Coprolite diversity from the archeological site Gruta Do Gentio Ll,Unaí,Minas Gerais,Brazil

Abstract

The first paleoparasitological analyses in Brazil are related to the Gruta do Gentio ll (GGll) an archeological site related to the beginning of the Una ceramist tradition (13,000–410 cal B.P.), with two subsistence horizons, an ancient one related do hunter-gatherers, and a more recent one related to a horticulturist population. Crucial cultural traces of Una tradition such as pottery, fabric, adornments made from animal teeth and shells, and food remnants were also identified during the GGII excavations. Coprolites, fossilized or mineralized feces are important elements in the studies on taphonomy and sedimentology, and yield valuable information on parasitological, environmental, producer origin, and diet. In the present study, GGll coprolites were submitted to morphological and morphometrical procedures to identify the probable origin of samples within the geographical location of study. The results of the identification of coprolites showed four different morphotypes including complex, flat, spherical, and cylindrical, in 10 distinct colors, distributed heterogeneously in 16 sectors and 11 stratigraphic layers, indicating a great variety of not only human but animal coprolites. With the collected data, along with previous archeological evaluations, we can propose a primary GGII paleoecological scenario, with the presence of animals and humans that used de cave in the Pleistocene and Holocene times of Southeast Brazil.

Keywords

Holocene Horticulturists Hunter-gatherer Pleistocene pre-Columbian Brazil Una tradition

Introduction

Buckland (1829) was the pioneer to use the term “coprolite” when he described fossilized feces in geological formations at the Lyme Regis, England. According to Buckland, coprolites are specimens with the original form of the producer, preserved without any type of interference until the state of lias shale (Buckland, 1829). Harshberger (1896) suggested bones and seeds undigested present in pre-historic human coprolite could reveal clues about their diet. In the last decade, coprolite studies have received attention due to the unique microhabitat, which preserves paleoecological interactions of intestinal parasitism and predator-prey interaction that otherwise would be unattainable. Nowadays, there is a shift in the focus of microbiome research, from comprehending the factors influencing community membership, interactions among multiple species, variations in function, and the stability of the entire ecosystem. These updated systems of microbiome research are also well included in coprolite studies (Dentzien-Dias et al., 2018; Jacobson et al., 2020; Yang et al., 2022).

Coprolites have been recognized as deposits of paleontological data (Qvarnström et al., 2016; Seilacher et al., 1985), including parasites, because of the ecological evidence related to the diet of extinct organisms present in these fossilized feces. To identify coprolite origin and organic constitution, several techniques have been applied, including morphological and morphometric essays, mineralogical composition, physicochemical analysis (de Oliveira and Santucci, 2017; Rodrigues et al., 2018); micromorphology of pollen grains and microremains to investigate diet (Baeten et al., 2018; Harshberger, 1896; Tavarone et al., 2020). Bile acids/sterol analysis also helps to identify producers (Porru et al., 2021; Rhode, 2003), and ancient DNA (aDNA) studies the origin of producers, the fauna producers preyed on, phylogeny and evolution of producers (Karpinski et al., 2017; Palacio et al., 2017; Yang et al., 2022). In addition, paleoparasitological methodologies to determine parasite constitution have contributed to the knowledge of the origin of human and animal coprolites (Araújo and Ferreira, 2000; Ferreira and Araújo, 2011; Salvadores-Cerda and Ramírez-Mercado, 2020). Paleoparasitology studies parasites in archeological or paleontological remains, using techniques developed to process samples such as sediments and coprolites (Araújo and Ferreira, 2000). Classically, for the analysis of coprolites, which are the main type of sample of interest in paleoparasitology, it is used the rehydration technique described by Callen and Cameron (1960), to return the desiccated sample to approximate fecal consistency. After rehydration, the spontaneous sedimentation of Lutz (1919) is used to concentrate and search for parasite lifeforms and microremains, enabling the analysis through microscopy. These analyses are conducted to comprehend the pathoecology of the infection, dietary habits, and, specifically for human samples, cultural and environmental features that influence the population health (Araújo and Ferreira, 2000; Ferreira and Araújo, 2011; Reinhard et al., 2013; Reinhard and Bryant, 2008). The introduction of molecular tools in paleoparasitological studies made possible the identification of parasites not recognized by microscopy in prehistoric populations (Iñiguez et al., 2003). The recovery of aDNA opened a field of study that includes the use of techniques such as Polymerase Chain Reaction (PCR) and, more recently, High Throughput sequencing (HTS)to identify not just parasites but hosts, environment, and dietary characteristics (Borry et al., 2020; Iñiguez, 2020).

