New observations from the intestinal fauna of Kerodon rupestris (Wied, 1820) (Rodentia, Cavidae), Brazil: a checklist spanning 30,000 years of parasitism

(With 1 figure) Abstract This checklist of parasites of Kerodon rupestris , an endemic rodent from the Brazilian semiarid region, revealed records of 25 enteroparasite taxa comprising Cestoda (Anoplocephalidae), Trematoda, Acanthocephala and Nematoda (Ancylostomidae, Ascarididae, Heterakidae, Oxyuridae, Pharyngodonidae, Trichuridae, Capillariidae, Trichostrongylidae, and Strongyloididae), and two taxa of coccidian. Paleoparasitological and parasitological studies published until 2019 were assessed in the present study and locality information, site of infection, sample dating, and host data were summarized from each reference. Analyses of recent feces and coprolites revealed the highest species richness in the Piauí State. The chronological data corroborated that Trichuris spp. and oxyurids are part of the parasitic fauna of K. rupestris . This represents the first checklist of intestinal parasites Acanthocephala e Nematoda (Ancylostomidae, Ascarididae, Heterakidae, Oxyuridae, Pharyngodonidae,


Introduction
Infections caused by parasites have an important role in conservation biology, for management decisions and issues related to the biology of the host population (Hudson, 2005;Thompson et al., 2010). For many vertebrate species there is a deficiency in the knowledge of their parasite fauna, thus important data area lacking concerning components of biodiversity (Poulin and Morand, 2004). Rodents account for approximately 44% of extant mammal species (see Wolf and Sherman, 2007), and serve as reservoirs for many zoonotic parasites. There are few parasite inventories from wild rodents in Brazil, and the Brazilian Northeast is especially deficient for these studies.
The genus Kerodon Cuvier, 1825 belongs to Caviidae and includes two endemic species from Brazil: K. rupestris (Wied-Neuwied, 1820) and K. acrobata Moojen, Locks andLangguth, 1997 (Oliveira andBonvicino, 2011). These species exhibit larger corporeal size than other species in the Caviinae. Both K. rupestris and K. acrobata have inhabited the semi-arid region of Brazil since the Pleistocene. These rodents are also reported in small zones of the humid region in the Northeast, and northern regions of Minas Gerais State, Southeast (Moojen, 1952;Alho, 1982;Almeida et al., 2008). Both species' habitats are confined to rocky outcrops and walls of mountains where they shelter in cracks (Oliveira and Bonvicino, 2011;Lacher Junior, 2016). Historically, these rodent species suffer from hunting pressure, as they are culturally used as an alternative source of animal protein by population in the interior of northeastern Brazil (Almeida et al., 2008;Lacher Junior, 2016). They are easily hunted and highly sought after due to their large size and the quality of the meat, respectively (Alves et al., 2009;Oliveira and Bonvicino, 2011). Kerodon rupestris is considered a species of least concern because it has a sizable population and occurs in protected areas according to the List of Species Threatened by the IUCN (Catzeflis et al., 2016;Lacher Junior, 2016). Kerodon rupestris serve as a host for blood feeding triatomines, Chagas disease vectors, in the Northwest Brazil, Caatinga biome, thus, it plays an important role in Trypanosoma cruzi transmission (Bezerra et al., 2014;Almeida et al., 2016).
Parasitological studies in K. rupestris have been performed that analyze feces, coprolites and enteric helminths have been reported from necropsies in several regions and archaeological sites in the Northeast of Brazil (i. e. Rodrigues et al., 1985;Araújo et al., 1989;Almeida et al., 2008;Lima et al., 2017). The main objective of this study is to compile and summarize information about enteroparasites reported in K. rupestris a Brazilian endemic rodent.
The following references were used in the list for classification and systematic arrangements: Levine (1988) and the current literature for Apicomplexa (i. e. Morrison 2009); Khalil et al. (1994) for Cestoda; Vicente et al. (1997) for Nematoda;and Amin (2013) for Acanthocephala. In addition, the checklist includes some helminth species recorded only to the order or filo level (undetermined species). The names of the species follow those provided in the most recent taxonomic literature.
The species of helminths and coccidian are presented in alphabetical order, followed by information on the locality of collection, site of infection and reference. The checklist includes helminths recorded only at the genus level (undetermined species).

