cannot entirely reject hypothesis 5 because the pollen-bearing sediments of the Casa Grande Fm. can be slightly younger than mid Eocene, yet further analysis (either biostratigraphic or radiometric) is needed. However, the presence of typical species of the Paleocene-Eocene (e.g., Verrustephanoporites simplex) along with the complete absence of key open-habitat representatives from the Neogene such as the widely distributed spiny pollen grains of the Asteroideae (daisy family) gives us the notion that the Casa Grande Fm. might not be younger than Paleogene.
Overall, we assume that our reconstructed mid Eocene plant community has no close analogue in the modern South American vegetation, although a broad resemblance to the seasonally-dry forest of the Chaco becomes increasingly probable. This is largely because of the co-occurrence of Fabaceae, Malvaceae Bombacoideae and Ulmaceae Phyllostylon, which grow today particularly across the humid and dry Chaco. Their occurrence, along with the presence of several species of palms (Arecaceae), lead us to suggest subtropical or tropical conditions and frost-free winters. More importantly, our analysis supports previous assumptions indicating that the threshold elevation at which the orographic rain shadow effect became established at these latitudes, post-date the accumulation of the Casa Grande 1 Formation.
Supporting information
S1 Appendix. Systematic section.
This section includes brief and informal descriptive remarks and dimensions on selected species recorded in the Casa Grande 1 assemblage.
https://doi.org/10.1371/journal.pone.0277389.s001
(DOCX)
S1 Table. Identified mophotype list and frequencies (%).
Frequencies are based on a count of 546 palynomorphs. A black circle indicates frequencies lower than 0.1%.
https://doi.org/10.1371/journal.pone.0277389.s002
(DOCX)
S2 Table. Data matrix (presence/absence) of pollen and spores from the Paleogene of the Salta Group.
OF: Olmedo Formation, TF: Tunal Formation, MF: Mealla Formation, MGF: Maíz Gordo Formation, LF: Lumbrera Formation, CGF: Casa Grande Formation (this work).
https://doi.org/10.1371/journal.pone.0277389.s003
(DOCX)
S3 Table. Comparative sampling-count chart among Grupo Salta Basin sedimentary units.
https://doi.org/10.1371/journal.pone.0277389.s004
(DOCX)
Acknowledgments
We thank S. Mirabelli for processing palynological samples, Luz M. Tapia for drawing the Eocene reconstruction and the Editor and two anonymous reviewers for their helpful comments. We also thank Mirta Quattrocchio, Eduardo Bellosi and Paula Narvaez for providing us hard-to-find papers.
References
- 1.
Cabrera AL. Ecología vegetal de la puna. In: Troll C, editor. Colloquium Geographicum Band 9. Proceedings of the UNESCO México Symposium. Bonn: Dümmler in Kommission; 1966. p. 91–116.
- 2. Matteucci SD. Ecorregión Puna. In: Morello J, Matteucci SD, Rodríguez AF, Silva M, editors. Ecorregiones y Complejos Ecosistémicos Argentinos. Buenos Aires: Orientación Gráfica SRL; 2012. pp. 87–127.
- 3. Pulgar Vidal J. La agricultura y la reforestación en la región Puna. Colloque d’Études Péruviennes-, Aix en Provence, Faculté de Lettres et SciencesHumainesd’Aix, France, Aix-en-Provence, Centre d’Eludes Latino Américaines; 1966. pp. 273–279.
- 4.
Navone SM, Maggi A, Introcaso R. Desertification, climate change and land use in Argentine Puna region since 1975. In: Winslow M, Sommer S, Bigas H, Martius C, Vogt J, Akhtar Schuster M, Thomas R, editors. Understanding Desertification and Land Degradation Trends. Proceedings of the UNCCD First Scientific Conference; 22–24 September 2009; Buenos Aires, Argentina. Luxembourg: Office for Official Publications of the European Communities; 2011. pp. 140–141.
- 5.
Reboratti C. Situación ambiental en las ecorregiones Puna y Altos Andes. In: Brown A, Martinez Ortiz U, Acerbi M, Corcuera J, editors. La situación ambiental argentina. Buenos Aires: Fundación Vida Silvestre Argentina; 2006. p. 33–39.
- 6.