Jouy-Avantin et al. (2003) created a method of coprolite description with a series of attributes fulfilled according to morphological and morphometric aspects (Jouy-Avantin et al., 2003). Paleoparasitological studies use Jouy-Avantin datasheet for coprolite identification, along with the morphological identification of mammal feces proposed by Chame (2003), Beltrame et al. (2012), Chimento and Rey (2008), Fugassa et al. (2006). Recently, the diet constitution, parasite diversity, and microbiome have been identified through technological approaches to coprolite studies, such as next generation sequencing (NGS) (Borry et al., 2020; Chessa et al., 2020; Flammer et al., 2018). Classical techniques have been widely used in coprolite studies to accomplish microscopic analysis of diet, pollen grains, vegetal composition, and active isotopes for human and animal remains (Beltrame et al., 2022; Iñiguez, 2020).

Measurements and shapes of coprolites can distinguish species of the same mammal group and, sometimes, diet composition. The work of Dalponte (1997) reported coprolites that are well known in a determined area of the study and showed specific nutrients of canids from South America (Chame, 2003; Dalponte, 1997). Chame (2003) identified that morphometry and volume patterns of terrestrial mammal feces of Northeast Brazil may reflect the capacity of mammals to spread. Integrating with studies of modern animal behavior it is possible to rebuild movements, ecosystems, and biological and ecological relationships (Chame, 2003). Demonstrating the importance of coprolites studied to understand animal or human origin, behavior, and diet.

Gruta do Gentio ll (GGll) is an archeological site located in a cave in the Unaí county of Minas Gerais, southeast Brazil, and is the most ancient site related to the Una ceramist tradition of Brazil. The Una tradition possibly originated in the Amazonia forest, and later, traces of this tradition were identified in localities of Southeast Brazil, close to the coast of Espírito Santo state, in the mountains of Rio de Janeiro, and the Cerrado biome of Minas Gerais state (Dias et al., 1984; Seda et al., 2011). The Una tradition has a particular type of pottery, small, technologically well-made with a rounded shape. Ceramic materials were submitted to a reduction burn, that has no contact with oxygen (Dias et al., 1979; Seda et al., 2011). The archeological site GGll is identified with two subsistence horizons. The hunter-gatherer horizonis the most ancient and related to the deepest layer with lithic artifacts of the Paracatu tradition (10,000 and 8125 cal kyr B.P.) (Dias et al., 1982). The later horizonrepresents the Una horticulturist population (410–3490 cal kyr B.P.), with the presence of ceramic, fabrics, baskets, animal bones, foods such as tubers, maize grains, and adornments like necklaces and bracelets. In addition, several coprolites in human burials (Dias et al., 1979; Sene, 2007) were distributed in the excavated sectors.

GGll was described as a site exclusively associated with ceremonialist events, inhabited only seasonally by the human population during funeral rituals that could last several weeks (Sene, 1999). GGll is an important archeological site because it is the first and the biggest one related to the Una tradition of Brazil, with the transition from hunter-gatherers to horticulturist people clearly detailed by the archeologists. In the first paleoparasitological studies of GGll, intestinal parasite eggs were identified in human samples related to the superficial layers excavated (Ferreira et al., 1980, 1983).

In the present study, coprolites were collected to obtain data about the human population, but during the excavations, different morphotypes of coprolites appeared, clearly indicating that the origin of these specimens was not human. The study was conducted to understand the initial panorama according to the presence of animal and human populations that utilized GGll at the same time and space related to the two horizons of subsistence. Based on the collected data and the previous paleoparasitological and archeological studies, we propose an initial paleoecological scenario, with the presence of animal and human populations in the pre-Columbian period of the Brazilian Cerrado.

Methodology

Gruta do Gentio ll archaeological site and samples

The archeological site GGll (10,000–410 B.P.) was excavated during the 1970s and 1980s by the team of the Institute of Brazilian Archeology (Instituto de Arqueologia Brasileira-IAB) under the coordination of Dr. Ondemar Diaz. GGII is situated in Unaí locality, state of Minas Gerais, Southeast of Brazil (16°15′S / 46°02′W). Coprolites had been at the IAB collection in compartments separated by burial excavation until 2017 when they were collected by the Paleogenetic Laboratory team, Laboratório de Parasitologia Integrativa e Paleoparasitologia (PL/LPIP/IOC/FIOCRUZ). The samples were obtained following the paleogenetic collection protocol of Iñiguez (2020), protected from light, preserved, and transported on ice to the Paleogenetic Laboratory (Iñiguez, 2020). After collecting, samples remained in the Paleogenetic archive until the analysis. All samples were stored at 4°C with the archeological identification.

