International Journal of Earth Sciences (2021) 110:995–1025 
https://doi.org/10.1007/s00531-021-02003-1
ORIGINAL PAPER
Late Neogene evolution of the Peruvian margin and its ecosystems: 
a synthesis from the Sacaco record
Diana Ochoa1  · Rodolfo Salas‑Gismondi1,2 · Thomas J. DeVries3 · Patrice Baby4 · Christian de Muizon5 · 
Alí Altamirano2 · Angel Barbosa‑Espitia6,7 · David A. Foster6 · Kelly Quispe8 · Jorge Cardich1 · Dimitri Gutiérrez8,9 · 
Alexander Perez1 · Juan Valqui1 · Mario Urbina2 · Matthieu Carré1,10 
Received: 21 October 2020 / Accepted: 1 February 2021 / Published online: 9 March 2021 
© The Author(s) 2021, corrected publication 2021
Abstract
The highly productive waters of the Humboldt Current System (HCS) host a particular temperate ecosystem within the 
tropics, whose history is still largely unknown. The Pisco Formation, deposited during Mio-Pliocene times in the Peruvian 
continental margin has yielded an outstanding collection of coastal-marine fossils, providing an opportunity to understand 
the genesis of the HCS ecosystem. We present a comprehensive review, completed with new results, that integrates geologi-
cal and paleontological data from the last 10 My, especially focusing on the southern East Pisco Basin (Sacaco area). We 
discuss the depositional settings of the Pisco Formation and integrate new U/Pb radiometric ages into the chronostratigraphic 
framework of the Sacaco sub-basin. The last preserved Pisco sediments at Sacaco were deposited ~ 4.5 Ma, while the overly-
ing Caracoles Formation accumulated from ~ 2.7 Ma onwards. We identified a Pliocene angular unconformity encompass-
ing 1.7 My between these formations, associated with a regional phase of uplift. Local and regional paleoenvironmental 
indicators suggest that shallow settings influenced by the offshore upwelling of ventilated and warm waters prevailed until 
the early Pliocene. We present an extensive synthesis of the late Miocene–Pleistocene vertebrate fossil record, which allows 
for an ecological characterization of the coastal-marine communities, an assessment of biodiversity trends, and changes in 
coastal-marine lineages in relation to modern HCS faunas. Our synthesis shows that: (i) typical endemic coastal Pisco ver-
tebrates persisted up to ~ 4.5 Ma, (ii) first modern HCS toothed cetaceans appear at ~ 7–6 Ma, coinciding with a decline in 
genus diversity, and (iii) a vertebrate community closer to the current HCS was only reached after 2.7 Ma. The genesis of the 
Peruvian coastal ecosystem seems to be driven by a combination of stepwise transformations of the coastal geomorphology 
related to local tectonic pulses and by a global cooling trend leading to the modern oceanic circulation system.
Keywords Pisco Basin · Sacaco · Mio-Pliocene transition · Humboldt current system · Faunal turnover · Biodiversity
*  Diana Ochoa 5 CR2P (CNRSMNHN, Sorbonne Université), Département 
 diana.ochoa@upch.pe Origines et Évolution, Muséum national d’Histoire naturelle, 
case postale 38, 57 rue Cuvier, 75231 Paris Cedex 05, France
1 Laboratorios de Investigación y Desarrollo (LID), Centro 6
de Investigación Para el Desarrollo Integral y Sostenible  Department of Geological Sciences, University of Florida, 
(CIDIS), Facultad de Ciencias y Filosofía, Universidad 241 Williamson Hall, Gainesville, FL 32611, USA
Peruana Cayetano Heredia, Av. Honorio Delgado 430, Lima, 7 Instituto de Investigaciones en Estratigrafía (IIES), 
Peru Universidad de Caldas, Calle 65 # 26-10, edificio Orlado 
2 Departamento de Paleontología de Vertebrados, Museo Sierra, Bloque B, segundo piso, Manizales, Colombia
de Historia Natural, Universidad Nacional Mayor de San 8 Programa de Maestría en Ciencias del Mar, Universidad 
Marcos, Lima, Peru Peruana Cayetano Heredia, Lima, Peru
3 Burke Museum of Natural History and Culture, University 9 Instituto del Mar del Peru (IMARPE), Dirección de 
of Washington, Seattle, WA 98195, USA Investigaciones Oceanográficas, Callao, Peru
4 Géosciences-Environnement Toulouse, UMR 10 LOCEAN Laboratory, Sorbonne Université 
CNRS/IRD/Université Paul Sabatier, 14 Avenue Edouard (UPMC)-CNRS-IRD-MNHN, Paris, France
Belin, 31400 Toulouse, France
Vol.:(012 3456789)
9 96 International Journal of Earth Sciences (2021) 110:995–1025
Introduction abundant, well-preserved, and diverse vertebrate fossil 
record of the western South American continental margin. 
The East Pisco Basin (EPB) is a forearc basin located along A wide range of coastal-marine fossil remains have been 
the Peruvian continental margin that has accumulated described, documenting the evolution and biogeographic 
marine sediments since the Eocene (Fig. 1; Thornburg and distribution of several living and extinct groups, including 
Kulm, 1981; Dunbar et al. 1990). The uplifted and exposed cetaceans, pinnipeds, crocodylians, sea birds, sharks, and 
portion of the EPB comprises extensive Eocene–Pleisto- aquatic sloths (e.g., Muizon and DeVries 1985; Esperante 
cene sedimentary successions that have yielded the most et al. 2008; Bianucci et al. 2016a, b). The giant raptorial 
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International Journal of Earth Sciences (2021) 110:995–1025 997
◂Fig. 1  a Major forearc basins existing along the Pacific Peruvian Recently, significant progress was made in characterizing 
continental margin, including the East Pisco Basin. Dotted areas the Miocene stratigraphic record from the Ica Valley in the 
show the East and West Pisco Basins (numbers 6 and 7). Map modi-
fied from Thornburg and Kulm (1981). The Coastal Cordillera cor- northern EPB (e.g., Di Celma et al. 2016a, 2017; Gariboldi 
responds to Outer Shelf High. b Onshore distribution of Mio-Pleis- et al. 2017; Bosio et al. 2019). Lithostratigraphic correla-
tocene marine deposits at the East Pisco Basin mapped according to tions across 100-m-thick successions kilometers apart were 
reports from the Peruvian Geological Service (INGEMMET 2017; defined and associated with absolute ages. This new cali-
maps 31  m, 31n, and 32n). Map shows location of the Ica Valley 
and the Sacaco sub-basin. Location and extension of the Caballas brated framework has been essential to characterizing the 
Basin (CB) as originally defined by Couch and Whitsett (1981) is chronology of the depositional phases from the northern 
also indicated. Basement rocks includes the Coastal Basal Complex EPB, particularly for the middle Mio-Pliocene Pisco For-
and the Saint Nicholas Batholith. Relief Map source: 30 arc-second mation. However, chronostratigraphic uncertainties remain 
DEM of South America (Data Basin Dataset), U.S. Geological Sur-
vey’s Center for Earth Resources Observation and Science (EROS). for the Sacaco sub-basin. Further efforts to establish reliable 
c Industrial seismic line RIB 93–76 across the Peruvian Pacific con- depositional ages and basin-wide (north–south) correlations 
tinental margin. From base to top, line shows seismic facies associ- are still required, so that observed biological and geologi-
ated with crystalline and sedimentary basement rocks affected by cal processes can be properly described and understood. In 
extensional and compressional events. Basement rocks are overlaid 
by high-frequency reflectors corresponding to the main Cenozoic this paper, we review, analyze, and integrate new and exist-
lithostratigraphic units of the basin (Paracas, Otuma, Chilcatay, and ing paleontological, sedimentological, and radiometric data 
Pisco formations). Reflectors associated with the Paracas and Otuma from the Pisco and Caracoles formations at the southern 
formations show grabens and half-grabens limited by synsedimentary EPB (Sacaco sub-basin; Fig. 1). We generate a new chron-
normal faults. The Otuma Formation is then separated from the over-
laying Chilcatay Formation by a regional erosional unconformity that ostratigraphic framework for the Mio-Pliocene sediments 
marked the end of the extensional tectonic regime. Growth strata and accumulated at the Sacaco area, which is then used to inter-
onlaps in the Chilcatay and Pisco formations recorded the uplift of an pret the sedimentary record and assess the evolution of the 
antiformal regional structure emerging to the south with the Coastal southern EPB. We further provide a detailed compilation of 
Cordillera (Outer Shelf High). Modified from Quispe et al. (2018) the existing vertebrate fossil record for the past 10 million 
years (My), with an updated taxonomy and stratigraphy. We 
sperm whale Livyatan melvillei (Lambert et al. 2010), the use this compiled dataset to define genera biostratigraphic 
aquatic sloth Thalassocnus (Muizon et al. 2003; 2004a), ranges and reconstruct the dynamics of the vertebrate faunas 
and the penguin Inkayacu paracasensis (Clarke et al. 2010) inhabiting the Peruvian coastal-marine settings during the 
are only a few of the most outstanding discoveries from the last 10 My. Finally, we assess how this late Mio-Pleistocene 
EPB. fossil assemblage compares to modern faunas associated 
Initial reconstructions of the late Miocene–early Plio- with the Humboldt Current System (HCS), and how the 
cene biotic and physical evolutionary history of the EPB ecosystem evolution is related to local and global environ-
have been based on the fossil record from Sacaco (Muizon mental changes.
and DeVries 1985), and have been focused on selected taxa 
(e.g., invertebrates in DeVries and Frassinetti 2003). This 
knowledge was only broadly defined due to the limited strati- Regional geology and stratigraphical setting
graphic and chronological control achieved, which occurs 
for three main reasons. First, rock exposures at Sacaco Definition of the East Pisco Basin
are highly fragmented, covered by recent eolian material, 
and have large thickness variations across space (Muizon The EPB starts at 13.5 ºS on the Peruvian continental margin 
and DeVries 1985; Brand et al. 2011). Second, the marine (Travis et al. 1976; Couch and Whitsett, 1981; Thornburg 
micropalaeontological record mostly relies on diatoms that and Kulm, 1981) and extends southward over more than 
show a tropical and high-latitude mixed signal. Thus, the 300 km. It is bounded to the west-southwest by the Coastal 
timing of bioevents may be puzzling, as it varies depending Cordillera (Outer Shelf High) and to the east-northeast by 
on whether authors use the Equatorial Pacific or the middle- the Coastal Batholith (Fig. 1). It progressively becomes shal-
to-high-latitude North Pacific zonation (Schrader and Ron- lower towards the south where the Coastal Cordillera shoals 
ning, 1988; Di Celma et al. 2016a; Gariboldi et al. 2017; forming several small perched depocenters (Thornburg and 
Solis 2018). Third, although absolute ages using radiometric Kulm 1981; Whitsett 1976). The southern EPB limit is thus 
(40Ar/39Ar, K/Ar) and isotopic (87Sr/86Sr) dating methods are not clearly defined, being broadly indicated as 14 ºS (Whit-
available (Table S1), their exact stratigraphic position is not sett 1976) or as 15.3 ºS (Marocco and Muizon 1988; Dunbar 
always well-defined in the Sacaco sub-basin (e.g., Muizon et al. 1990; León et al. 2008). Notwithstanding, comparable 
and Bellon 1986), which hinders basin-wide correlations Miocene sediments (with similar facies and correlatable fos-
(Brand et al. 2011). sil faunas) can be found from the Cerro Huaricangana in 
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 998 International Journal of Earth Sciences (2021) 110:995–1025
the northern EPB (15 ºS; see Balarezo et al. 1980; Dunbar 2020), which consequently has prevented a comprehensive 
et al. 1990; Stock 1990; León et al. 2008) up to the Sacaco understanding of the spatio-temporal evolution of the fossil 
area (15.2–16 ºS; see Adams 1906, 1908; Newell 1956; record at a basinal scale.
