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NEW PARASITE OCCURRENCES in Tamandua Tetradactyla (PILOSA: MYRMECOPHAGIDAE) in the NORTHEAST of BRAZIL: a PALEOPARASITOLOGICAL STUDY

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NEW PARASITE OCCURRENCES in Tamandua Tetradactyla (PILOSA: MYRMECOPHAGIDAE) in the NORTHEAST of BRAZIL: a PALEOPARASITOLOGICAL STUDY Oecologia Australis 24(1):141-153, 2020 https://doi.org/10.4257/oeco.2020.2401.11 NEW PARASITE OCCURRENCES IN Tamandua tetradactyla (PILOSA: MYRMECOPHAGIDAE) IN THE NORTHEAST OF BRAZIL: A PALEOPARASITOLOGICAL STUDY Mônica Vieira de Souza1,2, Marcia Chame1,2, Sheila Maria Ferraz Mendonça de Souza1, Gisele Daltrini Felice3, Niéde Guidon3 & Luciana Sianto1,2* 1 Fundação Oswaldo Cruz (Fiocruz), Escola Nacional de Saúde Pública Sérgio Arouca (ENSP), Laboratório de Paleoparasitologia e Ecologia, Rua Leopoldo Bulhões 1480 Manguinhos, CEP: 21041-210., Rio de Janeiro, RJ, Brazil. 2 Instituto Nacional de Ciência e Tecnologia de Arqueologia, Paleontologia e Ambiente do Semiárido do Nordeste do Brasil (INAPAS). Centro Cultural Sérgio Motta, s/n – Campestre, CEP: 64770-000, São Raimundo Nonato, PI, Brazil. 3 Fundação Museu do Homem Americano (Fumdham), Centro Cultural Sérgio Motta, s/n, CEP: 64770-000, São Raimundo Nonato, PI, Brasil. E-mails: [email protected]; [email protected]; [email protected]; [email protected]; guidon@ fumdham.org.br; [email protected] (*corresponding author) Abstract: Paleoparasitological studies have revealed parasite eggs in coprolites from humans and other animals, obtained in archaeological sites in the New and Old World. However, to date, the only parasite found in anteaters coprolites is Gigantorhynchus echinodiscus (Acanthocephala: Gigantorhynchidae). Here we present the results of paleoparasitological analysis of nine Tamandua tetradactyla coprolites, of layers dated from 8,870 and 3,190 years BP, collected in three archaeological sites: Toca dos Coqueiros, Toca da Passagem and Toca do Enoque, rock shelters located in the southeast of the Piauí state, Brazil. Each coprolite was rehydrated in 0.5% trisodium phosphate solution, homogenized with a glass rod for spontaneous sedimentation. A minimum of 20 slides of each sample was examined using light microscopy. Acanthocephalan eggs of three morphotypes were found: G. echinodiscus, Macracanthorhynchus hirudinaceus and Oligacanthorhynchus sp.. Three morphotypes of Nematoda eggs and oocysts of cf. Entamoeba sp. were also found. The finding of G. echinodiscus, a species commonly reported in anteaters, reinforces the previous data and highlights the specificity and antiquity of this host-parasite interaction. This is the first finding of Oligacanthorhynchidae and Aspidoderidae parasites in T. tetradactyla. These findings evidence the need for more studies of the parasitic fauna of T. tetradactyla from both ancient and current times aiming to broaden the knowledge about the parasite diversity of this host and the evolutionary processes that led to these interactions. Keywords: Acanthocephala; anteater; endoparasites; Paleoparasitology; semiarid. INTRODUCTION the north of Argentina and Uruguay, and occurs in all Brazilian biomes (Oliveira & Vilella 2003). It has Tamandua tetradactyla (Linnaeus, 1758), popularly medium size, a semi-prehensile tail, and short hair. known as collared anteater or mixila, belongs, This species is arboreal and feeds mainly on ants together with other anteaters, to the Family and termites (Nowak 1999). Anteaters have a large Myrmecophagidae Gray, 1825, restricted to the foraging area, due to the need for daily consumption Americas. It is found from the east of the Andes to of a large number of insects, dedicating part of their 142 | Parasites from Tamandua tetradactyla coprolites day to exploration activities (Montgomery 1985). Echinostoma sp. (Trematoda: Echinostomatidae) Currently, the species is classified in the category in feline coprolites (Sianto et al. 2014). However, of “least concern” according to the IUCN Red List the knowledge about anteater’s parasites in the (2014), threatened by the transformation of the past is still scarce. Here we report the finding of natural landscapes to agropastoral fields (Oliveira eggs of three morphospecies of Acanthocephala, & Vilella 2003). Nematoda eggs and larvae, and protozoan oocysts Studies investigating the parasitic fauna of in anteaters’ coprolites from the region known as living anteaters are frequent, carried out with “The Cradle of American Man”, in the Brazilian captive and free-living animals (Lainson & semiarid. Shaw 1990, 1991, Diniz et al. 1995, Freitas et al. 2006). However, Gigantorhynchus echinodiscus MATERIALS AND METHODS (Diesing, 1851) Hamann, 1892 (Acanthocephala: Gigantorhynchidae) is the only Acanthocephala Study area described so far for these animals, with dates of up Two archaeological sites are located in the Serra to 32,000 years (Ferreira et al. 1989). da Capivara National Park: Toca