Classification system of coprolites

Eighty coprolites related to several stratigraphic layers and different sectors of both horizons of subsistence were analyzed. The classical, non-destructive, and inexpensive morphometrical and morphological analyses were applied to bring basic information about the archeological site and the population.

The morphology and morphometry of coprolites were registered according to the attributes of Jouy-Avantin et al. (2003). Attributes indicated in the datasheet (Figure 1) were categorized, including coprolite’s color, based on the Munsell Soil Color Chart (1975) (Supplemental Figure 1), morphometrical measurements of weight, width, length, and morphological recognition of external color, shape, and volume, including macro and microremains observation. To improve a correct result and to lower the subjective taxa, double-checking of evaluations was implemented, with two operators. The descriptive form is divided into five main groups of attributes related to (1) archeological information, (2) external description of coprolites, (3) internal morphological analysis, (4) macro and microscopic data, and (5) molecular identification.

Figure 1.

An example of a coprolite identification form according to Jouy-Avantin et al. (2003) using sample GG01.

Furthermore, the morphology and morphometry of coprolites were also compared to the mammal feces classification proposed by Chame (2003), as the reference of the possible coprolite origin. Chame (2003) constructed a summary of fecal characteristics related to terrestrial mammals from America, Europe, Southern, and Eastern Africa. Including animals such as Lagomorpha, Artiodactyla order, families of Muridae, Sciuridae, Thrynomyidae, and Equinidae, primates, armadillos, large ungulates such as elephants, and a diverse scale of insectivores. Additionally, species of endemic animals of the Cerrado Biome were analyzed according to Costa and coauthors in 1981 (Costa et al., 1981).

Results

Coprolite database

All coprolites were submitted to the datasheet proposed by Jouy-Avantin et al. (2003) (Figure 1). According to the excavated data, 16 sectors contained coprolites, with 10 different colors, and constituted of 669 fragments distributed in 80 coprolites. Additionally, 11 stratigraphic layers containing coprolites, between both subsistence horizons, hunter-gatherers n = 16 and horticulturists n = 62, were cataloged (Table 1).

Table 1.

Morphology, layer, and colors of coprolites identified in all the sectors of GGll. Line colors refer to layers of color associated with each sector of the archeological site (Figure 4).