Caldas 1978). These similarities have caused the Miocene The Pisco Formation discontinuously extends from 
sediments to be considered as part of the same basin and so Pisco up to Yauca (13.5 º–15.6 ºS; Adams 1908; Caldas 
grouped under the same lithostratigraphic unit (i.e., the Pisco 1978; León et al. 2008) and shows variable thicknesses 
Formation; see Adams 1906, 1908; Caldas 1978; Fig. 1b). (200–1000 m; Dunbar et al. 1990; León et al. 2008; Di 
Whether the Sacaco area was an isolated small basin or was Celma et al. 2017). It unconformably overlies either Mio-
merely a local depocenter part of the larger EPB during the cene sediments from the Chilcatay Formation, Eocene-to-
Mio-Pliocene remains elusive. Herein, it will be considered Oligocene deposits from the Paracas and Otuma formations, 
as a small sub-basin of the EPB, containing the southern- or basement igneous rocks (Caldas 1978; León et al. 2008). 
most known deposits of the Pisco Formation. The top is capped by Plio-Quaternary alluvial, eolian, or 
marine deposits corresponding to the Cañete, Changuillo or 
Tectonostratigraphic setting Huamaní formations in the northern EPB (Petersen 1954; 
Davila 1989; León et al. 2008), and by the Caracoles or 
The EPB is structurally formed by numerous normal faults Pongo formations in the Sacaco sub-basin (DeVries 2020). 
and rotated blocks linked to grabens and semi-grabens with Although at the basin scale, the Pisco Formation appears 
predominant NW–SE orientations (Macharé 1987; Alarcón mostly flat-lying, there is structural deformation, expressed 
et al. 2005; Rustichelli et al. 2016; Viveen and Schlunegger as folding and NW–SE faulting that cuts and displaces strata 
2018). The EPB has been first regarded as formed under (e.g., DeVries and Jud 2018).
an extensional regime (Macharé et al. 1986; Macharé and The Pisco Formation contains various sedimentary facies 
Ortlieb, 1992; León et al. 2008) associated with the Nazca (e.g., Stock 1990; DiCelma et al. 2017) and a wide vari-
Plate subduction. This view was recently reassessed by ety of lithologies, including (tuffaceous or diatomaceous) 
Quispe et al. (2018) through integration and reinterpreta- siltstones and sandstones, diatomites, cherts, phosphorites, 
tion of surface and offshore seismic information, indicating and even dolomites (Dunbar and Baker 1988; León et al. 
that the EPB was under an extensional regime during the 2008). Based on its lithological features, it was informally 
Eocene, changing to a compressional setting from the late subdivided into a lower member dominated by tuffaceous 
Oligocene onwards (Fig. 1c). Neogene deformation associ- sands and an upper diatomaceous-rich member (Lower and 
ated with the Andean uplift generated thrust or reverse faults Upper Pisco; see Dunbar et al. 1990; León et al. 2008). In 
that induced flexural subsidence and promoted the tilting of the Sacaco sub-basin, the Pisco Formation predominantly 
some deposits. From the Pliocene onwards, migration of the consists of medium-grained massive to plane-parallel sand-
Nazca Ridge formed a high topographic anomaly and forced stones, occasionally interbedded with diatomites, tuffaceous 
the collapse of the sedimentary deposits to find an isostatic and diatomaceous sandstones, contrasting with the northern 
equilibrium, generating different responses in the upper crust sector where diatomaceous beds are regularly present. In the 
(Hampel 2002; Espurt et al. 2007). northern EPB, the Pisco Formation is composed of at least 
three fining-upward, unconformity-bounded transgressive 
Lithostratigraphic record of the Sacaco sub‑basin sequences (P0, P1, and P2 in Fig. 2; Di Celma et al. 2017). 
In the Sacaco sub-basin, only one intraformational uncon-
The successions here reviewed correspond to the last marine formity has been reported (Muizon and DeVries, 1985). 
sediments preserved in the Sacaco sub-basin (Fig. 1b), The unit is interpreted as a coastal to shallow-marine unit 
excluding the late Pleistocene marine terraces. deposited across open or protected shoreface and offshore 
shelf environments affected by waves and coastal upwelling 
The Pisco Formation (Dunbar et al. 1990; DiCelma et al. 2016b).
The Pisco Formation is one of the best-known lithostrati- The Caracoles Formation
graphic units of the EPB because of its abundant and well-
preserved fossils. In contrast to the attention given to the This unit was recently described and so far, only identified in 
fossil record, the sedimentary and stratigraphic context has the Sacaco sub-basin (DeVries 2020). The Caracoles Forma-
received much less consideration in the Sacaco sub-basin. tion was defined based on its unconformable boundaries and 
Existing studies have mostly addressed the unit’s tecton- distinctive lithological features (lesser ash content and finer 
ostratigraphic history using primarily the record from the grained sediments compared to the Pisco and Pongo forma-
northern EPB (e.g., Dunbar et al. 1990; León et al. 2008; Di tions, respectively). It ranges from 30 to 50 m in thickness, 
Celma et al. 2017, 2018; DeVries and Jud 2018; Bosio et al. and is composed of green olive-to-brown medium-grained 
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International Journal of Earth Sciences (2021) 110:995–1025 999
massive and bioturbated sandstones, interbedded with indu- and MG4-1Mz in Figs. 3f, S1). The MG4-1Mz sample was 
rated coquina beds containing bivalves, gastropods, and bar- collected from the same tuff reported by Muizon and Bellon 
nacles (DeVries, 2020). The unit unconformably overlies (1980) (Muizon, personal observation). Both samples are 
the Pisco Formation, and its upper boundary is also an ero- part of the Sacaco Monocline described by DeVries (2020) 
sive surface with the overlying Pongo Formation (Fig. 2). and should correspond to the oldest beds exposed across the 
Sediments from the Caracoles Formation are less deformed Sacaco locality. The overlying Caracoles Formation is only 
relative to the Pisco deposits, and have been interpreted to present in the northeastern hills above the valley (see Cerro 
have accumulated in shallow-marine settings, likely a (semi) Amarillo locality).
restricted embayment, during the late Pliocene–early Pleis-
tocene (DeVries 2020). Yauca locality
The Pongo Formation The Yauca succession is located between the villages of 
Chaviña and Yauca (Fig. 3a). Sediments from the Pisco 
This 70 m-thick lithostratigraphic unit contains the last Formation unconformably sit over igneous basement from 
marine-influenced sediments from the Sacaco sub-basin, the Proterozoic Coastal Basal Complex. The exposed sec-
exclusive of the late Pleistocene terraces (Macharé and Ort- tion is 12 m-thick and consists of at least four prominent 
lieb 1992). The Pongo Formation includes two depositional and indurated shell banks (SB 1–4 in Fig. 3e) with lateral 
sequences, separated by an intraformational unconformity variations to well-cemented, bio-supported whitish sand-
occurring few meters above an extended and well-developed stone beds containing articulated and disarticulated bivalves 
coquina bed that mainly contains shells of the gastropod and barnacles. Shell banks intercalate with immature grey 
Crepidula (DeVries, 2020). Sediments from the Pongo For- medium-to-coarse sand beds, that are massive, poorly 
mation have been considered to be accumulated in coastal cemented, and moderately sorted (see Supplementary Infor-
environments on high-energy sandy beaches during the mation). The section contains a few centimeters-thick, white 
Pleistocene (DeVries, 2020). tuff bed, between the third and fourth most distinctive shell 
banks (MG-138A in Figs. 3e, S1). The stratigraphic sec-
tion is capped by recent eolian material or the Panamerican 
Geological sections Highway 1S. The contact between the Pisco and Caracoles 
formations is thus either not exposed or likely not present.
Fieldwork data and sampling
Cerro Amarillo locality
New data presented herein are derived from field obser-
vations made along the Sacaco sub-basin (Fig. 3a, b; see The Cerro Amarillo locality is situated between the towns of 
Supplementary Information). The composite stratigraphic Puerto Lomas and Chaviña (Fig. 3a), and it provides one of 
section presented herein comprises the uppermost beds the best rock exposures of the upper Pisco and lower Cara-
from the Pisco Formation and the lowermost levels from coles formations at the Sacaco sub-basin (Fig. 3c). The Pisco 
the Caracoles Formation (Fig. S1). However, geologically Formation consists of alternating fine-to-medium-grained 
older localities (e.g., Aguada de Lomas and Sud-Sacaco), mature sands and tuffaceous sandy beds (see Supplemen-
were also surveyed to address Miocene faunas and deposi- tary Information). Towards the top, sands are replaced by 
tional settings of the sub-basin. an indurated sandstone bed containing abundant phosphate 
nodules, shark and ray teeth, and broken bones (Fig. S1). 
Sacaco locality The top of this indurated bed corresponds to an erosional 
surface marking the end of the Pisco Formation at the 
Sediments from the Sacaco locality include the homony- Cerro Amarillo locality (Fig. 3c). A 0.3–0.5 m-thick tuff 
mous prolific vertebrate fossiliferous level (SAO) of the bed occurs close to the top of the succession (MG3-09 in 
Pisco Formation (Fig. 3a; Muizon and DeVries 1985; Brand Figs. 3c, S1).
et al. 2011; Lambert and Muizon 2013). The Sacaco strati- Above the erosional unconformity, the Caracoles For-
graphic section is 10 m-thick and is primarily composed of mation crops out with a gentle northeast dip (S0 = 125/5, 
a thick yellow medium-grained sandy sequence, intercalated n = 5) compared to the moderate tilting of the Pisco unit 
with grey fine-grained tuffaceous sandstones, several shell (S0 = 120/12, n = 5). The Caracoles Formation comprises 
banks containing Anadara chilensis and Dosinia ponderosa dark-olive, massive to parallel laminated (sandy) silts, inter-
(SB in Figs. 3b, S1), and at least three well-developed tuff bedded with grey-to-yellowish fine-grained sandstones, and 
levels (see Supplementary Information). The uppermost two occasional centimeter-thick diatomites, blackish siltstones, 
tuffs were sampled for U/Pb radiometric dating (MG3-25 
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 1000 International Journal of Earth Sciences (2021) 110:995–1025
Fig. 2  Existing chronostratigraphic frameworks for the Sacaco sub- (Di Celma et  al. 2016a, b; Di Celma et  al. 2017; Gariboldi et  al. 
basin showing known age of main vertebrate fossiliferous localities 2017; Bosio et al. 2019). Box to the right shows updated chronostrati-
(Muizon and Bellon, 1980; 1986). Red vertical lines represent time graphic framework for the Sacaco sub-basin after this study. * Note 
bins used to assess faunal changes throughout time. Stratigraphic that abbreviations refer to localities rather than vertebrate-bearing 
sequences: P0, P1, and P2, from the northern EPB are also indicated levels
and thin shells banks. Near the base of the formation, a tuff comprises sediments from the Pisco and the Caracoles 
bed occurs (MG3-57 in Figs. 3c, S1). formations (DeVries 2020); however, the latter formation 
presents better exposures (Fig. 3d). The Pisco Formation 
Quebrada Caracoles locality mainly consists of medium-grained olive sandstones, inter-
calated with thin fine-grained grey indurated sand beds, 
The succession from the Quebrada Caracoles is located tuffaceous sandstones, shell banks, and thin layers of chert 
along an intermittent stream with the same name, 10 km and diatomaceous mudstone (Fig. S1; see Supplementary 
WSW of the Bella Union Village (Fig. 3a). The section Information). Upwards in the stratigraphic section, beds of 
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International Journal of Earth Sciences (2021) 110:995–1025 1001
Fig. 3  a Satellite image of the Sacaco sub-basin showing studied stratigraphic location of the MG3-57 tuff. d Unconformity between 
localities: Aguada de Lomas (AGL), Sacaco Classic (SAO), Sud- Pisco and Caracoles formations at Quebrada Caracoles, showing the 
Sacaco (SAS), Caracoles (CAR), Cerro Amarillo (CAM), Yauca typical geomorphological appearance of the Caracoles Formation. 