dos Coqueiros The identification of parasites in ancient remains (768076 UTM E, 9022106 UTM N) and Toca da helps to understand the evolution and ecology of Passagem (750514 UTM E, 9049988 UTM N), and parasitic infections. It also provides information one in the Serra das Confusões National Park: Toca about the paleoenvironment and the paleoclimate, do Enoque (658743 UTM E, 8988649 UTM N), both by studying their biological cycles, since parasites in the state of Piauí, Northeast Brazil (Figure 1). The are influenced by biotic and abiotic factors (Hugot Toca dos Coqueiros site is a rock shelter, located in et al. 1999, Arriaza et al. 2010, Beltrame et al. 2015). Serra Talhada, municipality of Coronel José Dias, The interest in parasitism in nonhuman animals state of Piauí. In this site, the skeleton of a man from prehistory has intensified. Nowadays, dating back 11,000 years BP was found associated similar studies are conducted in several countries, with lice-infested hair (Lessa & Guidon 2002). One providing data that prove the antiquity of host- coprolite collected from a layer dated 8,870 ± 60 parasite relations (e.g. Reinhard 1990, Gonçalves et years BP was analyzed. Toca da Passagem is also al. 2003, Sianto et al. 2017). a rock shelter located in the northwestern part Animal coprolites are often studied in of Serra da Capivara, in the Serra Branca region, Paleoparasitology, and the first study in Brazil also in the municipality of Brejo do Piauí. Cave was conducted by Araújo and colaborators paintings and lithic pieces were the only vestiges (1980), who found eggs of Parapharyngodon of human occupation found until now (Fumdham sceleratus (Nematoda: Pharyngodonidae) in lizard 2007). From this site, one coprolite of the family coprolites dating from 9,000 years BP. Other studies Myrmecophagidae was recovered from an conducted later, in Brazilian samples, helped to archaeological layer dated of approximately 3,190 identify new parasite species, occurrences in new ± 70 years BP. The third site, Toca do Enoque, is a hosts and regions, or to establish the antiquity rock shelter located inside the Serra das Confusões of these relations. As examples, we may cite the National Park, in the Serra das Andorinhas, finding of eggs of the species Strongyloides ferreirai municipality of Guaribas (Guidon & Da Luz 2009). n. sp. (Nematoda: Strongyloididae), Trichuris A set of well-preserved human graves was found sp. (Nematoda: Trichuridae) and Syphacia sp. associated to a great amount of ornaments made (Nematoda: Oxyuridae) in coprolites of Kerodon with animal matter (Guidon & Da Luz 2009, Faure rupestris (Rodentia: Caviidae) (Araújo et al. 1980, et al. 2011). The occupancy dates for the site are 1989, Souza et al. 2012); and Echinopardalis between 8,270 ± 40 and 3,430 ± 40 years old AP sp. (Acanthocephala: Oligacanthorhynchidae) (Guidon & Da Luz 2009). From this site, seven (Noronha et al. 1994); Spirometra sp. (Cestoda: samples of anteater coprolites were recovered. Diphyllobothriidae) , Toxocara cati, (Nematoda: Archaeological excavations in these sites were Toxocaridae), Calodium cf. hepaticum (Nematoda: carried out by the team of archaeologists of the Capillaridae), Trichuris cf. muris, Oncicola sp. American Man Museum Foundation (Fumdham), (Acanthocephala: Oligacanthorhynchidae) and who recovered and sent the coprolites to the Oecol. Aust. 24(1): 141–153, 2020 Souza et al. | 143 Figure 1. Location of Serra da Capivara National Park, Serra das Confusões National Park, and the archaeological sites of Toca do Coqueiro, Toca da Passagem and Toca do Enoque, in the southeast of the state of Piauí, Brazil. Laboratory of Paleoparasitology of the Oswaldo previous occurrence records in hosts, according to Cruz Foundation, Rio de Janeiro, for analysis. All the current literature. archaeological sites were occupied by human groups in the prehistory. RESULTS Paleoparasitological analysis All nine coprolites were identified as belonging The identification of the zoological origin to T. tetradactyla because of the morphological of the coprolites (Figure 2) was made in the characteristics of the material: long, cylindrical laboratory considering morphometric and food and continuous, and compatible morphometry content analyses (which is mostly composed of for this species, ranging from 3.00 to 6.50 cm x Hymenoptera (ants) and Isoptera (termites) for 1.50 to 2.50 cm, according to those described by the family Myrmecophagidae, as proposed by Chame (2003). In the analysis of the macroscopic Chame (2003)). Small fragments (between 0,5 and remains, fragments of Hymenoptera (ants) and 1g) of each coprolite were immersed separately Isoptera (termites) were identified, which are items in 0.5% aqueous solution of trisodium phosphate usually found in dietary studies of this anteater for a period of 72 hours (Callen & Cameron 1960), species (Chame 2003), confirming the zoological followed by
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