Evidence of co-parasitism between different species of chiggers (Trombidiformes: Trombiculidae) parasitizing cricetid rodents in Morro Grande Forest Reserve, São Paulo State, Brazil

Chigger mites are ectoparasites of terrestrial vertebrates and can even accidentally bite humans, causing lesions on their skins. The coparasitism is gradually being reported for this family, and recent studies have highlighted this relationship worldwide. In Brazil, only some records of chigger species co-parasitizing rodents and lizards in the Pernambuco and Piauí States were done. The present study reports six co-parasitism situations in cricetid rodents collected in the Morro Grande Forest Reserve, Cotia Municipality, São Paulo State, Brazil.

Many studies have been done on the taxonomy and systematics of chigger mites, but little is known about their ecology. The co-parasitism relationship exists for mites and is gradually being reported for this family as well. Although there are few records in literature (Goff 1979), recent studies have highlighted the co-parasitism within different species of chiggers around the world (Barnard et al. 2015;Moniuszko et al. 2018;Jacinavicius et al. 2019;. In Brazil, some co-parasitism cases were already reported for two states (Jacinavicius et al. 2019;. In Pernambuco State, Pseudoschoengastia petrolinensis Jacinavicius, Bassini-Silva & Barros-Battesti, 2019, Eutrombicula batatas (L., 1758) and Quadraseta falconensis Goff & Brennan, 1977 parasitizing the same whiteeared opossum, Didelphis albiventris Lund, 1840 (Didelphimorphia: Didelphidae) and also, P. petrolinensis and Q. falconensis were collected again together in a second host of the same species, D. albiventris, in the same state (Jacinavicius et al. 2019). While in the state of Piauí, six cases of co-parasitism were reported, (1) Eutrombicula alfreddugesi (Oudemans, 1910), Microtrombicula brachytrichia Brennan, 1971 Goff, Whitaker & Dietz, 1983; and P. klompeni and P. petrolinensis .
The taxonomy chigger mites survey of Morro Grande Forest Reserve, Cotia Municipality, São Paulo State, Brazil, was previously reported by Jacinavicius et al. (2015Jacinavicius et al. ( , 2018aJacinavicius et al. ( , 2018b. However, the present study aims to show the co-parasitism observed between different chigger mite species collected from small mammals in the Morro Grande Forest Reserve. The Morro Grande Forest Reserve represents one of the most significant remnants of forests on the Planalto Paulistano (Metzger et al. 2006), extending from the Serra do Mar to the city of Campinas. The collections of the small mammals took place in two localities of this reserve, one close to the Pedro Beicht Dam (23°42'56"S; 46°57'29"W) and Graça Dam (23°39'11"S; 46°57'58"W) between March 2013 and December 2015, during five days per month. All mites were collected and stored in 100% alcohol for further studies. Each host represented a collection event; thus, all collected mites were stored together to do the screening later.
The mites collected were sent to the Acarological Collection of Instituto Butantan (IBSP) to be slide-mounted and identified, following the preparations described by Barros-Battesti et al. (2021). For the chigger identification, we use the genera key made by Brennan & Goff (1977) and the original descriptions of all species described in the identified genera.
It is worth commenting that in all these collections, in addition to the chigger collections, ticks (Ixodida: Ixodidae), laelapid, and macronyssid mites (Mesostigmata: Lealapidae and Macronyssidae) were also collected.
During the field work, it was observed that the surroundings of the Morro Grande Forest Reserve are highly anthropogenic. The area receives considerable pressure due to the expansion of real estate and being constantly invaded for fishing and illegal hunting activities. The idea raised by Goff (1979) and Moniuszko et al. (2018) that coparasitism can happen due to anthropogenic pressure may be one of the causes of the present study.
On the other hand, a parasitic preference was observed, because each genus has been found in a different place on the host's body. The species of Quadraseta Brennan, 1970 were all found inside the host's ear. In contrast, Kymocta species were all intranasal, and T. bakeri was found parasitizing the ear edge region of the same hosts. In this way, it can be said that at least the co-parasitism observed in these hosts did not bring competition for space or food regarding genera competition. However, the Quadraseta species appear to compete among them, which was found up to three different species in one same host's ear. New studies must be carried out, and the co-parasitism reported. In this way, we can begin to understand the population dynamics and patterns of parasitism related to chiggers.