(YAU), and location of sampled volcanic tuffs (red stars). b Satellite Red star shows stratigraphic location of the MG-117A tuff. e View 
image of the Sacaco Classic area, showing location of the MG3-25 of the Yauca section (south to the Panamerican 1S highway). Yellow 
and MG4-1Mz tuffs (red stars), the latter sample corresponds to the lines indicate prominent shell banks (SB), red star shows stratigraphic 
same tuff dated by Muizon and Bellon (1980) (maps in A. and B. location of the MG-138A tuff. f Close-up view of the MG3-25 tuff 
adapted from Google Earth). c Unconformity between Pisco and Car- (Sacaco locality). Note that abbreviations refer to localities rather 
acoles formations (red dotted line) at Cerro Amarillo. Red star shows than vertebrate-bearing levels
chert and diatomaceous mudstones become frequent and are Strike and dip measurements [S0 = 26/8 for Pisco Formation 
associated with a tuff bed that was sampled for U/Pb radio- (n = 10) versus S0 = 322/5 for Caracoles Formation (n = 5)] 
metric dating (MG-117A in Figs. 3d, S1). As in the Cerro reveal that a nearly disconformable contact develops into an 
Amarillo locality, the top of the Pisco Formation is marked angular unconformity towards the northwestern part of the 
by the presence of a massive to nodular-bedded indurated Sacaco sub-basin.
sandstone, containing phosphate nodules, abundant lithic Sediments from the Caracoles Formation overlie the 
fragments, eroded shark teeth, and fragmented vertebrate erosional unconformity. At this locality, the Caracoles 
bones and shells (Fig. S1). The top of this indurated level, Formation is well exposed, reaching a total thickness of 
referred to as “Capa de los Dientes” by DeVries (2020), about 30 m. The lowermost part of the Caracoles Forma-
is overlain by a subtle erosional unconformity (Fig. 3D). tion (first five meters) locally consists of olive-to-brown 
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 1002 International Journal of Earth Sciences (2021) 110:995–1025
well-cemented sandstones, arranged in tabular bodies with- Sediments of the Pisco Formation in the Sacaco 
out evidence of bioturbation, but with common occurrences sub‑basin
of bivalve fragments and molds (see Supplementary Infor-
mation). The Caracoles Formation continues for another The total thickness of the Pisco Formation in the Sacaco 
25 m until interrupted by an erosional unconformity that sub-basin is unknown; however, based on our field observa-
places into contact with the overlying Pongo Formation tions, a conservative estimate would indicate that the unit is 
(DeVries 2020). at least 400 m thick. The sedimentary successions predomi-
nantly consist of light grey-to-brownish medium-grained 
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International Journal of Earth Sciences (2021) 110:995–1025 1003
◂Fig. 4  Details of sedimentary structures and facies present in the energy (Fig. 4f–j), in which fine suspended particles accu-
Pisco Formation in the Sacaco sub-basin. a Outcrop view of the mulated by either hemipelagic settling, bottom currents, or 
Pisco Formation at the Sud-Sacaco locality, showing typical irregu-
lar (erosive) bases, cross-stratification (xs) and parallel laminations fine-grained suspension currents, under low oxygen condi-
(pl), bioturbation marks (B). b Close-up of herringbone cross-strat- tions given the near absence of bioturbation (Fig. 4f). As 
ified (hcs) mid-to-coarse grained sandstones reflecting deposition in occurs in the northern EPB, there are dolomite nodules, 
tidally influenced settings, interbedded with finely laminated diato- which would likely have formed under increased porewater 
maceous beds. c Alternating levels of grey, olive and brownish mid-
grained sandstone layers, showing irregular erosive bases (eb), con- alkalinities and pH due to the reduction of sulfate (Gariboldi 
volute stratification (cs) and parallel laminations (pl). d Sedimentary et al. 2015; Gioncada et al. 2018). At times of reduced sili-
structures similar to the ones shown in photo 5C, also showing local ceous accumulation and low terrigenous supply, either by 
bioturbation (bt), large-scale cross-stratification (xs). e Close-up of rainfall or sea-level changes, sediment starvation occurred, 
sandstones showing hummocky cross-stratification (h-xs), typically 
formed on the shelf, close to the offshore transition zone. f Medium- also allowing the formation of phosporite-rich levels.
grained grey sandstone package with symmetric wave-related current The Pisco Formation in the Sacaco sub-basin is thus 
ripples, without bioturbation marks, typically occurring above the characterized by sand-sized terrigenous clastic deposits, 
storm-wave base. g Rock exposure facing to west at the Yauca local- interbedded with (bio)clastic and volcanic-derived deposits 
ity, showing massive to slightly bedded medium-grained sandstones 
with abundant bioturbation, overlaid by a prominent shell bank. h (Brand et al. 2011; DeVries, 2020). In the northern EPB, in 
Close-up of intensively vertically bioturbated sandstones. i Massive contrast, sediments with high biogenic siliceous contents 
tuffaceous sandstone (ts) to the base, irregularly passing to a medium- predominantly accumulated (e.g., Dunbar et al. 1990; León 
grained sandstone package with parallel laminations (pl), finish- et al. 2008; DiCelma et al. 2017). Clastic deposits shed into 
ing upwards with a hardground surface with Fe staining, boring and 
intense burrowing towards the top. j Rock exposure showing regular the Sacaco sub-basin from erosion of nearby topographic 
intercalations of parallel to massive beds of grey medium-grained highs, which mainly included early Miocene sediments 
sandstones, intercalated with hardground surfaces (hg s) with boring (~ 20 Ma) and Paleozoic basement igneous rocks (Table S3). 
and burrowing marks The distinctive nature of the northern and southern Pisco 
sediments (diatomaceous-rich versus sand-rich sediments) 
massive to faintly laminated sandstones, interbedded with suggests that by the late Miocene, the Sacaco sub-basin was 
yellow fine-to-medium-grained heterolithic sandstones, a shallower depositional area compared to the northern EPB, 
(siliceous-rich) limestones, and diatomites (Fig. 4). Sand- which could have been acting as an independent depocenter 
stone beds typically have sharp bases that are commonly within the EPB.
erosive, laterally discontinuous, and form packages with 
smooth to distinct fining- and thinning-upward trends 
(Fig. 4a–e). Sandstone packages containing parallel, cross-, Updated chronological framework
and/or hummocky cross-laminations also occur. Parallel 
laminations are often accompanied by different scale con- Existing chronological constraints
volute laminations (Fig. 4c–e). Massive or structureless 
sandstone beds with abundant bioturbation are also found A breakthrough in understanding the chronostratigraphic 
(Fig. 4g-h). Limestone or very fine-grained sandstone beds framework of the northern EPB successions was recently 
are typically grey (Fig. 4f), either finely laminated or lack- made by integrating radiometric and diatom-based biostrati-
ing internal structures, and with absent or poorly developed graphic data with sedimentological and stratigraphic studies 
bioturbation (Fig. 4j). These architectural characteristics, (e.g., Brand et al. 2011; Di Celma et al. 2017; Gariboldi 
along with the faunal remains, indicate a great variability et al. 2017; Bosio et al. 2020). In the northern EPB, at least, 
of high-energy depositional conditions, varying from wave- three unconformity-bounded sequences for the Pisco Forma-
dominated shoreface (> 5 mbsl) to offshore settings (> 100 tion have been defined from oldest to youngest as follows: a 
mbsl), with episodes of deposition occurring in the foreshore basal Langhian–Serravallian P0 sequence (14.8–12.4 Ma), 
area as evidenced by the array of sedimentary structures a Tortonian P1 sequence (~ 9.5–8.6 Ma), and a Tortonian-
and the occurrence of shell banks (Fig. 4g). Sedimentary Messinian P2 sequence (from ~ 8.4 Ma to at least 6.71 Ma) 
structures, such as hummocky cross-stratification, indicate (See Fig. 2; Di Celma et al. 2017; Bosio et al. 2019; 2020). 
accumulation in wave-dominated infralittoral environments, Younger Pisco deposits exposed north of the Ica Valley still 
under processes of turbiditic, longshore wave, or storm-dom- need to be integrated into this stratigraphic framework.
inated currents (Fig. 4d). Processes related to density flows The chronostratigraphic framework of the Sacaco sub-
at stream mouths, turbidity currents (convolute structures basin (based on radiometric datings, strontium isotopes dat-
present in fine-to-mid-grained sandstones; Fig. 4F), and ings, and biostratigraphy, Table S1) is in contrast less refined 
tidal-influenced currents (herringbone cross-stratification; as rock exposures are disconnected and often covered with 
Fig. 4b) locally occurred as well. Deposition of limestones recent eolian material (see Fig. 3b–d). Ages of the vertebrate 
and/or fine-grained sand indicates phases of relatively low levels for this sub-basin are estimated in relation to closely 
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 1004 International Journal of Earth Sciences (2021) 110:995–1025
located tuffs, isolated 87Sr/86Sr isotopic measurements and/ grains. Further details on geochemical analysis and zircon 
or the overall fossiliferous content (Muizon and Bellon U/Pb age determinations are given in the Supplementary 
1980, 1986; Muizon and DeVries 1985; Ehret et al. 2012). Information.
The stratigraphic succession of fossiliferous localities is, to 
date, defined as follows: (i) Tortonian sediments occur at U/Pb radiometric ages
El Jahuay (Alto Grande; ~ 9.5–7.46 Ma), Aguada de Lomas 
(~ 8.8–7.9 Ma), and Montemar (~ 7.3 Ma); (ii) Messinian In general, zircon data show a wide range of single grain 
deposits at the Sud-Sacaco locality (~ 6.6–5.9 Ma); and ages, implying a variety of sources (especially at Quebrada 
(iii) Messinian–Zanclean sediments at the Sacaco locality Caracoles and Yauca) and that some tuffs incorporated 
(~ 5.89–3.9 Ma) (Fig. 2; Muizon and Bellon 1980, 1986; reworked detrital zircons (Table S3). Given the confidence 
Ehret et al. 2012). Other fossiliferous localities without intervals found in each sample, we interpreted these radio-
absolute ages but considered as Pliocene or Plio-Pleistocene metric ages as representatives of the depositional age of 
based on their stratigraphic position or paleontological con- each sampled bed (Table 1). The oldest tuffs correspond to 
tent include: Yauca, Quebrada Caracoles, Cerro Amarillo, those from the Sacaco locality, with maximum 206Pb/238U 
Quebrada Pongo, Acarí, and Chaviña (DeVries 2020). depositional ages of 5.85 ± 0.031 Ma and 5.74 ± 0.056 Ma 
Geographic and/or stratigraphic uncertainties have so far (MG3-25 and MG4-1Mz; Fig. S4). Note that the latter tuff 
precluded any accurate stratigraphic correlation between corresponds to the one reported as 3.9 ± 0.2 Ma by Muizon 
locations within the Sacaco sub-basin or with the northern and Bellon (1980; see Fig. 3f). The tuff collected below the 
EPB (see Brand et al. 2011). As a consequence of that, con- angular unconformity at Cerro Amarillo (MG3-09) yielded 
troversies remain regarding the relative age, stratigraphic five crystals with a 206Pb/238U mean age of 5.645 ± 0.032 Ma 
position, and geographic extension of fossiliferous beds and (Fig. S4). The next oldest tuffs were collected at Yauca (MG-
localities in the Sacaco sub-basin (Brand et al. 2011; Lam- 138A) and Quebrada Caracoles (MG-117A). The former 
bert and Muizon 2013). We thereafter present an updated contained 14 crystals with an estimated 206Pb/238U age of 
and more precise chronological framework for the Sacaco 4.85 ± 0.044 Ma and the latter included 2 crystals with an 
sub-basin based on new radiometric ages. estimated age of 4.541 ± 0.061 Ma. Finally, the youngest tuff 
occurs a few centimeters above the angular unconformity at 
Dating methods Cerro Amarillo (MG3-57), with three crystals indicating an 
estimated age of 2.7 ± 0.035 Ma (Fig. S4).