Results
Reports of parasites of K. rupestris consisted of 25 enteroparasite taxa identified based on morphometrics of eggs, oocysts and cyst as well as from whole parasite animals. Enteroparasites including Nematoda (n=20), Cestoda (n=1), Trematoda (n=1), Acanthocephala (n=1) and coccidians (n=2). A total of 6 partially identified species of helminths studies was also included here. Nine and 20 taxa were found in coprolites and recent fecal samples, respectively ( Figure 1). Nineteen records were found in the literature that reported on fecal parasites; 6 (31.6%) were paleoparasitological analyses and 13 (68.4%) used recent feces of K. rupestris. The list of species and genera reported follows in this section and further information on the studies is summarized in Table 1. The coccidians, cestodes, and trematodes did not appear in past periods in K. rupestris. Trichuris spp. (11 reports), Strongyloides spp. (7 reports), and P. uncinata (5 reports), are the enteroparasites that infected the host with the highest prevalences of 58%, 37% and 26%, respectively. Strongyloides ferreirai was described in K. rupestris and found in 8,000-year-old samples until the present. Paraspidodera uncinata appears in three studies with prevalence that reach 31%. Lagochilascaris sp. was identified for the first time after 30 years of studies in the region, with K. rupestris acting as an intermediate host.

Discussion
Intestinal helminths that have a close and long association with their hosts over the time, may reflect behaviors and lifestyles of rodents as well as with the local environmental conditions, allowing a better understanding of the hostparasite relationship (Hugot et al., 1999;Ferreira, 2011). In this work, we observed a large number of intestinal taxa in K. rupestris. These studies on K. rupestris began in the 1980s, in the Serra do Capivara National Park, with the aim of comparing the results obtained by Paleoparasitology (Felice et al., 2014). Since then, the most frequently reported taxa have been the nematode Trichuris spp., followed by Oxyuridae and Ascarididae. The first study registered was conducted by Vaz and Pereira (1934) who reported the presence of Syphacia criceti (Nematoda: Oxyuridae) in a necropsied animal dead in captivity in São Paulo, Brazil. Trichuris sp. is one of the oldest helminths recorded in the New World, at 30,000 years BP (Ferreira et al., 1991).
Eimeria sp. was the only coccidia report in K. rupestris, and could be an occasional parasite, since is found in a great diversity of hosts in Brazil as Canidae, Felidae, Suidae, ruminant mammals, birds, and few rodents. However, others coccidia were reported in the region as Giardia sp., Cryptosporidium sp., and Cystoisospora sp., but in other caviids (Gressler et al., 2010). The survey presented here, spanning more than 80 years of studies, shows that the analyses have been done focusing mainly on helminth parasites and little is known about the protozoan parasites.
Trichurids are present in all vertebrate groups, but mainly in birds and mammals (Anderson, 2000;Schmidt and Roberts, 2009). They possess a stenoxenic cycle adapted to a single host or hosts phylogenetically close related. The eggs are quite resistant to environmental factors due to their thick shell and can remain viable in the soil for up to six years (Fortes, 1997). Twenty-seven species of Trichuris were described in rodents from South and North America, with only four species reported in Brazil, one in Caviidae (Yamaguti, 1963;Robles et al., 2018). The species T. gracilis and T. muris were reported in studies with ancient and modern material (Almeida et al., 2008;Vieira de Souza, 2013;Vieira de Souza et al., 2019;Saldanha, 2016). In the more recent study, Trichuris sp. eggs were found near human villages, where the small populations of K. rupestris remained in the border areas of the hill ranges and rocky canyons (Saldanha, 2016;Vieira de Souza et al., 2019). It is not possible to affirm that the same species is found in modern and ancient material, however, the present review shows the persistence of the Trichuris genus in this Brazilian region for at least 30,000 years, until present day. The data allow to speculated a possible adaptation of this parasite to the climate, since the genus is dependent on specific conditions of humidity and temperature to conclude its biological cycle in the soil. The suitable temperature for the development of Trichuris sp. eggs in soil varies between 25 °C and 37.5 °C, with lower temperatures retarding or preventing the process, and higher temperatures accelerating or harming egg development (Spindler, 1929;Vejzagic et al., 2016). In periods of rain, Trichuris sp. becomes more active due to greater humidity, while in periods of less humidity, such as in the dry season, the reproduction of helminths is low, with little egg elimination. In times of drought, however, the parasite may remain in available humid places (Spindler, 1929;Vejzagic et al., 2016).