	Line Color	Layer	Datation	Horizon	Morphology	Color	Possible origin
01	Red	10/20 cm	3500 cal kyr B.P.	H	CX	5/2	Mammal
02	Dark Green	40/50 cm	8595–9040 cal kyr B.P.	HG	CX	5/2	Mammal
03	NI	NI	3500 cal kyr B.P.	H	FL	4/2	UN
04	Light Green	30/40 cm	8595–9040 cal kyr B.P.	HG	FL	4/2	UN
05	Light Brown	80/90 cm	8125–7295 cal kyr B.P.	HG	FL	4/2	UN
06	Yellow	20/30 cm	3500 cal kyr B.P.	H	CX	5/2	Mammal
07	Dark Brown	0/10 cm	NI	NI	CX	5/2	Mammal
08	Yellow	20/30 cm	1,500 cal kyr B.P.	H	FL	5/2	UN
09	Yellow	20/30 cm	1500 cal kyr B.P.	H	FL	5/4	UN
10	Red	10/20 cm	1500 cal kyr B.P.	H	CX	5/2	Mammal
11	Brown	0/10 cm	1500 cal kyr B.P.	H	CX	5/1	Mammal
12	Light Green	30/40 cm	3490 ± 410 cal kyr B.P.	H	CX	2,5/1	Mammal
13	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	CX	5/1	Mammal
14	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
15	Dark Brown	0/10 cm	3500 cal kyr B.P.	H	CX	5/2	Mammal
16	Red	10/205 cm	2–3500 cal kyr B.P.	H	CX	5/2	Mammal
17	Dark Brown	0/10 cm	2–3500 cal kyr B.P.	H	CX	5/2	Mammal
18	Red	10/20 cm	2–3500 cal kyr B.P.	H	CX	5/2	Mammal
19	Light Green	30/40 cm	3500 cal kyr B.P.	H	CX	2,1/1	Mammal
20	Yellow	20/30 cm	3500 cal kyr B.P.	H	CX	5/2	Mammal
21	NI	NI	3500 cal kyr B.P.	H	FL	5/4	UN
22	Red	10/20 cm	3490 ± 410 cal kyr B.P.	H	FL	5/2	UN
23	Light Green	30/40 cm	3490 ± 410 cal kyr B.P.	H	CX	5/5	Mammal
24	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	CX	5/5	Mammal
25	NI	CL	3500 cal kyr B.P.	H	CX	5/5	Mammal
26	NI	CL	3500 ca kyr B.P.	H	CX	5/2	Mammal
27	Dark Brown	10/20 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
28	Dark Green	40/50 cm	8595–9040 cal kyr B.P.	HG	CX	5/2	Mammal
29	Pink	60/70 cm	8595–9040 cal kyr B.P.	HG	CX	5/2	Mammal
30	Light Green	30/40 cm	8595–9040 cal kyr B.P.	HG	CX	5/2	Mammal
31	Purple	50/60 cm	8595–9040 cal kyr B.P.	HG	CX	4/2	Mammal
32	Yellow	20/30 cm	8595–9040 cal kyr B.P.	HG	CX	5/2	Mammal
33	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
34	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	5/4	Mammal
35	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
36	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	4/2	Mammal
37	Pink	60/70 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
38	Red	10/20 cm	3490 ± 410 cal kyr B.P.	H	CX	6/1	Mammal
39	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
40	Dark Green	40/50 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
41	Dark Green	20/30 cm	3490 ± 410 cal kyr B.P.	H	CX	4/2	Mammal
42	Dark Brown	0/10 cm	3500 kyr B.P.	H	CX	5/4	Mammal
43	Light Brown	80/90 cm	9–10,000 cal kyr B.P.	HG	CX	5/3	Mammal
44	NI	SV	3500 cal kyr B.P.	H	CX	5/2	Mammal
45	Light Blue	150/155 cm	9–10,000 cal kyr B.P.	HG	CX	2,5/1	Mammal
46	Dark Blue	90/100 cm	9–10,000 cal kyr B.P.	HG	CX	2,5/1	Mammal
47	NI	CL	3500 cal kyr B.P.	H	CX	2,5/2	Mammal
48	Light Brown	80/90 cm	9–10,000 cal kyr B.P.	HG	CX	5/2	Mammal
49	NI	70 line 4	3500 cal kyr B.P.	H	CX	5/2	Mammal
50	Pink	60/70 cm	8125–7295 cal kyr B.P.	HG	FL	2,5/2	UN
51	Dark Green	40/50 cm	8125–7295 cal kyr B.P.	HG	CX	5/2	Mammal
52	Dark Green	30/40 cm	3490 ± 410 cal kyr B.P.	H	CX	5/3	Mammal
53	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	CX	5/3	Mammal
54	Green Light	30/40 cm	3490 ± 410 cal kyr B.P.	H	CX	7/3	Mammal
55	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
56	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
57	Red	10/20 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
58	Red	10/20 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
59	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
60	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	SP	5/2	Cervids
61	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	FL	5/2	UN
62	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	CY	5/2	Rodent
63	NI	NI	NI	NI	FL	5/2	UN
64	NI	SL	3500 cal kyr B.P.	H	CX	5/1	Mammal
65	NI	UL	3500 cal kyr B.P.	H	FL	5/2	UN
66	Red	10/20 cm	3490 ± 410 cal kyr B.P.	H	FL	5/2	UN
67	NI	4	3500 cal kyr B.P.	H	FL	5/2	UN
68	NI	SL	3500 cal kyr B.P.	H	FL	5/2	UN
69	Yellow	20/30 cm	3490 ± 410 cal kyr B.P.	H	FL	5/2	UN
70	Red	10/20 cm	3490 ± 410 cal kyr B.P.	H	FL	5/2	UN
71	Pink	60/70 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
72	NI	01/87	3500 cal kyr B.P.	H	CX	5/2	Mammal
73	Pink	60/70 cm	3490 ± 410 cal kyr B.P.	H	FL	5/2	UN
74	Purple	50/60 cm	3490 ± 410 cal kyr B.P.	H	FL	5/2	UN
75	Dark Green	40/50 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
76	Dark Brown	0/10 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
77	Dark Blue	90/100 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal
78	NI	NI	8125–7295 cal kyr B.P.	HG	CX	2,5/2	Mammal
79	Light Brown	80/90 cm	8125–7295 cal kyr B.P.	HG	CX	5/2	Mammal
80	Light Brown	80/90 cm	3490 ± 410 cal kyr B.P.	H	CX	5/2	Mammal

CL: cleaning of layers before the excavation. SL: rescue of samples after collapsing wall; SV: saving of samples before the wall collapses; UL: samples collected during the withdrawal of the sector; NI: not informed; UN: undetermined; H: horticulturists; HG: hunter-gatherer; CX: complex; FL: flat; SP: spherical; CY: cylindrical.