Six tuffs were collected along the Sacaco sub-basin The youngest Pisco sediments thus occur at the Quebrada 
(Table 1), five from the Pisco deposits [Sacaco (n = 2), Caracoles (4.541 ± 0.061 Ma) and Yauca (4.85 ± 0.044 Ma) 
Yauca (n = 1), Quebrada Caracoles (n = 1), and Cerro Ama- localities (Table 1). These U/Pb radiometric ages confirm an 
rillo (n = 1)], and one from the lowermost known Caracoles early Pliocene age for the uppermost known sediments from 
sediments (Quebrada Caracoles). 206Pb/238U weighted mean the Pisco Formation in the Sacaco sub-basin.
ages were used to calculate maximum depositional ages, Tuffs from the Sacaco locality yield older mean ages 
using a weighted mean of at least the three youngest zir- (5.85–5.74 Ma). This age is a robust time constraint, con-
con grains reported with standard error uncertainties at 2σ sidering the large population (n = 35) of similar age zircons 
and 95% confidence intervals (Table 1). Only in the case of found in one of the samples (Fig. S4; Table 1). These results 
samples MG4-1Mz (Sacaco locality) and MG-117A (Que- contrast with a K/Ar radiometric analysis by Muizon and 
brada Caracoles) ages were estimated using the two youngest Bellon (1980) that estimated the age of the Sacaco locality 
Table 1  U–Pb analyses of zircon for six tuffs sampled in the Sacaco sub-basin
Locality Sample ID Lat Long Weighted mean Standard error (σ) Confidence interval Formation
age (Ma)
Sacaco MG3-25 − 15.551 − 74.737 5.848  ± 0.031 0.060 (n = 35/36) Pisco
Sacaco MG4-1Mz − 15.551 − 74.736 5.741  ± 0.056 0.706 (n = 2/3)* Pisco
Yauca MG-138A − 15.655 − 74.587 4.85  ± 0.044 0.086 (n = 14/17) Pisco
Quebrada Caracoles MG-117A − 15.502 − 74.754 4.541  ± 0.061 0.119 (n = 2/4)* Pisco
Cerro Amarillo MG3-09 − 15.551 − 74.721 5.645  ± 0.032 0.089 (n = 5/6) Pisco
Cerro Amarillo MG3-57 − 15.551 − 74.722 2.7  ± 0.035 0.68 (n = 3/4) Caracoles
Radiometric ages were calculated from the weighted average of a coherent zircon population (n ≥ 3), excepting in those samples indicated with 
*, whose ages were obtained from the two youngest zircon crystals
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International Journal of Earth Sciences (2021) 110:995–1025 1005
as 3.9 ± 0.2 Ma. Such radiometric age differences are likely and calcitic-cemented clasts, basement rock fragments, and 
related to some argon loss associated with alteration affect- abraded vertebrate fossils from the Pisco Formation (Fig. 
ing the K/Ar system in biotites. Unfortunately, corrections S1; DeVries 2020). Note that these layers display similar 
to the K/Ar ages or updates to the newest standard reference lithological features but differ in age. At the Sacaco sub-
ages for K/Ar and 40Ar/39Ar radiometric ages from Muizon basin, the Pisco beds are often (sub)horizontally lying. 
and Bellon (1980) are not possible as parameters, such as However, some late Miocene beds locally exhibit dips of 
the irradiation flux, are unknown. Nevertheless, our results up to 30 degrees along the axis of an N-S monocline struc-
agree with previous strontium-based (87Sr/86Sr) isotopic ture (Sacaco Monocline of DeVries 2020) that runs for over 
dates yielding an average value of 5.89 Ma (6.76–4.86 Ma; 10 km. Whether the monocline corresponds to a reactivation 
Ehret et al. 2012), as well as with an unpublished Ar/Ar date fault or an extensional/compressional fault propagation fold 
of 5.75 ± 0.05 Ma (reported by Ehret et al. 2012) obtained is unknown. However, previous works have indicated the 
from the “DV-514–2 Snee” tuff (Fig. 3f). These combined presence of a compressional phase affecting the Peruvian 
results imply that preserved sediments from the Sacaco coast around 12–16 ºS (e.g., Macharé and Ortlieb 1992). The 
locality (and its associated fossiliferous content) were depos- angular nature of the Pisco-Caracoles surface, along with 
ited between 5.7 and 5.8 Ma, i.e., almost 2 My earlier than the presence of a monocline deformation structure, provides 
previously thought. evidence for the tectonic origin of this erosional surface and 
Finally, the oldest known sediments from the Pisco For- thus can be related to a (local) upheaval event. Such surficial 
mation in the Sacaco sub-basin were defined as ranging uplift would have subaerially exposed the sediments depos-
from ~ 9.6 Ma, based on two K/Ar radiometric ages from El ited in the Sacaco sub-basin around 4.5 Ma, promoting their 
Jahuay (Alto Grande; Muizon and Bellon 1980). We have later subaerial erosion.
demonstrated that the youngest known Pisco sediments 
occur at Quebrada Caracoles and were deposited during the 
early Pliocene (Table 1). Hence, the time span encompassed Paleoceanographic conditions
by the Pisco Formation in the Sacaco sub-basin should now 
be referred to as ranging from ~ 9.6 to 4.5 Ma (Fig. 2). Evidence from the sedimentary and fossil record
Modern oceanographic conditions along the Peruvian con-
A regional unconformity: evidence tinental margin are determined by the coastal upwelling 
of an early Pliocene episode of Andean uplift system, which brings to the surface cool nutrient-rich deep 
waters that promote high rates of primary production (Tog-
The presence of a hiatus spanning the Mio-Pliocene transi- gweiler et al. 1991; Pennington et al. 2006), and a permanent 
tion in the northern EPB has been previously documented shallow Oxygen Minimum Zone (OMZ). The intensity and 
(Dunbar et al. 1990; León et al. 2008). In the Sacaco sub- extent of this OMZ are controlled by high oxygen demand, 
basin, the uppermost Pisco sediments are capped by an ocean stratification, and the advection of low-oxygen deep 
unconformity that places them in contact with Plio-Pleisto- waters (Helly and Levin 2004). Presently, the OMZ extends 
cene deposits. DeVries (2020) mapped the regional exten- up to 100 km offshore and ranges from 50 to 600 mbsl across 
sion of this erosive surface across the sub-basin. The time the Peruvian continental margin (Helly and Levin, 2004; 
gap represented by the Pisco-Caracoles unconformity was Pennington et al. 2006; Gutiérrez et al. 2009; Salvatteci et al. 
previously estimated as between 4 and 1 My based on the 2014). However, reconstructions of the OMZ variability dur-
malacological content (DeVries, 2020). The radiometric ing the late Quaternary have demonstrated that its intensity 
ages found below and above the unconformity at Cerro and extent across the continental margin fluctuate at dif-
Amarillo (5.6 ± 0.032 Ma and 2.7 ± 0.035 Ma, respectively; ferent geological timescales (Arntz et al. 2006; Paulmier 
Table 1) indicate that the angular unconformity represents and Ruiz-Pino 2009; Gutiérrez et al. 2006; Cardich et al. 
a time gap of about 2.9 My at this locality. Nonetheless, at 2019), showing also a decoupling between oxygen values 
the sub-basin scale, the unconformity only represents 1.8 and paleonutrient proxies (Salvatteci et al. 2016).
My considering the younger ages found for the Pisco sedi- The EPB is currently located in front of a strong and 
ments at Quebrada Caracoles (4.54 ± 0.061 Ma). Further- permanent upwelling cell (14-l6°S; Tarazona and Arntz 
more, it remains uncertain whether sediment accumulation 2001). Reconstructing past upwelling and oxygen condi-
was reactivated at the same time (~ 2.7 Ma) throughout the tions prevailing during the deposition of the Pisco Formation 
Sacaco sub-basin. is needed as this oceanographic feature would dictate the 
The unconformity, although of low angle, is angular in ecological constraints for past marine ecosystems, coastal 
nature (generally 5–10º), and occurs at the top of indurated climatic regimes, sedimentation processes, and possibly the 
brownish layers containing authigenic nodules, phosphatic preservation of fossil faunas. The sedimentary record shows 
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 1006 International Journal of Earth Sciences (2021) 110:995–1025
that silica fluxes were common in the EPB during the accu- Miocene Pisco sediments based on the presence of warm-
mulation of the Pisco Formation, especially at the northern water or tropical mollusks and elasmobranch taxa (DeVries 
EPB, where abundant diatomite beds exist (Dunbar et al. and Frassinetti 2003; Bosio et al. 2020). Whilst, cold seawa-
1990; Brand et al. 2004; León et al. 2008). These diatomite- ter temperatures were estimated for the late Miocene based 
rich sequences provide indication of high productivities and on δ18O derived from bone phosphates (13–17.2 ºC; Amiot 
frequent upwelling conditions (Marty 1989; Dunbar et al. et al. 2008). However, the recovery of two extinct long-
1990; Schrader and Sorknes 1991; Abrantes et al. 2007). snouted crocodylian taxa (Piscogavialis and a Tomistominae 
The Pisco Formation record is, however, less conclusive taxon) from Mio-Pliocene sediments of the Pisco Formation 
regarding a paleo-OMZ. Most of the Pisco sediments from (Table S2) challenges the latter isotope-based temperature 
the Sacaco sub-basin correspond to silt and sandstones hav- reconstructions. Furthermore, remains of a long-snouted 
ing massive or thick planar- to cross-laminations (Fig. 4; crocodylian form were also found in Miocene deposits from 
e.g., Muizon and DeVries, 1985) with frequent and abun- Chilean coasts (at 27 ºS in the Bahia Inglesa Formation; 
dant horizontal and vertical trace fossils, including ichnofos- Walsh and Suárez 2005). Crocodylians are ectothermic ver-
sils such as Thalassinoides, Ophiomorpha, and Gyrolithes tebrates limited to warm to temperate aquatic environments 
(Fig. 4; DeVries, 2020) accumulated under well-oxygenated (Grigg and Kirshner 2016), so their record is indicative of 
conditions at the fair-weather and storm-wave base (above warm coastal seawaters. Today, the southernmost limit of 
100 mbsl). It remains unclear whether a permanent OMZ a crocodylian in the eastern Pacific (i.e., Crocodylus acu-
existed at deeper depths (below 100 m depth). However, the tus) occurs in northernmost Peru (~ 4 ºS; Thorbjarnarson, 
occasional presence of fine-laminated and non-bioturbated 2010), where sea surface temperatures (SST) average 20–25 
limestone and diatomaceous beds in the Sacaco sub-basin ºC (Ayón et al. 2008). The fossil record of these vertebrates 
indicate sporadic reduced infaunal activity at the seafloor. in Peru and Chile (Muizon and DeVries, 1985; Kraus 1998; 
Furthermore, local occurrences of deep-water dysoxic to Walsh and Suárez 2005) thus indicates that late Miocene 
anoxic benthic foraminifers’ genera, such as Cancris, Val- SST along the Pacific coast (12–28 ºS) were substantially 
vulineria, and Nonionellina (León et al. 2008), indicate that, higher than today. These warm conditions would have 
besides having episodes of reduced content of dissolved remained at least until ~ 4.5 Ma, when the last occurrence 
oxygen, the depositional area also underwent deepening of the gavialoid Piscogavialis in the EPB is observed. This 
phases moving from the inner–outer shelf to the continental fossil evidence is consistent with paleotemperature recon-
slope (below 100 mbsl). The sporadic occurrence of fine- structions from oxygen isotope analyses performed on 
laminated beds and benthic foraminifers evidences that, at late Miocene bivalve shells (Chlamys and Anadara) from 
those depositional sites, such anoxic events would have been the Sud-Sacaco locality that indicate warmer than present 
transient, whereas high-oxygen seafloor conditions persisted temperatures (20–30 ºC; Muizon 1981), contrasting with 
during most of the deposition of the Pisco Formation at the colder values (12–20 ºC) obtained from two specimens 
Sacaco sub-basin (~ 10–4.5 Ma). Similar oxic conditions (Mesodesma and Eurhomalea) from a younger Pleistocene 
were interpreted for the northern EPB (Esperante et al. terrace lying above the Pisco Formation (Muizon, 1981).