Matteucci SD. Ecorregión Puna. In: Morello J, Matteucci SD, Rodríguez AF, Silva M, editors. Ecorregiones y complejos ecosistémicos argentinos. Universidad de Buenos Aires, Facultad de Arquitectura, Diseño y Urbanismo: GEPAMA, Grupo de Ecologiìa del Paisaje y Medio Ambiente, Universidad de Buenos Aires: Orientación Grafica Editora. Buenos Aires, Argentina; 2012. p. 87–127.
- 7.
Perovic PG, Trucco Aleman CE, Tellaeche CG, Bracamonte JC, Cuello PA, Novillo A, et al. Mamíferos puneños y altoandinos. In: Grau HR, Babot MJ, Izquierdo AE, Grau A, editors. La Puna Argentina. Naturaleza y cultura. Serie Conservación de la Naturaleza, 24. Tucumán: Fundación Miguel Lillo; 2018. p. 182–206.
- 8. Masek JG, Isacks BL, Gubbels TL, Fielding EJ. Erosion and tectonics at the margins of continental plateaus. J Geohys Res. 1994; 99 (B7): 13941–13956.
- 9.
Alonso RN, Bookhagen B, Carrapa B, Coutand I, Haschke M, Hilley GE, et al. Tectonics, climate, and landscape evolution of the southern central Andes: the Argentine Puna Plateau and adjacent regions between 22 and 30 S. In: Oncken O, Chong G, Franz G, Giese P, Götze HJ, Ramos VA, et al., editors. The Andes. Berlin: Springer; 2006. p. 265–283.
- 10. Vera C, Baez J, Douglas M, Emmanuel CB, Marengo J, Meitin J, et al. The South American low-level jet experiment. Bull Am Meteorol Soc. 2006;87: 63–78.
- 11. Hyland EG, Sheldon ND, Cotton JM. Terrestrial evidence for a two-stage mid-Paleocene biotic event. PalaeogeogrPalaeoclimatolPalaeoecol.2015; 417: 371–378.
- 12. Andrews E, White T, del Papa C. Paleosol-based paleoclimate reconstruction of the Paleocene-Eocene thermal maximum, northern Argentina. Palaeogeogr Palaeoclimatol Palaeoecol. 2017; 471: 181–195.
- 13. Do Campo M, Bauluz B, del Papa C, White T, Yuste A, Mayayo MJ. Evidence of cyclic climatic changes recorded in clay mineral assemblages from a continental Paleocene-Eocene sequence, northwestern Argentina. Sediment Geol. 2018; 368: 44–57.
- 14. Do Campo M, Bauluz B, Payrola P, Yuste A, Mayayo MJ. Terrestrial record of cyclic early Eocene warm-humid events in clay mineral assemblages from the Salta basin, northwestern Argentina. Sediment Geol. 2021; 425: 106004.
- 15.
Powell JE, Babot MJ, García López DA, Deraco MV, Herrera CM. Eocene vertebrates of northwestern Argentina: annotated list. In: Salfity JA, Marquillas RA, editors. Cenozoic geology of the central Andes of Argentina. Salta: SCS publisher; 2011. p. 349–370.
- 16. Quattrocchio M. Contribución al conocimiento de la palinología estratigráfica de la Formación Lumbrera (Terciario Inferior, Grupo Salta). Ameghiniana. 1978; 15(3–4): 285–300.
- 17. Quattrocchio M, Volkheimer W, del Papa CE. Palynology and paleoenvironment of the “Faja Gris”; Mealla Formation (Salta Group) at Garabatal Creek (NW Argentina). Palynology. 1997; 21(1): 231–247.
- 18. Quattrocchio M, del Papa CE. Paleoambiente de la Secuencia Maíz Gordo (¿ Paleoceno Tardío-Eoceno Temprano?), Arroyo Las Tortugas, Cuenca del Grupo Salta (NO Argentina). Palinología y sedimentología. Spanish Journal of Palaeontology. 2000; 15(1): 57–70.
- 19. Volkheimer W, Novara MG, Narváez PL, Marquillas RA. Palynology and paleoenvironmental significance of the Tunal Formation (Danian) at its type locality, El Chorro creek (Salta, Argentina). Ameghiniana. 2006; 43(3): 567–584.
- 20.
Narváez PL. Palinoestratigrafía, paleoambientes y cambios climáticos durante el Cretácico final y Paleógeno de la Cuenca del grupo Salta, República Argentina. [Ph.D. thesis]. Mendoza: Universidad Nacional de Cuyo; 2009. Available from: https://planificacion.bdigital.uncu.edu.ar/objetos_digitales/5502/narvaez-tesisd.pdf
- 21.