Morphology and morphometry analyses

The four attributes of the volume of coprolites proposed by Jouy-Avantin et al. (2003) were identified in GGll coprolites: Flat, cylindrical, spherical, and complex (Figure 3). Undetermined nomenclature was changed to Complex in this study due to no specific volume identification. A dichotomous key was built according to Barrios-de Pedro et al. (2018) (Figure 2) to represent the classification of volumes assigned to GGII coprolites. About 51 coprolites with a type of complex volume, 20 flat coprolites, 3 spherical coprolites, and 6 cylindrical type of volume (Table 1). All samples showed the external presence of macroremains such as vegetal segments and invertebrates. According to morphometry, a vast range of lengths was identified, varying from tiny segments measuring 10 mm to huge segments of almost 30 cm (Figure 2).

Figure 2.

Dichotomous key of GGII coprolites volumes. The contoured rectangle represents the overall volume of coprolites and the external ends. The colored rectangle is the final definition of the volume, classified as flat, cylindrical, rounded, and complex. The representation of coprolites consists mainly of fragments, except for the cylindrical ones, which are complete pieces of coprolite.

Coprolite morphologies and morphometries were according to Chame (2003). Coprolites of spherical volume (Figure 3c) could be related to Lagomorpha order or some ungulates and cylindrical pellets could be related to rodents (Figure 3d). Flat and complex could not fit in any group of mammal feces volume, because of the convoluted coprolite nature associated with taphonomic effects. Additionally, different types of colors are observed: pink 7/3 (A), brown 5/2 (C, D), and dark brown 2, 5/2 (B) according to the Munsell Soil Chart (Supplemental Figure 1).

Figure 3.

Morphological identification of coprolites and coprolites fragments in stratigraphic layers of Gruta do Gentio ll. (a) A Complex fragment. (b) A Flat fragment. (c) Spherical coprolites. (d) Cylindrical coprolites.

Coprolites were collected in layers up to 155 cm in depth along with a bonfire dated by 8125 cal kyr B.P. in the North, internal part of the cave. Quadrants were made for a better spatial understanding of the disposition of the coprolites within the excavated sectors. Rather they are located in the back part of the cave, in the entryway, or close to human burials and the bonfire (Figure 4).

Figure 4.

Quadrant representing the excavated sectors of GGll. Bones are represented by the human burials identified, and the dated bonfire located at the north, external part of the archeological site. Quantity of layers is represented by the multicolored bars in each sector. Yellow quadrants – External area. Blue quadrants – Intermediate area Green quadrants – Internal area.

The results showed heterogeneity concerning the number of coprolites by sector, with NA4 and NC4 sectors with the greatest number of coprolites (n = 12) (Figure 5a). The stratigraphic layer containing coprolite by sector revealed a diverse quantity of layers excavated containing coprolites, including sector 155 cm deep, with sectors NB4 and LB0 with the greatest quantity of layers excavated with coprolites (Figure 5b).

Figure 5.

Identification and correlation between numbers of coprolite, sectors, and stratigraphic layers of Gal. (a) Number of coprolites (N = 80) by archeological sectors of Gruta do Gentio ll site. Axis x – Excavated sectors. Axis y – Number of coprolites, <> – Coprolites with no sector identification. (b) Stratigraphy of excavated samples by sector of GGll site. Axis x – Stratigraphy deep determined by colors. Axis y – Sectors. (c) Coprolite colors identified by sectors. Axis x – Colors identified by Munsell Color Chart. Axis y - Sectors. (d) Coprolite morphologies by stratigraphic deep. Axis x – Types of morphology. Axis y – Stratigraphic layers deep.

Regarding the external coprolite color, 10 colors were identified according to the Munsell Soil Chart Color. Sector NA4 showed the highest diversity of coprolite color with 6 templates (Figure 5c). Related to coprolite volume by the stratigraphy, all the volume types proposed were identified in all the layers, with the 10/20 cm and 20/30 cm deep with at least three different volumes (Figure 5d).

Discussion

When coprolites are assessed and cataloged, recording their morphology and morphometry is important. This is especially important as most subsequent analyses are destructive so there may be little remaining sample to refer back to in the future. On the data sheet by Jouy-Avantin et al. (2003), we observe that the main morphological and morphometrical information of coprolites could be stored and managed for future monitoring and organization. Categorizing is an extremely important stage in investigations of soil samples. Without proper cataloging, information that can help classify coprolites, like specific volume and measurements, can be lost in the process and during the analysis. In GGll, the coprolite composition of the excavated sectors showed heterogeneity in the distributions of coprolites per sector, stratigraphic layers, and colors, indicating no patterns for coprolite positions in the archeological site (Figure 5a–c).