2015). Open Ocean Connectivity of the Sacaco sub-basin. The 
Therefore, continuous high primary productivity condi- EPB is bounded to the west-southwest by the Coastal Cor-
tions existed in the EPB either related to upwelling or verti- dillera (Outer Shelf High in Fig. 1a), and it remains unclear 
cal mixing, based on the lithological and sedimentological how this regional topographic feature would have affected 
features of the Pisco Formation. However, such high pro- the depositional settings at the Sacaco sub-basin, consider-
ductivity did not necessarily translate into persistent and ing its shallower depositional settings compared to the north-
extended low-oxygen conditions in those areas from the ern EPB. The significant shoaling of the Coastal Cordillera 
Sacaco sub-basin where the Pisco sediments were accu- reported from 14 ºS to 16ºS (Thornburg and Kulm 1981) 
mulated. It remains unknown if an OMZ was permanently could have induced (semi)isolated conditions for this sub-
established at greater depths in the continental margin dur- basin, potentially influencing its temperature and chemistry. 
ing Mio-Pliocene times, or how oxygen availability in the Therefore, defining the degree of connectivity of the Sacaco 
water column and at sediment–water surface interface did sub-basin with the open ocean is key for determining the 
vary in time. influence of the coastal upwelling, local temperature, pro-
ductivity, and the occurrence of anoxia.
Coastal sea surface temperatures The open ocean connectivity can be assessed to some 
level using strontium isotope ratios. The residence time of 
Coastal climatic conditions along the Peruvian coast during the 87Sr/86Sr ratio (≈106 years) in oceanic waters is consider-
Mio-Pliocene times are still poorly known. Warmer than ably larger than the ocean water mixing rates (≈103 years; 
present seawater temperatures were inferred for middle Hodell and Woodruff 1994; McArthur et al. 2012), and so, 
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International Journal of Earth Sciences (2021) 110:995–1025 1007
under normal conditions, strontium isotopic values should be gradient (Zhang et al. 2014) and El Niño-like mean condi-
the same in coeval records across the world. In marginal or tions (Wara et al. 2005), which would suggest a reduced 
(semi)isolated basins, the 87Sr/86Sr ratio is influenced by the equatorial upwelling and cold tongue. On the Peruvian 
continental runoff (ground and surface waters), reflecting the margin, SST reconstructions from the ODP 1237 sediment 
catchment geology and local hydrological dynamics (McAr- core show 2 º to 3 °C warmer conditions from 5 to 3 Ma 
thur et al. 2012). Strontium isotope ratios constrained by (Dekens et al. 2007). The lower amplitude of this warming 
independent ages can thus be used to estimate the river water compared to the equatorial Pacific suggests that the coastal 
influence and the basin connectivity. To date, five 87Sr/86Sr upwelling in Peru was already active in the early Pliocene. 
estimates exist for the Sacaco sub-basin (Ehret et al. 2012). Climate model simulations of the warm Pliocene climate 
The strontium isotopic analysis from the Sacaco locality, suggest that the Pacific thermocline was deeper, and that 
the only locality containing independent chronostratigraphic warmer and more ventilated waters were upwelled off Peru 
controls from U/Pb datings, has yielded a mean 87Sr/86Sr (Brierley et al. 2009). These authors also suggest that lower 
value of 0.7090005 with a 2σ error lower than ± 0.00002 poleward heat transport related to lower SST gradients in 
(Ehret et al. 2012). This measured ratio does not deviate that period would have been compensated by a stronger ver-
from the Messinian average global seawater 87Sr/86Sr that tical mixing of the ocean. In addition, model experiments 
would correspond to three existing independent radiomet- showed that lower Andean elevations, similar to the Miocene 
ric dates (Fig. 5), but it is significantly higher than modern period conditions, reduce the wind stress and the coastal 
strontium values from coastal rivers entering the Pacific upwelling strength, especially in southern Peru (Sepulchre 
Ocean between 14 and 16 ºS, which have catchments domi- et al. 2009). Thus, several lines of evidence suggest that 
nated by igneous rocks that supply very low 87Sr/86Sr (rang- while a coastal upwelling was probably active in Peru during 
ing from 0.70561 to 0.70809, n = 7; Scaffidi et al. 2020). the late Miocene-early Pliocene, it was likely weaker and 
This indicates that, although the Sacaco sub-basin represents upwelled warmer and more ventilated waters compared to 
a marginal and shallow area, during the Messinian it did not present day. Such an upwelling could have maintained a high 
receive large river inputs with different Sr isotopic composi- primary productivity and warm-water fauna, but was prob-
tion, and so major salinity fluctuations due to changes in the ably not associated with a strong permanent OMZ off Peru.
freshwater supply were unlikely to occur when the sediments 
from the Sacaco locality were accumulated (~ 5.8–5.7 Ma).
Considering that the late Miocene was likely charac- The vertebrate paleontological record
terized by increased rainfall in the Central Andean region 
(e.g., Poulsen et al. 2010; Insel et al. 2012) and the Peru- Compiled data and methods
vian margin (Dekens et al. 2007), this result suggests that 
the connection between the sub-basin and the open ocean We systematized data from a wide variety of vertebrate taxa 
was either constant or large enough during the late Miocene from different evolutionary clades (exclusive of non-tetra-
(~ 5.8–5.7 Ma) to allow for a full mixing with the ocean pod Osteichthyes), involving a broad range of ecological 
waters. Therefore, the topographic highs from the Coastal niches and environmental requirements. Paleontological data 
Cordillera may have been protective barriers but did not were gathered from 20 localities across the northern and 
isolate the Sacaco sub-basin nor significantly restrict the southern EPB, spanning from the late Miocene to the mid-
seawater exchange with the Pacific Ocean. This result is dle Pleistocene (~ 10–1 Ma). Nonetheless, faunas recorded 
supported by a diverse late Miocene molluscan fauna typi- at the Chilcatay (~ 19–17  Ma) and lower Pisco forma-
cal of open ocean–facing habitats, that shows no indication tions (~ 14–10 Ma) were also reviewed to fully understand 
of endemic species associated with restricted environments regional evolutionary trends. A complete list of all verte-
(DeVries 2020), as does occur in modern restricted embay- brate fossils reported from each locality with correspond-
ments across the Pacific margin (DeVries and Wells 1990). ing references can be found in Table S2. Genus richness 
Further assessment of the basin connectivity and freshwater (incidence-based Chao2 index; Chiu et al. 2014) and per 
discharge for other time periods is still needed to understand capita rates of origination (p) and extinction (q) using per 
the sub-basin oceanographic conditions. million-year intervals (Foote 2000), were also calculated to 
evaluate faunal turnover patterns between 11 and 4.5 Ma. 
The regional and global context See Supplementary Information for complete details on data 
compilation, treatment, and diversity analyses.
SST reconstructions from the Eastern and Western equa- A reference assemblage of modern coastal-marine 
torial Pacific show 3 º to 5 °C warmer conditions across vertebrate species living at the Pisco region (13–14.6 ºS, 
the whole Pacific from 10 to 5 Ma, with a slightly larger Table S2) was compiled as a benchmark for assessing past 
anomaly in the eastern Pacific, indicating a reduced zonal changes in faunal composition with reference to present-day 
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 1008 International Journal of Earth Sciences (2021) 110:995–1025
Fig. 5  Global ocean 87Sr/86Sr ratios for the late Miocene–early (0.7090005 ± 0.00002). Brown boxes show three independent age 
Pliocene (~ 7–4.5  Ma), data from the LOWESS dataset (V.5; Fit constraints with error bars (a–c) for the same locality. Note that inde-
26/03/13; McArthur et  al. 2012). Dotted line shows the stron- pendent radiometric ages fall within error of the globally-estimated 
tium isotopic value reported for the Sacaco locality by Ehret et  al. strontium values
(2012) with its 2σ estimated error represented by the blue band 
HCS communities. This assemblage will be hereafter (~ 10–7 Ma), late Miocene-early Pliocene (~ 7–4.5 Ma), and 
referred to as Modern Sample (MS). The taxonomic resem- late Pliocene-early Pleistocene (2.7–1 Ma).
blance between fossil and extant vertebrate faunas was 
estimated by the Simpson Coefficient (SC; Simpson 1960) Vertebrate paleontology review
using presence/absence data. The coefficient quantifies the 
percentage of shared taxa (here at the genus level) between The compiled fossil record comprises a wide taxonomic 
extant and fossil communities. Minimum and maximum val- diversity, including mysticetes, odontocetes, pinnipeds, sire-
ues were estimated, considering that faunal representation nians, xenarthran sloths, crocodylians, turtles, birds, carti-
of fossil communities is potentially biased by depositional laginous fishes, and few terrestrial mammals, ranging from 
settings or taphonomic processes. The minimum similarity the early Miocene to the middle Pleistocene (~ 19–1 Ma; 
coefficient (SCmin) corresponds to the percentage estimated Figs. 6, 7). The fossil vertebrate dataset includes 102 taxa, 
using the number of shared taxa identified to genus level, of which 90 are described and named genera (Table S2). The 
whereas the maximum value (SCmax) assumes that fossil dataset also includes specimens that are not identified at the 
specimens identified above the genus level can be assigned genus level due to the limited knowledge of some groups, 
to any existing genus from the modern sample (Croft 2007). the lack of diagnostic characters, or poor preservation. The 
To estimate this coefficient, fossiliferous localities were most diversified groups are cetaceans (e.g., Piscobalaena, 
clustered in four time bins according to their relative chron- Inkakujira, Brachydelphis, Piscolithax, Ninoziphius, Acro-
ostratigraphic position (see Supplementary Information), as physeter, and Livyatan; Fig. 6) and chondrichthyans (e.g., 
follows: Miocene older than 10 Ma (> 10 Ma), late Miocene Carcharocles, Cosmopolitodus, and Carcharhinus; Fig. 7). 
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International Journal of Earth Sciences (2021) 110:995–1025 1009
Pinnipeds and marine birds are also rich groups. Terrestrial 2017). Current evidence suggests the presence of four gen-
mammals such as procyonids, rodents, and continental birds, era of monachine phocids at the Sacaco sub-basin (i.e., 
are scarce and represented by fragmentary evidence. Non- Acrophoca, Piscophoca, Hadrokirus, and Australophoca), 
tetrapod osteichthyes (bony fishes) although broadly rep- being Acrophoca longirostris (Muizon, 1981) the most 
resented (Muizon and DeVries, 1985) were excluded from common taxon (Fig. 6; Table S2). A fifth pinniped taxon, 
this review because of the lack of taxonomic and anatomical recovered from the Sacaco locality (SAO level), would have 
studies. also been present (MNHN.F.SAO130). The last record of 
phocid seal remains occurs at the early Pliocene (~ 4.8 Ma; 
Temporal distribution of taxa from ~ 10 to 4.5 Ma Muizon and DeVries, 1985). No indisputable remains of 
otariids have been recovered from the late Miocene–early 
The vertebrate assemblages along the late Miocene-early Pliocene (Fig. 6, Table S2). Recent surveys across the Cara-
Pliocene (~ 10–4.5 Ma) interval remain relatively stable and coles and Pongo formations (late Pliocene–early Pleisto-
includes forms of presumably regional distribution. How- cene) recovered several specimens referable to the living 
ever, variations in taxonomic richness and faunal turnovers genus Arctocephalus (MUSM 3608, 3628). The holotype of 
within clades can be identified (Figs. 6, 7). A detailed review Hydrarctos lomasiensis (MP UNI 04; Museo Mineralógico 
of the temporal distribution of taxa by phylogenetic groups y Paleontológico de la Universidad Nacional de Ingenie-
is available in the Supplementary Information. ría in Lima, Peru), originally attributed to the living genus 
Cetaceans. They form a phylogenetically and ecologically Arctocephalus (Muizon 1978), might have been recovered 
diverse group throughout the late Miocene-early Pliocene, from similar Plio-Pleistocene beds. Lastly, the Caracoles and 
comprising at least 36 genera (6 mysticetes and 30 odon- Pongo formations have also yielded fragmentary bones and 
tocetes; Figs. 6, 8). Beaked whales (Ziphiidae) are abundant teeth of a giant walrus (Odobenidae; Fig. 6; Table S2).
in late Miocene sediments (~ 10–7 Ma) and are mainly rep- Sirenians. This group is represented by a mandible of the 
resented by stem taxa mostly belonging to the Messapicetus dugongid Nanosiren that was recovered from the Aguada 
clade (Bianucci et al. 2016b). Sperm whales (Physeteroidea) de Lomas locality (~ 9.5 Ma; Muizon and Domning 1985; 
are mainly represented by raptorial forms (e.g., Acrophyseter Domning and Aguilera 2008). Along with a roughly coeval 
and Livyatan: Lambert et al. 2010, 2016) and pygmy sperm isolated tooth from the Bahía Inglesa Formation in north-
whales (e.g., Koristocetus, Scaphokogia; Muizon 1988; Col- ern Chile, these are the youngest records of sirenians in the 
lareta et al. 2017a; Benites-Palomino et al. 2020), and show southeastern Pacific (Bianucci et al. 2006; Domning and 
no significant changes in taxonomic composition and diver- Aguilera 2008). Sirenians are obligate aquatic herbivorous 
sity. In contrast, other odontocete clades, such as beaked and restricted to subtropical and tropical waters (Domning 
whales (Ziphiidae), iniod dolphins (Inioidea), and porpoises 2001). The body mass of Nanosiren is calculated in 150 kg 
(Phocoenidae), experienced a taxonomic turnover at the end and it probably fed upon sea grasses within very shallow 
of the Tortonian (at ~ 7 Ma; Fig. 6). Odobenocetops, a pre- waters (Domning and Aguilera 2008; Velez-Juarbe et al. 
sumably coastal and endemic form from the southeastern 2012).