Narvaez P, Volkheimer W. Palynostratigraphy and paleoclimatic inferences of the Balbuena and Santa Bárbara subgroups (Salta Group Basin, Cretaceous-Paleogene): Correlation with Patagonian basins. In: Salfity JA, Marquillas RA, editors. Cenozoic geology of the central Andes of Argentina. Salta: SCS publisher; 2011. p. 283–300.
- 22. Carrapa B, DeCelles PG. Eocene exhumation and basin development in the Puna of northwestern Argentina. Tectonics.2008; 27(1):1–19.
- 23. López Steinmetz RL, Ávila P, Dávila FM. Landscape and drainage evolution during the Cenozoic in the Salinas Grandes Basin, Andean Plateau of NW Argentina. Geomorphology (Amst). 2020; 353: 1–16.
- 24. del Papa C, Hongn F, Powell J, Payrola P, Do Campo M, Strecker MR, et al. Middle Eocene-Oligocene broken foreland evolution in the Andean Calchaquí Valley, NW Argentina: insights from stratigraphic, structural and provenances studies. Basin Res. 2013; 25: 574–593.
- 25. Ehlers TA, Poulsen CJ. Influence of Andean uplift on climate and paleoaltimetry estimates. Earth Planet. Sci. Lett. 2009; 281(3–4): 238–248.
- 26. Lagomarsino LP, Condamine FL, Antonelli A, Mulch A, Davis CC. The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae). New Phytol.2016; 210(4): 1430–1442. pmid:26990796
- 27. Montero López C, del Papa C, Hongn F, Strecker MR, Aramayo A. Synsedimentary broken‐foreland tectonics during the Paleogene in the Andes of NW Argentine: new evidence from regional to centimetre‐scale deformation features. Basin Res. 2018; 30: 142–159.
- 28. Bond M, López G. Los mamíferos de la Formación Casa Grande (Eoceno) de la provincia de Jujuy. Argentina. Ameghiniana. 1995; 32(3): 301–309.
- 29.
Babot MJ, García López DA, Deraco V, Herrera CM, del Papa C. Mamíferos paleógenos del subtrópico de Argentina: síntesis de estudios estratigráficos, cronológicos y taxonómicos. In: Muruaga CM, Grosse P, editors. Ciencias de la Tierra y Recursos Naturales del NOA: Relatorio del XX Congreso Geológico Argentino; 2017 August 7–11; Tucumán, Argentina. Tucumán. 2017. p. 730–753.
- 30. Fernández J, Bondesio P, PascualR. Restos de Lepidosiren paradoxa (Osteichthyes, Dipnoi) de la Formación Lumbrera (Eógeno, ¿Eoceno?) de Jujuy. Ameghiniana. 1973; 10(2): 152–172.
- 31. Boll A. Hernández RM. Interpretación estructural del área Tres Cruces: Boletín de Informaciones Petroleras. Tercera Época. 1986; 3(7): 2–14.
- 32. DeCelles PG, Carrapa B, Horton BK, Gehrels GE. Cenozoic foreland basin system in the central Andes of northwestern Argentina: Implications for Andean geodynamics and modes of deformation. Tectonics. 2011; 30(6): 1–30.
- 33. Del Papa CE, Kirschbaum A, Powell J, Brod A, Hongn F, Pimentel M. Sedimentological, geochemical and paleontological insights applied to continental omission surfaces: a new approach for reconstructing an Eocene foreland basin in NW Argentina. J South Am Earth Sci. 2010; 29(2): 327–345.
- 34. Herrera CM, Powell JE, del Papa CE. Un nuevo Dasypodidae (Mammalia, Xenarthra) de la Formación Casa Grande (Eoceno) de la provincia de Jujuy, Argentina. Ameghiniana. 2012; 49(2): 267–271.
- 35. Phipps D, Playford G. Laboratory techniques for extraction of palynomorphs from sediments. Papers. Department of Geology. University of Queensland. 1984; 11(1): 1–23.
- 36.
Traverse A. Topics in geobiology. Paleopalynology.2nd ed. Dordrecht, the Netherlands: Springer; 2007.
- 37. Noetinger S, Pujana RR, Burrieza A, Burrieza HP. Use of UV-curable acrylates gels as mounting media for palynological samples. Revista del Museo Argentino de Ciencias Naturales. 2017; 19(1): 19–23.