The four volumes of coprolites proposed by Jouy-Avantin et al. (2003) were identified, with the complex volume predominantly in all the sectors and layers (Figure 5d). To understand the complexity of a subject, and organize data, a dichotomous key was created according to Barrios-de Pedro et al. (2018) Dichotomous keys of coprolites can categorize samples with morphotype-specific features, leading to the diagnosis of different specimens (Barrios-de Pedro et al., 2018). In GGll, the classification of coprolite datasheet had more than 50% of the volumes related to a complex or a flat sample (Figure 3). According to Thulborn (1991), dehydration undoubtedly leads to a decrease in volume, impacting shape and size (Thulborn, 1991), indicating that the layers with these types of coprolite features could have suffered of taphonomical alterations.

Studies that use morphological and morphometrical information on coprolites have been used in the last decades by archeological (de Araújo et al., 1985; Taylor et al., 2020; Teixeira-Santos et al., 2015) and Paleontological (Chipman et al., 2020; Francischini et al., 2016; Rakshit et al., 2019) investigation, including differential diagnosis to identify diet and coprolite composition (Qvarnström et al., 2019; Shillito et al., 2020; Zhang et al., 2019). Diet analysis is the most common strategy to identify coprolite origin, along with isotopic identification (Pucu et al., 2020; Verostick et al., 2019). As mentioned, more recently, other methods are being used to categorize coprolites, like PCR and NGS. Those techniques recover genetic sequences of aDNA related not just to samples of coprolites, but other archeological and paleontological specimens, such as bones and sediments of latrines (Delgado et al., 2020; Hong et al., 2019; Iñiguez, 2020).

In the present study, no pattern for coprolite disposition is seen in the representation of layers per sector with coprolites, human burials, and both coprolite and human burial (Figure 6). During the excavations, most of the coprolites were associated with burials along all the extensions of the archeological site. However, there are sectors and layers without human burials where coprolites can be found, as we see in all layers of the LB0 sector and the superficial layers of the NC4 sector, related to the dated bonfire. Some of the sectors have deep layers with both, coprolites and human burials, like the NA4 sector.

Figure 6.

Representation of coprolite and human burial presence by the layers in each sector. (a) Layers with coprolites (blue rectangle), layers with coprolite and human burials (brown rectangle), and layers with only human burial (light green rectangle). (b) Macro representation of GGII layers, bone symbols represent human burials, feces symbols represent coprolites and stone symbols represent rocks found in some layers.

The GGll excavation was divided into three main groups, the external, intermediate, and internal areas (Figure 4). The entryway and near the bonfire have a clear high quantity of coprolites. Sectors and layers with more coprolites and human burials (Figure 5) are related to the internal area of the cave where the bonfire is located, mainly in sectors NB4 and NC4. The domain of fire is deeply related to human existence, the fire maintained by cultural practices has an important role in all fields of human life, including cooking, heating, protecting, and celebrating (Scheel-Ybert, 2013). The larger quantity of coprolites in layers of bonfire sectors could be related to the principal locations human populations used inside a cave in pre-Columbian times, where bonfires were even used for burial ceremonies. The greater quantity of coprolites in the entry of the cave could be associated with it being a transition zone from the inside to outside the cave. Animals would also be attracted by the preparation and consumption of food or by the food offered in ceremonies, both situations could take place around the fireplaces.

More coprolites of the horticulturist horizon were detected (Table 1) and could be related to the horticulturist populations having the characteristic of staying in a specific place to store, cultivate, and harvest (Baeyer, 2010). The shift from hunter-gatherer populations to horticulturist ones is marked by the first epidemiological transition, when humans changed the gathering lifestyle to a sedentarism routine, primarily expressed by food production (Barrett et al., 1998). The different lifestyles led to changes in the human social organization, including demography. The relevant quantity of coprolites in the horticulturist horizon of GGII could be directly related to the number of individuals in the populations, which increased significantly during the most recent horizon of subsistence.

GGll is characterized as a ritualistic archeological site, where the human population utilized the space only for some days until the ritual was complete (Sene, 2007). In the meanwhile, animals of different classes and species could have used the cave for shelter and hunting. In addition, animals possibly were in association with humans at the same time and space, because feathers, teeth, shell adornments, and animal skeletons were associated with human burials in some graves. Extremely preserved bones of a Papagaio bird (Parrot), an animal of the Psittacidae family, were identified as associated with a human burial in the study of Sene (2007) and recognized as a possible domesticated specimen. Moreover, a musical instrument made from a gastropod shell was found in a human burial as well, amongst a lot of freshwater shells, showing the possibility of a direct association with several animals like invertebrates, birds, and mammals classes identified in the Pleistocene Cerrado of Brazil, such as rodents, peccary, armadillo, and canids (Vasconcelos et al., 2015).