Pacific (Muizon and Domning 2002), became common dur- Xenarthrans. This group is represented by Thalassocnus, 
ing the ~ 7–4.5 Ma interval, when the first occurrences of a lineage of marine sloths composed by five species docu-
delphinid dolphins are also recorded (Stenella, cf. Delphinus mented from the late Miocene to the early Pliocene (~ 10 to 
and Cephalorhynchus and/or Lagenorhynchus; Muizon and 4.5 Ma), being particularly abundant during the late Mio-
DeVries, 1985; Fig. 8). Baleen whale remains are abundant cene–early Pliocene (Fig. 6; see Table S2).
during the late Miocene-early Pliocene, however, their taxo- Crocodylians and Testudines. The fossil record of croco-
nomic diversity is poorly known (Brand et al. 2011). Five dylians includes two extinct long-snouted crocodylian forms 
genera have been documented between 10 and 7 Ma, but from different clades: Piscogavialis (gryposuchine gavia-
only two genera are recorded after the Mio-Pliocene tran- loid; Kraus 1998; Salas-Gismondi et al. 2019) and a new 
sition, the putative cetotheriid Piscocetus, and the extant taxon identified as a Tomistominae (MUSM 161, MUSM 
rorqual Balaenoptera (Fig. 6; Bouetel and Muizon, 2006; 162). These taxa appear to have distinctive chronostrati-
Pilleri and Siber 1989). Regarding Piscocetus, its taxon- graphic distributions. Both are recorded from middle to late 
omy and systematics are uncertain since it has been neither Miocene beds (~ 7 Ma), but only Piscogavialis continues up 
revised nor included in recent phylogenetic analyses. into the early Pliocene (~ 4.5 Ma; Fig. 7). As for testudines, 
Pinnipeds. Their fossil record includes various well-pre- remains of marine turtles have only been recovered from the 
served earless seals specimens (Phocidae) from the north- Ica Valley. The record consists of the cheloniid Pacifichelys 
ern EPB (Bianucci et al. 2016a, b; Lambert et al. 2017); urbinai (Parham and Pyenson 2010; Bianucci et al. 2016b) 
however, none of them has been properly described and so and one dermochelyid species (MUSM 407) more closely 
their taxonomic identity remains uncertain (Lambert et al. 
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International Journal of Earth Sciences (2021) 110:995–1025 1011
◂Fig. 6  Chronostratigraphic distribution of extinct (in black) and Non-aquatic mammals. These remains are rare and have 
extant (in blue) genera of marine mammals recorded over the been recovered from late Miocene deposits (~ 10–7 Ma; 
last ~ 14 Ma within the EPB along with those inhabiting the coastal-
marine ecosystems of the Humboldt Current System at the basin´s Fig. 7; see Table S2). They include elements of the car-
latitude. Sea level (SL) curve and global temperature after Miller nivoran procyonid Cyonasua (MNHN SAS 1625, MNHN 
et al. (2011) and Zachos et al. (2001), respectively. CAR-PONCara- PPI 262; Muizon and DeVries, 1985; Tarquini et al. 2020), 
coles-Pongo formations; Piace: Piacenzian, ID Initial Diversification; the hystricognath rodent Tetrastylus (MNHN PPI 263, 264), 
HD High Diversity; ID SH Initial Diversification Southern Hemi-
sphere; DD Diversification Decline; CAS Central American Seaway; a medium-sized macraucheniid litoptern (MUSM 226), and 
TSW Tethys Seaway; PSW Panama Seaway; NHG Northern Hemi- a small marsupial (MUSM 225).
sphere Glaciations. † Last known occurrence
Diversity trends from ~ 10 to 4.5 Ma
related to Dermochelys than to Psephophorus (J. Parham The taxonomic richness of the vertebrate assemblage 
pers. comm). reached its highest values during the Tortonian (10–8 Ma; 
Aves. Coastal seabirds, such as boobies (Sulidae), cormo- Fig. 9), ranging from 121.3 to 126.8 ± 40 taxa. This high 
rants (Phalacrocoracidae), and penguins (Spheniscidae), are richness appears to be mostly driven by chondrichthyans, 
relatively well documented in the Pisco Formation, includ- after the discovery of a shark tooth-bearing horizon from 
ing several skeletons and hundreds of isolated bones (Fig. 7; Cerro Colorado representing a nursery area and which 
see Table S2). In contrast, remains of pelicans are restricted included at least 15 genera (Landini et al. 2017a, b). Ceta-
to a single bone occurrence in the Sacaco sub-basin (Mon- ceans, although abundant and diverse throughout the record 
temar locality; Altamirano-Sierra 2013). The Pisco record (Fig. 6), do not contribute as much to the observed Torto-
also includes specimens of extinct taxa of cathartiforms nian richness (Fig. 9). Lower richness values occur from 8 
(New World vultures; Stucchi and Emslie 2005; Stucchi et al. to 5 Ma, when genus richness ranges from 56.6 to 64.5 ± 6 
2015a), procellariforms (e.g., petrels, albatrosses), charadrii- taxa. At this time, the entire fossil assemblage shows steady 
forms, and other seabirds with no extant close relatives, such values, but a major drop in cetacean richness is observed in 
as pelagornithids and the sulid Ramphastosula (e.g., Stucchi the 6–5 Ma-time bin (11 taxa; Table S2). The Chao2 index 
and Urbina, 2004; Chavez et al. 2007; Stucchi et al. 2015b). was not estimated for the 5–4 Ma-time bin given the small 
Chondrichthyes. The record is mostly dominated by Car- size of the sample (two localities [Yauca and Acarí] account-
charhiniformes and Lamniformes (Fig. 7; see Table S2). ing for 9 genera).
Teeth of the requiem sharks belonging to Carcharhinus and The dynamics of diversity was further assessed through 
the lamnid Cosmopolitodus (= Carcharodon) are relatively estimates of origination and extinction per capita rates per 
common, in contrast to those of the lemon shark Negaprion million years (Fig. 9). Origination rates are considerably 
and the sawshark Pristiophorus, which are represented by a higher from 11 to 8 Ma (values > 0.35), coinciding with 
few isolated pieces. The non-serrated teeth of Cosmopolito- the highest richness values. A maximum peak on per cap-
dus hastalis are recorded throughout the late Miocene ita origination rates occurs at the 9–8 Ma-time bin (0.48). 
(~ 10–7 Ma) time bin, while teeth with incipient serrations This matches a previous origination peak reported at 9 Ma 
appear in the record for the first time by ~ 7  Ma (Car- for marine faunas from the South American Pacific coast 
charodon hubbelli type of teeth). Serrated teeth typically (Villafaña and Rivadeneira 2014). From 8 to 4 Ma, origina-
of Carcharodon are found from the late Miocene onwards tion rates show a marked decrease, while per capita rates of 
(~ 7–1 Ma). The otodontid lamniforms, a popular clade extinction slightly increase and surpass origination rates. A 
known as ‘megatooth’ sharks, are all extinct and comprise maximum value of extinction rates (0.47) is observed at the 
large to giant sharks recovered from the Chilcatay and Pisco 7–6 Ma-time bin, although no change in richness is detected 
formations (Table S2). The giant Carcharocles megalodon compared to previous and next time bins. Similar patterns 
was the last survivor of this group and has been recorded (i.e., increase of extinctions and decrease of origination 
up to the top of the Pisco Formation (Bianucci et al. 2016a, rates) were also described for marine fossil assemblages by 
b; Muizon and DeVries, 1985; Landini et al. 2017a). To Villafaña and Rivadeneira (2014).
date, Carcharocles is absent from Plio-Pleistocene deposits 
(Fig. 7). The extant lamnids Carcharodon, Carcharias, and 
Pseudocarcharias are found as fossils in the Pisco Forma-
tion but no longer inhabit the Peruvian coasts. The broad-
nose sevengill shark Notorhynchus is the only shark from the 
Caracoles Formation not found in older deposits. Myliobati-
formes and Chimaeriformes are restricted to Myliobatis and 
Callorhinchus, respectively.
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International Journal of Earth Sciences (2021) 110:995–1025 1013
◂Fig. 7  Chronostratigraphic distribution of extinct (black bars) and Kogia (Fig. 8; Benites-Palomino et al. 2021). Some marine 
extant (blue bars) genera of reptilians, seabirds, chondrichthyans and birds (Spheniscus, Phalacrocorax) and the rorqual Balae-
non-aquatic mammals recorded over the last ~ 14 Ma within the EPB 
along with those inhabiting the coastal-marine ecosystems of the noptera occur since ~ 10 Ma (Figs. 6, 7). Among chondrich-
Humboldt Current System at the basin´s latitude. Note that genera thyan fishes, the Mio-Pliocene (~ 7–4.5 Ma) fauna includes 
in blue designate extant genera living outside the HCS domain. Sea the earliest record of the great white shark Carcharodon, the 
level (SL) curve and global temperature after Miller et al. (2011) and school shark Galeorhinus, and the chimaera Callorhynchus. 
Zachos et  al. (2001), respectively. CAR-PON: Caracoles-Pongo for-
mations; Piace: Piacenzian. NA: North American; SA: South Ameri- However, disregarding the potential taphonomic bias driven 
can; CAS: Central American Seaway; TSW: Tethys Seaway; PSW: by the overrepresentation of chondrichthyans, analysis sug-
Panama Seaway; NHG: Northern Hemisphere Glaciations. † Last gests that less than 40% of the genera diversity of modern 
known occurrence coastal-marine environments from the HCS was present 
before ~ 4.5 Ma, when the latest known Pisco paleoenviron-
Evolution of the coastal‑marine communities ments are documented (Figs. 6, 7; Table 2). Late coloniz-
from the central Peruvian margin ers of the HCS, are either reported from the Caracoles and 
Pongo units (eared seals: Otariidae), or have no fossil record 
Fossil versus Modern assemblages to date in the EPB (e.g., the porpoise Phocoena, the hump-
back whale Megaptera, and the marine otter Lontra).