- 38. Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A. Glossary of pollen and spore terminology. Rev. Palaeobot. Palynol. 2007; 143(1–2): 1–81.
- 39.
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2019; URL https://www.R-project.org/.
- 40. Kalgutkar RM, Braman DR. Santonian to? earliest Campanian (Late Cretaceous) fungi from the Milk River Formation, Southern Alberta, Canada. Palynology.2008; 32(1): 39–61.
- 41.
Van Geel B. Non-pollen palynomorphs. In: Smol JP, Birks HJB, Last WM, editors. Tracking environmental change using lake sediments Dordrecht: Springer; 2002. Vol. 3. Terrestrial, Algal, and Siliceous Indicators. p. 99–119.
- 42. Cook EJ, Van Geel B, Van der Kaars S, Van Arkel J. A review of the use of non-pollen palynomorphs in palaeoecology with examples from Australia. Palynology. 2011; 35(2): 155–178.
- 43.
Weigmann G, Deichsel R. Acari: limnicoribatida. In: Gerecke R, editor. Süßwasserfauna von Mitteleuropa. Berlin: Springer; 2006 (Bartsch I, Davids K, Deichsel R, Di Sabatino A, Gabrys G, Gledhill T, et al. Chelicerata: Araneae/Acari I Vol. 7/2-1). p 89–112.
- 44. Hall SA. Atmospheric transport of freshwater algae Pediastrum in the American Southwest. Grana. 1998; 37: 374–375.
- 45. Kołaczek P, Karpińska Kołaczek M, Worobiec E, Heise W. Debaryaglyptosperma (De Bary) Wittrock 1872 (Zygnemataceae, Chlorophyta) as a possible airborne alga: a contribution to its palaeoeocological interpretation. Acta Palaeobotanica. 2012; 52(1): 139–146.
- 46. Montoro Girona M, Navarro L, Morin H. A secret hidden in the sediments: Lepidoptera scales. Front. Ecol. Evol. 2018; 6: 1–5.
- 47. Navarro L, Harvey AÉ, Morin H. Lepidoptera wing scales: a new paleoecological indicator for reconstructing spruce budworm abundance. Can J For Res. 2018; 48(3): 302–308.
- 48. Van Geel B. A palaeoecological study of Holocene peat bog sections in Germany and the Netherlands, based on the analysis of pollen, spores and macro-and microscopic remains of fungi, algae, cormophytes and animals. Rev Palaeobot Palynol.1978; 25(1): 1–120.
- 49. Van Geel B, Coope GR, Van Der Hammen T. Palaeoecology and stratigraphy of the Late glacial type section at Usselo (The Netherlands). Rev Palaeobot Palynol. 1989; 60(1–2): 25–129.
- 50. Shumilovskikh L, O’Keefe JM, Marret F. An overview of the taxonomic groups of non-pollen palynomorphs. The Geological SocietySpecialPublications. 2021; 511(1): 13–61.
- 51. Nielsen IC. Mimosaceae (Leguminosae-Mimosoideae). Flora Malesiana—Series 1, Spermatophyta. 1992; 11(1): 1–226.
- 52. Pennington RT, Prado DE, Pendry CA. Neotropical seasonally dry forests and Quaternary vegetation changes. J Biogeogr. 2000; 27(2): 261–273.
- 53. Zizka A, Carvalho Sobrinho JG, Pennington RT, Queiroz LP, Alcantara S, Baum DA, et al. Transitions between biomes are common and directional in Bombacoideae (Malvaceae). J Biogeogr. 2020; 47(6): 1310–1321.
- 54. Premaor E, Saxena RK, de Souza PA, Kalkreuth W. Fungal spores and fruiting bodies from Miocene deposits of the Pelotas Basin, Brazil. Revue de micropaléontologie. 2018; 61(3–4): 255–270.
- 55. Barreda VD, Palazzesi L, Pujana RR, Panti C, Tapia MJ, Fernández DA, Noetinger S. The gondwanan heritage of the eocene–miocene patagonian floras. J South Am Earth Sci. 2021; 107:103022.
- 56. Quattrocchio ME, Volkheimer W. Paleogene paleoenvironmental trends as reflected by palynological assemblage types, Salta Basin, NW Argentina. Neues Jahrb Geol Palaontol Abh. 1990: 377–396.