Indeed, by morphological and morphometrical investigations, nine coprolites, with spherical and cylindrical shapes, may give information about their origin (Figure 3). These coprolites were found in a stratigraphic layer 30 cm deep. The spherical coprolites were found in the NC4 sector of the site in the north part of the cave, where the bonfire is located, dated with radiocarbon, and correlated to the hunter-gatherer horizon. The cylindrical coprolites were found in the NB2 sector, still in the north part but not associated with the dated bonfire. The latest is located in a layer dated into 3490 ± 410 cal kyr B.P. horizon related to the Una tradition and the horticulturist subsistence layer.

Spherical coprolites are associated with animals of the order Lagomorpha or superorder Euungulata. In the Brazilian biome of Cerrado, state of Minas Gerais, there are three species of cervids, Ozotoceros bezoarticus (Veado-campeiro) and two species of the genus Mazama, Mazama americana (Veado-mateiro) and Mazama gouazoubira (Veado-catingueiro). Regarding Lagomorph animals, species of the genus Sylvilagus are commonly found in the Cerrado of Minas Gerais (Costa et al., 1981). Due to the large size of the spherical coprolite, there may be a possibility this sample is related to one of the cervids identified in the GGII region.

Rodents belonging to the Cerrado of Brazil are distributed in 10 families, 34 genres, and more than 90 species (Costa et al., 1981), several species live in Minas Gerais State. We can suggest the cylindrical coprolite corresponds to rodent remains based on its morphological and morphometrical data, and its slight size. Rodents were probably circulating in the area of the site in the horticulturist horizon, because of the dating of layer where coprolites were found. To Kerber in 2017, South American rodents belong to six main groups: Caviomorpha, Cricetidae, Sigmodontinae, Sciuridae, Heteromyidae, and Geomyidae, all with different origins and likely to be found in Brazil. In an archeological site of Minas Gerais identified in the Lagoa Santa complex, the Gruta Cuvieri, bones of rodents Dasyproctidae, agouties (Dasyprocta aguti), and pacas (Cuniculus paca) were identified in Pleistocene times (Chahud, 2020; Kerber, 2018), indicating these animals were circulating in the Cerrado biome long before the horticulture subsistence period.

Morphometries and morphologies of coprolites presented in the current study agree with previous paleoparasitological and paleogenetic studies conducted on GGll coprolites (Ferreira et al., 1980, 1983; ). Ferreira et al. (1980) analyzed 22 human coprolites found in the layers of 410–3490 cal kyr B.P., corresponding to Una horticulturist population and identified helminth eggs of Trichiura trichiura, and ancylostomids, possibly Necator americanus, geohelminth parasites specific to the human host, result that confirmed the producer of coprolites (Ferreira et al., 1980). Later, Ferreira and coauthors studied a naturally mummified body of a child, which was collected inside the cave, and helminth infection by T. trichiura and ancylostomids in GGII was confirmed. Trichostrongylus sp. eggs, a zoonotic helminth parasite, were identified in GGII coprolites that exhibited a complex morphology consistent with Group IX coprolite descriptions by Chame (2003), with shape and size indicative of mammalian hosts. The paleogenetic analysis identified these samples as being of human origin (Gurjão, 2020). Ancylostomatids, parasites that can infect mammals with species-specific to humans, were also identified in a complex-type coprolite with morphology related to the IX Group, and the human origin was also confirmed through paleogenetic analyses (Gurjao, 2019). Another complex-type coprolite was identified as an ocelot (Leopardus pardalis) producer, according to paleogenetic analysis, and also contained helminth eggs belonging to Echinostoma sp. and Spirometra sp., zoonotic parasites that need an aquatic environment to complete their life cycle (Gurjao, 2019). Finally, a coprolite, whose producer was identified as jaguar (Panthera onca) through paleogenetics and with capillariid parasite eggs, was determined as a complex-type coprolite. The integration of these results supported that complex-type coprolites classified in the present study were mainly from human and feline producers following paleoparasitological and paleogenetic data. The paleoparasitological and paleogenetic study conducted at GGII, along with the morphology and morphometry of coprolites, unveiled significant findings about the human and parasitic history of the pre-Columbian population of southeast Brazil.