A comparison of the reviewed fossil vertebrate faunas to 
the MS provides an initial understanding on when and Faunal Turnover: Progressive changes over the last 
how modern taxa became established along the Peruvian 10 My
Pacific coast. Remains of shark and rays are abundant in the 
fossil record relative to other vertebrates (Fig. 6), even in Our analyses of faunal similarities along with estimates of 
outcropping successions with less prospecting effort than per capita origination and extinction rates identified selec-
those achieved at the traditional Pisco Formation localities tive faunal turnovers between time bins over the last 10 
(such as Sacaco, Sud-Sacaco, Montemar, and Aguada de My (Table 2; Fig. 9). In general, differences are driven by 
Lomas; Muizon and DeVries 1985). This taphonomic fea- changes within marine mammal communities, primarily 
ture may bias community assessments (e.g., Boessenecker within odontocetes and pinnipeds (Fig. 6). As high trophic 
et al. 2014). Sharks and rays are also known for their reduced level vertebrates (Pauly et al. 1998), changes in their assem-
evolutionary rates compared with other marine vertebrates blages through time might reveal shifts in productivity, type 
(Hara et al. 2018), which could mask changes in ecosystems of resources, and functioning of the ecosystem (Tucker and 
through time when their record represents an important por- Roger 2014; Pyenson and Vermeij, 2016). Here, we ana-
tion of the whole community. We thus performed two SC lyze the main faunal changes between time bins and discuss 
estimates, with and without sharks and rays (Table 2). putative patterns of turnover related to tectonics and global 
We compared the fossil fauna present in each of the four climate trends.
time bins previously defined (i.e., Miocene older than 10 Ma 
[> 10 Ma], late Miocene [~ 10–7 Ma], late Miocene–early  ~ 10–7 Ma: morphological diversification of crown 
Pliocene [~ 7–4.5 Ma], and late Pliocene–early Pleistocene delphinidans and dawn of endemic taxa
[2.7–1 Ma]; see Supplementary Information) with the MS. 
Resemblance analysis including sharks and rays provided Basal odontocetes with double-rooted cheek teeth (e.g., 
the following values, from older to younger time slices: 25%, Inticetus), platanistoids (e.g., Huaridelphis, Macrosqualo-
26.3/29.8%, 37.2/44.2%, 70.6/82.4%. When Chondrichthyes delphis), and archaic delphinidans (e.g., Incacetus, Atoce-
were excluded, the following values were obtained: 4.8%, tus, ‘Kentriodontidae’) experienced a demise at ~ 10 Ma or 
13.2/18.4% 26.7/33.3%, 70.0/90.0% (Table 2). The oldest much earlier within the EPB (Colbert 1944; Muizon 1988; 
time bin only has one SC value as the minimum and maxi- Lambert et al. 2017; Bianucci et al. 2018, 2020). Some pla-
mum number of shared genera is the same for each analysis. tanistoids and ‘kentriodontids’, however, did survive longer 
Both analyses show an increasing trend but the values with- in isolated marine and freshwater settings (Ichishima et al. 
out Chondrichthyes are consistently lower. With or without 1994; Marx et al. 2017), as the South Asian river dolphin 
Chondrichthyes, analyses indicate a moderate rise in the Platanista, the only extant representative of the platanistoids 
resemblance with the MS from the late Miocene (~ 10–7 Ma) (Barnes et al. 2006). The earliest record of sperm whales 
to the late Miocene-early Pliocene time slice (~ 7–4.5 Ma) (Physteroidea) in the EPB includes the basal taxon Raphi-
(Table 2). This is led by the first putative record of conspicu- cetus valenciae from Chilcatay sediments (Lambert et al. 
ous representatives of the modern HCS community among 2020b) and two undescribed forms from the lower Pisco 
odontocetes, such as the delphinid dolphins Stenella and cf. Formation (Di Celma et  al. 2017, 2018; Lambert et  al. 
Delphinus, Lagenorhynchus, and the pygmy sperm whale 2020a; Table S2).
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1 014 International Journal of Earth Sciences (2021) 110:995–1025
Fig. 8  Selected toothed cetaceans from the Sacaco locality. a–d cf. 30): periotic in dorsal (e) and ventral (f) views. G-H. Delphinapteri-
Delphinus sp. (MNHN.F.SAO 211): left arm in ventral view (a), right nae indet. (MNHN.F.SAO 206): periotic in dorsal (g) and ventral (h) 
tympanic bulla in ventral view (b), periotic in dorsal (c) and ventral views. i Kogia (MUSM 3888): partial cranium in dorsal view
(d) views. e, f Cephalorhynchus or Lagenorhynchus (MNHN.F.SAO 
Although similarity values relative to the MS show Benites-Palomino et al. 2020). This morphological disparity 
a low increase between the oldest time bins (from 4.8 to might be associated with a global peak in cetacean diversity 
13.2/18.4%), profound changes in the marine communities and speciation rate reached during Tortonian times (Fig. 9), 
did occur at ~ 10 Ma (Figs. 6, 9). For instance, the late Mio- which could have been driven by a burst in diatom diversity 
cene (~ 10–7 Ma) time bin is also characterized by the first associated with global marine productivity (Steeman et al. 
record and large diversification of beaked whales (Ziphi- 2009; Marx and Uhen 2010). Although true dolphins (Del-
idae) and dwarf sperm whales (Kogiidae), as well as crown phinidae) might have already diversified by the late Miocene 
delphinidan subclades, such as porpoises (Phocoenidae) (Steeman et al. 2009; Bianucci et al. 2013; Murakami et al. 
and toninhes (Pontoporiidae). Prior to ~ 10 Ma, several 2014), no delphinid remains have been recovered from late 
groups of odontocetes possessed a long-snouted morpho- Miocene (~ 10–7 Ma) sediments in the EPB (Fig. 6).
type, including longirostrine and hyperlongirostrine forms in The late Miocene (~ 10–7 Ma) time bin also marks the 
marine environments (Bianucci et al. 2020; Norris and Mohl dawn of endemic forms, such as the aquatic sloth Thalassoc-
1983). After the evolution of crown delphinidan subclades, nus and the walrus-like delphinidan Odobenocetops (Fig. 6). 
odontocete snout shape diversified and reached putative spe- Both taxa, along with other vertebrates (e.g., the pontoporiid 
cializations in feeding strategies (Fig. 9; Werth 2006; Boess- Brachydelphis, the long-snouted seal Acrophoca, the pen-
enecker et al. 2017). The late Miocene (~ 10–7 Ma) assem- guin Spheniscus, and crocodylians), have also been recov-
blage of the Pisco Formation exemplifies the extraordinary ered from the northern coast of Chile (Walsh and Naish 
disparity of odontocete snout shapes in coastal environments 2002; Canto et al. 2008; Gutstein et al. 2009; Pyenson et al. 
(Fig. 6), including a wide range of long-, blunt-, bulky-, and 2014; De los Arcos et al. 2017), suggesting that the south-
short-snouted forms (Muizon 1988; Collareta et al. 2017a; eastern Pacific coastal areas (~ 14–25 ºS) have shared similar 
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International Journal of Earth Sciences (2021) 110:995–1025 1015
Fig. 9  Upper box: Chao2 richness index calculated per million-year ita origination (filled dots) versus extinction (crosses) rates estimated 
for all genera present in the fossil assemblage (filled triangles), as per million-year, excluding singletons. Note the strong diversity drop 
well as for the two most abundant phylogenetic groups: cetaceans in cetaceans after the 6 Ma, as well as the high extinction rate peak 
(filled squares) and chondrichthyans (filled dots). Lower box: Per cap- observed between 7 and 6 Ma
and unique environmental conditions and an original evolu- This drop, captured by the Chao2 index (Fig. 9), also occurs 
tionary trajectory at least since the late Miocene. The sole in the Ziphiidae, Phocoenidae, and Pontoporiidae clades 
record of sirenians in the EPB occurred at the beginning of (Fig. 6). It coincides with the global Messinian diversity 
this time bin. Shortly thereafter, Thalassocnus was the sole decline (Marx et  al. 2017), which has been linked to a 
herbivorous mammal within the Pisco ecosystem, possibly decrease in ocean primary productivity after a strong reduc-
indicating a reduction of seagrass beds. tion in diatom diversity (Marx and Uhen 2010). Sampling 
bias has been invoked as a possible cause for this diversity 
 ~ 7–4.5 Ma: Diversity decline and the first record of extant reduction (Uhen and Pyenson 2007; Marx et al. 2017). How-
odontocete genera ever, our extended synthesis shows a robust decline in some 
groups of odontocetes in the EPB record (Figs. 9, 10). 
Crown odontocete subclades from the EPB lost substantial As mentioned before, the marked increase in similarity 
genus richness (from 10 to 3 genera) at ~ 7–6 Ma (Fig. 6). values in the late Miocene–early Pliocene (~ 7–4.5 Ma) time 
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Table 2  Faunal resemblance index (Simpson Coefficient) among fossil faunas and modern coastal-oceanic taxa dwelling in waters at 13–14ºS 
latitude
Simpson coefficient (SC) per time bin  > 10 Ma 10–7 Ma 7–4.5 Ma 2.7–1 Ma Modern
Taxa count 36 57 43 17 59
Taxa count (without Chondrichthyes) 21 38 30 10 41
Minimum/maximum number of shared genera (with chondrichthyes) (9)/(9) (15)/(17) (16)/(19) (12)/(14) –
Minimun (SCmin) and maximum (SCmax) value of faunal similarity (with chondry- 25.0 26.3–29.8 37.2–44.2 70.6–82.4 –
chtyes)
Minimum/maximum number of shared genera (without chondrichthyes) (1)/(1) (5)/(7) (8)/(10) (7)/(9) –
Minimun (SCmin) and maximum (SCmax) value of faunal similarity (without chondry- 4.8 15.8–18.4 26.7–33.3 70.0–90.0 –
chtyes)
Fossil localities have been clustered based on their chronostratigraphic position as: Miocene older than 10  Ma (> 10  Ma), late Miocene 
(~ 10–7 Ma), late Miocene to early Pliocene (~ 7–4.5 Ma), and Plio-Pleistocene (2.7–1 Ma). Complete list of fossil genera is available in the 
Table S2
bin is driven by the first occurrence of extant genera of dwarf of two otariids (eared seals) and a walrus (Fig. 6). Both 
sperm whales and true dolphins (Delphinidae) (Fig. 6). In otariids and the walrus might have dispersed from the 
the EPB, the oldest true dolphin remains include four dis- northern hemisphere during the middle Pliocene, but the 
tinct taxa recorded at the Sacaco locality (~ 5.8–5.7 Ma; precise time and mode are currently uncertain. Otariids 
Fig. 6). The observed decline in some coastal odontocetes are typically confined to cool waters and coastal upwelling 
could also be associated with the diversification of true dol- (Deméré et  al. 2003), suggesting a cooling of coastal 
phins, which has been documented to occur at 13 and 4 Ma waters were cooler by 2.7 Ma.
with a peak at 7.5 Ma (e.g., Steeman et al. 2009; Bianucci 
2013; Rabosky 2014). Taxa with putative regional and more Paleoecology of the coastal‑marine communities 
limited distribution, such as phocid seals, Thalassocnus, and during the late Miocene–early Pliocene
Odobenocetops, arose and became abundant at this time 
(Fig. 6), suggesting local stability of the coastal-marine Insights into the structure of the Pisco coastal-marine com-
environments. munities (hereafter referred to as the Pisco ecosystem) are 
As for the endemic forms, such as the aquatic sloth Thal- provided by the fossil record of predators, food resources, 
assocnus, the walrus-like dolphin Odobenocetops, and the and their agonistic interactions. This evidence allows for 
gavialoid Piscogavialis, the record shows that they persisted reconstructing putative trophic levels and comparison with 
until the last preserved Pisco beds (Figs. 6, 7). These animals modern conditions.
are regarded as highly dependent on coastal settings; there- Raptorial sperm whales (e.g., Acrophyseter, Livyatan) 
fore, any disruption of foreshore habitats by Andean tecton- were probably the top mammalian predators in the Pisco 
ics or reduction of neritic zones after sea-level oscillations ecosystem throughout the middle Miocene–early Pliocene, 
(see Pimiento et al. 2017) might have occurred later, during a trophic position now occupied by the killer whale, Orcinus 
the 4.5–2.7 Ma sedimentary hiatus (Fig. 10). orca (Lambert et al. 2014, 2016). These animals are con-
sidered as macroraptorial feeders (i.e., they consume large 
2.7–1 Ma: the Caracoles‑Pongo fossil record preys). The largest raptorial sperm whale, Livyatan, would 
have reached up to 16 m and preyed upon medium-sized 
After a gap of 1.8 My, accumulation and preservation of baleen whales (Lambert et al. 2010). Anatomical features 
sediments was reestablished by the late Pliocene (2.7 Ma) supporting these interpretations are based on their large to 
with no traces of the endemic forms from the upper Pisco giant size, massive teeth, presence of buccal maxillary exos-
sediments. The existing paleontological data point to a toses, robust jaws, and powerful temporal muscles (Lambert 
loss of some ecological roles (e.g., marine herbivory prac- et al. 2010, 2014). Yet, bite-marked bones attributed to their 
ticed by the aquatic sloth Thalassocnus, macroraptorial active hunting or scavenging behavior have not been found.
feeders) and suggest a change in coastal environmental Lamniform sharks are expected to occupy a similar 
conditions and a shift into a functionally structured com- trophic level as raptorial sperm whales. In this case, several 
munity closer to that of the modern HCS (Fig. 10). Top bones of baleen whales and phocid seals exhibit shark bite 
predators of the Caracoles and Pongo formations include marks attributed to the giant Carcharocles megalodon (Col-
delphinid dolphins and a pinniped assemblage consisting lareta et al. 2017a), which is estimated to reach up to 17 m 
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International Journal of Earth Sciences (2021) 110:995–1025 1017
Fig. 10  Summary of main faunal changes experienced in the coastal- in this work. Grey bars indicate taxonomic richness (at genus level) 
marine vertebrate communities from the central Peruvian Margin of fossil groups, and blue bars taxonomic richness (at genus level) of 
during the last 10 Ma. Red stars indicate new U/Pb ages presented extant groups
of total body length (Pimiento and Balk, 2015). The white (longirostry) and an elongated neck and body (Muizon 
shark Carcharodon and its putative ancestor, Cosmopolito- 1981). Longirostry and precise tooth interlocking suggests a 
dus, are probably ecological analogs of Carcharocles, but pierce-based feeding strategy suitable for foraging on fishes, 
of much smaller size at adulthood (5–7 m; Shimada 2002, cuttlefishes, and octopuses (Muizon 1981; Berta et al. 2018). 