Capillaria, which belongs to the same order as Thichuris sp., is a large genus that includes species found in almost every organ and tissue of all vertebrate classes (Schmidt and Roberts, 2009). Therefore, finding eggs in K. rupestris feces may be an occasional case due to the rodent's coprophagy habit.
Oxyurids mainly infect mammals, but also invertebrates, amphibians and birds (Hugot, 1988). They have a high host specificity and a monoxenic cycle, with transmission and development similar in invertebrate and vertebrate hosts (Hugot, 1988;Hugot et al., 1999;Anderson, 2000). Oxyuroidea are currently grouped into three families: Oxyuridae, Pharyngodonidae and Heteroxynematidae (Skrjabin et al., 1974;Hugot, 1988;Petter and Quentin, 2009). According to the present review, the oldest oxyuriid recorded in K. rupestris was Syphacia sp., 5,300 years ago. Modern records included two studies in necropsied animals and one in feces. Syphaciinae is apparently a recent group that emerged and dispersed in the main groups of rodents, with morphological adaptations of their different hosts (Hugot, 1988). However, Oxyuridae have fragile and light eggs, deposited in the perianal region of the host, which may hamper the number of egg findings in feces. Other oxyurid reported was Parapharyngodon sp. (Pharyngodonidae), parasite of reptilians, in Serra da Capivara National Park. The finding represents an accidental parasitism event, related to the ingestion of lacertid feces (Sianto, 2009). Helminthoxys sp. was most recently recorded for the first time in K. rupetris from the same region, parasites of neotropical caviomorphas rodents that inhabit the caecum and large intestine of their hosts (Hugot and Sutton, 1989). It currently comprises nine species, with H. freitasi Quentin, 1969and H. urichi (Cameron & Reesal, 1951) Hugot, 1986 described for rodents from Brazil (Gonçalves et al., 2006;Quentin, 1969).
Eggs of nematodes belonging to the genus Paraspidodera (Gardner, 1991), which infect Caviidae, Dasyproctidae and Leporidae (Vicente et al., 1997) were also reported. In Brazil, three species of Cavia (C. fulgida, C. porcellus and C. aperea) were cited as hosts for Paraspidodera uncinata (Vicente et al., 1997). Since they are in sympatry with K. rupestris, it is possible to suggests that they share these parasites. Another interesting finding is Lagochilascaris cf. minor, a parasite of Public Health importance (Saldanha, 2016). However, it was not possible to confirm true parasitism due to lack of complementary information on the biological cycle of this helminth. The parasite has been identified in humans (Fortes, 1997), dogs and domestic cats (Campos et al., 1992). According to experimental studies, rodents would act as intermediate hosts of Lagochilascaris spp. (Campos et al., 1992). Other authors argue that rodents can be considered definitive hosts of L. minor due to the observation of an adult helminth, but without data of egg laying .
Thysanotaenia congolensis is a cestode currently described for African rodents (Dronen et al., 1999), and was found in a single study in Rio Grande do Norte (Almeida et al., 2008). Thysanotaenia congolensis is a cestode currently found in African rodents of the Thynomyidae family (Dronen et al., 1999). However, there is one report in K. rupestris from Rio Grande do Norte, Brazil (Almeida et al., 2008). The authors suggested that their presence in K. rupestris is probably due to the common origin of these rodent families, or could be acquired by cohabitation with other caviomorphas, as already suggested for Vianella lenti, parasite of Galea spixii, also found in K. rupestris (Almeida et al. 2008).
A species of Strongyloides was described only for the host K. rupestris and named S. ferreirai by Rodrigues, Vicente and Gomes (1985).
In addition, it has coprophagic habits (Moojen, 1952;Alho, 1982;Chame, 2007;Almeida et al., 2008), that allow the acquisition of parasites from sympatric animals, as canids and felines. Investigations of the helminth fauna could help in the monitoring of parasite populations in the region, in the prediction of the emergence or extinction of parasites species, and in the impacts that these ecological processes may have on future of animal populations (Ogunseitan, 2005).
In conclusion, the present compilation of literature demonstrated that Trichuris spp. are still the most reported helminths parasitizing K. rupestris, followed by oxyurids. Consequently, they appear to be, in fact, the parasitic fauna of this rodent. Sporadic reports of other helminths and coccidia are probably related to the presence of animals that cohabit the region, or to anthropization.
This survey constitutes the first checklist of enteroparasites in K. rupestris. These data may be useful for studies on the biology of local species conservation.