During the excavations of GGll, which was identified as a human ceremonial archeological site, were found ceremonial accessories made using shells and animal teeth, indicating GGll people had close contact with the local fauna. Rock paintings on the cave walls and the presence of several bones from small and large animals were observed in the 11 stratigraphical layers. With this finding, we can speculate about the relationship between GGll population of humans and animals, evidencing the clear complexity of the archeological site, provided by the primary characterization of the coprolites. As perspectives, GGII coprolites will be submitted to extensive new paleoparasitological and paleogenetic analyses in order to contribute relevant data about the origin of producers, parasitic infections, diet, and health status in the paleoecological context of GGII.

Conclusions

The morphological and morphometrical analysis of Gruta do Gentio II coprolites demonstrate their vast diversity, in several stratigraphic layers, colors, and different sectors, indicating the possibility not only humans, but different species of animals circulated in the cave between 3490 and 8125 years cal kyr B.P., in the same geographical space and at the same time. This arose the hypothesis that the different populations of humans and animals of GGll shared more than geographical space, such as food and water sources, prey, and even parasites.

Using different tools to catalog, register, and classify coprolites is significant since samples will be destroyed for further analysis. Most of the coprolites in GGII were described as having flat or complex volumes due to taphonomical processes when utilizing the datasheet proposed by Jouy-Avantin et al. (2003) or the data set. Nevertheless, spherical and cylindrical coprolites give insights into the possible origin of samples, such as cervids and rodents, animals endemic to Minas Gerais Cerrado in Brazil.

Those are the first findings of the coprolite analysis of Gruta do Gentio ll and despite the use of differential techniques to presume coprolite origin, the morphological and morphometrical study is still important to initial results and the construction of a paleoinventory. Results showed the importance of the application of a variety of techniques to classify coprolites by morphology and morphometry, even if samples can be affected by taphonomy. The possibility that a great variety of distinct coprolites could indicate a vast diversity of species that circulated inside the cave between the subsistence horizons is not excluded.

Thus, an ecological interaction between humans and mammal species may have happened in both subsistence horizons, hunter-collector and horticulturist, with probably different diets and parasitic infections related to the first epidemiological transition, from the Pleistocene to a more technological population in the Holocene. Other tools should be applied to understand more about the paleoecological and paleoepidemiological scenario of this pre-Columbian archeological site, including paleoparasitological, paleogenetic, and paleogenomic analysis.

Supplemental Material

sj-docx-1-hol-10.1177_09596836241275019 – Supplemental material for Coprolite diversity from the archeological site Gruta Do Gentio Ll, Unaí, Minas Gerais, Brazil

Supplemental material, sj-docx-1-hol-10.1177_09596836241275019 for Coprolite diversity from the archeological site Gruta Do Gentio Ll, Unaí, Minas Gerais, Brazil by Ludmila Gurjão, Ondemar Dias, Jandira Neto and Alena Iñiguez in The Holocene

Footnotes

Acknowledgements

We would like to thank the Paleogenetic team and the Laboratório de Parasitologia Integrativa e Paleoparasitologia, Instituto Oswaldo Cruz/FIOCRUZ staff members for their support and cooperation. We would also like to thank Dr. Gláucia Sene and Dr. Paulo Seda from the Universidade do Estado do Rio de Janeiro for additional archeological data about GGII archeological site. We also thank Dr. Maurício Vasconcellos from the Laboratório de Avaliação e Promoção da Saúde Ambiental (LAPSA/FIOCRUZ) for the microscopy lease and Dr. Sérgio Miranda also for microscopy support. We thank Paloma Câmara for the support in the development of the pictures and figures.

Author contributions

Ludmila Gurjão: Formal analysis; Investigation; Methodology; Writing – original draft; Writing – review & editing.

Ondemar Dias: Data curation; Resources; Validation; Visualization.

Jandira Neto: Data curation; Resources; Validation; Visualization.

Alena Iñiguez: Conceptualization; Data curation; Funding acquisition; Project administration; Resources; Supervision; Validation; Writing – review & editing.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This research was financially supported by grants and fellowships from Fundação de Amparo à Pesquisa do Rio de Janeiro (http://www.faperj.br/) (AMI, Grant Numbers E-26/210.131/2023, E-26/201.069/2021); Conselho Nacional de Desenvolvimento Científico e Tecnológico (http://www.cnpq.br/) provided fellowships (AMI, Grant Number 315634/2021-9); Coordenação de Aperfeiçoamento de Pessoal de Nível Superior () (LLG, Grant Numbers 88887.508110/2020-00, 88887.694725/2022-00). The funding entities were not involved in the formulation of the study, data collection, analysis, decision to publish, or manuscript preparation.

ORCID iD

Alena Iñiguez

Supplemental material

Supplemental material for this article is available online.

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