2019). Similar shark tooth marks are preserved in limb Hadrokirus bears the most robust dentition among phocid 
bones of the aquatic sloth Thalassocnus, indicating that seals. Since this feature is coupled with a powerful neck 
large sharks also fed upon this marine sloth in coastal areas. and masticatory apparatus, durophagy (i.e., a diet based on 
However, establishing an indisputable perpetrator is espe- hard food, such as crabs, lobsters, sea urchins) or carnivory 
cially difficult, since serrated teeth (e.g., Carcharocles, Car- of higher level (penguins) is expected (Amson and Mui-
charodon) can inflict both smooth and serrated marks (see zon 2013). As for Piscophoca, similarities with the monk 
Cortés et al. 2019). As commonly reported for the extant seal Monachus suggest a comparable diet, including fishes, 
white shark, the Mio-Pliocene Carcharodon also scavenged squids, and hard-shelled invertebrates (Gilmartin and For-
on whale carcasses as suggested by a tooth embedded within cada 2009). Australophoca, with an estimated body length 
the jawbone of a baleen whale found in the Sud-Sacaco of one meter, is smaller than any living pinniped (Valen-
(west) locality (Ehret et al. 2009). Crocodylians from the zuela-Toro et al. 2015). Quantitative analyses on the feeding 
Pisco ecosystem were not top predators since both taxa bear anatomy of this phocid seal community are crucial to test the 
long and slender snout, linked to the capture of rapid and aforementioned assessments.
small prey (e.g., fishes; Salas-Gismondi et al. 2019). Marine herbivores are absent in the modern HCS, but 
Up to four phocid seal species of distinct body size Thalassocnus was most likely a common aquatic herbivorous 
and snout shape coexisted (at SAS and SAO; Muizon and mammal during the late Miocene–early Pliocene (Muizon 
DeVries 1985). Highly diverse communities are strongly and McDonald 1995; McDonald and Muizon 2002; Mui-
linked to coastal upwellings near continental margins zon et al. 2004a, b). Thalassocnus was a bottom walker of 
(Deméré et al. 2003), while different snout and tooth shapes protected, shallow waters which mainly fed upon rhizomes 
might represent a variety of diet preferences. Acrophoca of seagrasses (Muizon et al. 2004b; Amson et al. 2015). 
is a large, idiosyncratic seal with a long and slender snout Thalassocnus feeding anatomy suggests that meadows of 
1 3
 1018 International Journal of Earth Sciences (2021) 110:995–1025
seagrasses were relatively common in the past. The record anchovy Engraulis rigens (Tarazona et al. 2003). However, 
from the Pisco Formation is silent in this matter; however, alternations in the abundance between Engraulis and Sardi-
seagrass leaves (Heterozostera) have been reported from Pli- nops occur naturally by environmental changes, in which the 
ocene mudstones located nearby the Nazca area (Hacienda biomass of the sardines (and other fishes) rises and prevails 
Tunga; Phillips et al. 1996). Nowadays, a single species of during warm and oxygenated El Niño conditions (3–8 ºC 
seagrasses, Heterozostera chilensis, inhabits the southeast- warm anomalies; DeVries and Pearcy, 1982; Deméré et al. 
ern Pacific, and it is disjunctively present in a couple of bays 2003; Gutiérrez et al. 2012). The presence of Sardinops in 
in central Chile (Kuo 2005; Short et al. 2007). Such con- the fossil record during the early Pliocene is consistent with 
fined distribution is attributed to the high-energy exposure the evidence of El Niño-like conditions in the Pacific dur-
of those coasts, which prevents a uniform expansion of the ing that time (Wara et al. 2005; Dekens et al. 2007; Brierley 
seagrass (Kuo 2005). Since Thalassocnus fossils have been et al. 2009).
recovered from the youngest deposits of the Pisco Forma-
tion, protected, shallow water environments with extensive 
meadows might have persisted up to 4.5 Ma at the Sacaco Conclusions
sub-basin.
The fossil record of the main guano-producer seabirds Since the pioneering work of Muizon and DeVries (1985), 
(Phalacrocorax, Sula, and Spheniscus) is indicative of large the EPB has yielded numerous paleontological discoveries 
populations since the late Miocene (Urbina and Stucchi that contribute to the understanding of the evolution of dif-
2005; Stucchi 2007; Stucchi et al. 2016). This assemblage ferent clades. In this work, we revisited the Mio-Pliocene 
is present in the highly productive upwelling systems of chronostratigraphy of the Sacaco sub-basin, reviewed the 
the southern hemisphere (Benguela, Humboldt) and sug- vertebrate paleontological record, and addressed biodiversity 
gests similarities with the modern HCS conditions in terms and ecological changes over the last 10 My in an integrated 
of food resources (Chavez-Hoffmeister et al. 2014). In the geological and environmental context. Main findings are 
HCS, these genera mainly feed upon the pelagic Peruvian summarized as follows:
anchovy Engaulis rigens (Thiel et al. 2007). Extinct species 
of Spheniscus (S. muizoni, S. urbinai, S, megaramphus) and 1. Radiometric results indicate that the last known pre-
Sula (S. magna, S. figueroae, S. brandi, S. aff. variegata; S. served Pisco sediments from the Sacaco sub-basin are 
sulita) might have had a diet similar to their modern counter- dated as 4.5 (Quebrada Caracoles) (Table 1), whilst the 
parts, but higher species richness and body size disparity in succession from the Sacaco locality was accumulated 
fossil forms might reflect a wider range of prey items (e.g., at 5.8–5.7 Ma, as indicated by Ehret et al. (2012). The 
Stucchi 2002; Acosta-Hospitaleche et al. 2011; Stucchi et al. Pisco Formation at the Sacaco sub-basin thus spans 
2016; Chavez-Hoffmeister, 2020). from ~ 10 to 4.5 Ma (Fig. 2).
Direct evidence documenting the trophic relationships in 2. The base of the late Pliocene Caracoles Formation was 
the Pisco ecosystem is provided by some rare cases of ago- dated at 2.7 My, this unit was accumulated under more 
nistic interactions recorded as trace fossils. A beaked whale proximal settings (shoreface) than the underlying Pisco 
specimen of Messapicetus from Cerro Colorado (MUSM Formation. The contact between these formations is 
2252) had numerous skeletons and scales of the clupeid fish characterized by an erosive surface with subtle changes 
Sardinops (sardine) preserved within the chest region and in dip angles, evidencing the presence of an angular 
around the head (Lambert et al. 2015). Dermal and bony unconformity (Fig. 3b). The minimum time gap repre-
remains of Sardinops interpreted as forestomach content sented by this hiatus is of 1.8 My. We associate this 
were also found between the posterior ribs of a small Pisco- unconformity with a Pliocene phase of surficial uplift, 
balaena-like baleen whale (Collareta et al. 2015). Addition- which would have led to the cessation of sedimentation, 
ally, a partial skeleton of a juvenile individual of the lam- uplifting, and erosion from 4.5 to 2.7 Ma.
niform shark Cosmopolitodus preserved opercles and large 3. Different communities have existed over the last 10 My 
scales typical of Sardinops as well, probably belonging to on the Peruvian margin. Faunal changes occur across 
the extant Pacific pilchard S. sagax (Collareta et al. 2017b). various phylogenetic groups but are especially observed 
These findings suggest that the pilchard was an abundant within marine mammals (odontocete cetaceans, and 
resource, even for predators with dissimilar feeding anatomy pinnipeds). The late Miocene assemblages (> 10 Ma 
and strategies. Sardine remains are also identified across and ~ 10–7 Ma) were dominated by several cetacean 
the Sacaco sub-basin up to the early Pliocene (Muizon and clades (i.e., ziphiids, phocoenids, pontoporiids) that 
DeVries, 1985), indicating that this fish was likely an impor- show a marked decline at ~ 7 Ma. An early faunal change 
tant link in the food chain. In the highly productive modern among odontocetes is observed between 7 and 6 Ma. 
HCS, the dominant schooling fish is the pelagic Peruvian Besides seabirds, the first record attributable to con-
1 3
International Journal of Earth Sciences (2021) 110:995–1025 1019
spicuous representatives of the modern HCS community MAGNET program (Contract Nº 07-2017-FONDECYT). Funding was 
(i.e., the delphinid dolphins Stenella, Delphinus, Lagen- also available through the Consejo Nacional de Ciencia, Tecnología e 
orhynchus, and the pygmy sperm whale Kogia) appear Innovación Tecnológica (CONCYTEC) –FONDECYT research grants 
105-2018 and 104-2018 awarded to DO and RS-G, respectively.
in the record by ~ 7 Ma. Phocid seals and endemic taxa 
(e.g., the sloth Thalassocnus, the walrus-like dolphin Data availability Not applicable.
Odobenocetops, and the crocodylian Piscogavialis) pre-
vail and survive until the last known Pisco deposits. The Code availability Not applicable.
time of the extinction of these inhabitants from the Pisco 
ecosystem occurred between 4.5 and 2.7 Ma (Fig. 10). Declarations 
A new community, much closer to the modern one is 
observed in the Plio-Pleistocene (2.7–1 Ma), although Conflict of interest Not applicable.
some key taxa (e.g., Megaptera, Otaria) of the modern Open Access This article is licensed under a Creative Commons Attri-
HCS ecosystems are still absent (Figs. 6, 7). The sub- bution 4.0 International License, which permits use, sharing, adapta-
stantial ecosystem reorganization that occurred during tion, distribution and reproduction in any medium or format, as long 
the 4.5–2.7 Ma sedimentary hiatus was likely linked to a as you give appropriate credit to the original author(s) and the source, 
coastal geomorphological transformation due to tectonic provide a link to the Creative Commons licence, and indicate if changes 
were made. The images or other third party material in this article are 
uplift. included in the article’s Creative Commons licence, unless indicated 
4. The abundant diatom-rich beds, schooling fishes (Sar- otherwise in a credit line to the material. If material is not included in 
dinops) as well as the trophic chains supporting giant the article’s Creative Commons licence and your intended use is not 
cetaceans are indicators of continuous high upwelling permitted by statutory regulation or exceeds the permitted use, you will 
need to obtain permission directly from the copyright holder. To view a 
related productivity during Mio-Pliocene times. Except copy of this licence, visit http://c reati vecom mons.o rg/l icens es/b y/4.0 /.
for transient oxygen-depleted events, the sedimentologi-
cal record from the Pisco Formation at the Sacaco sub-
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