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A species-level association in Pheidole Westwood (Hymenoptera: Formicidae) ants with a parasitoid wasp of the genus Orasema Cameron (Hymenoptera: Eucharitidae) in Brazil

Eucharitid wasps are exclusive parasitoids of ants and certain groups of eucharitids have specific associations with their hosts. This type of specificity is widely documented in more inclusive groups (subfamilies and/or genus-groups). However, we do not know if this specificity occurs in less inclusive groups (such as species or populations) or if it is more strongly influenced by local and/or regional environmental constraints. We provide a new association record between Pheidole gibba Mayr, 1887 and Orasema chunpi Burks, Heraty & Dominguez, 2018, while expanding their known distribution to the Brazilian state of Bahia. A R T I C L E I N F O Article history: Received 10 January 2020 Accepted 04 April 2020 Available online 15 May 2020 Associate Editor: Jeffrey Sosa-Calvo

Myrmicinae is the most speciose and widespread subfamily of ants; they comprehend circa 7000 described species (Bolton, 2020) -almost 50% of the total number of species for the family -occurring in almost all geographic regions in the globe (Baccaro et al., 2015). Members of the subfamily have a wide range of strategies for reproduction, nidification, and food acquisition (Baccaro et al., 2015). Among all ants, the myrmicine Pheidole Westwood is the most diverse ant genus, with 1,095 valid species (Bolton, 2020) of which their high levels of morphological variation may reflect numerous distinct feeding and nidification strategies (Wilson, 2003;Moreau, 2008). Due to their high diversity and ability to explore a variety of resources, Pheidole is a ubiquitous group of ants in almost every terrestrial ecosystem (Wilson, 2003;Economo et al., 2015). Its high-prevalence in natural and human-modified landscapes can be of extreme importance to explore drivers of host-parasitoid interactions.
Orasema Cameron is a chalcidoid wasp genus belonging to the ant-parasitoid Eucharitidae. The genus is restricted to the New World and is considered the most diverse group among the genera of Oraseminae (Burks et al., 2017), with 67 described species (Heraty, 2019). Species belonging to this genus are known parasitoids of Myrmicinae ants, with unverified records in Dorylinae and Formicinae (Heraty, 2002;Lachaud and Pérez-Lachaud, 2012).
In the initial stages of their life-cycles Orasema species have associations with plants, which serve as oviposition sites. It is believed that, apart from the specificity of eucharitid subfamilies towards their ant hosts, some species of these wasps chose specific groups of plants to oviposit whereas other choose particular plant structures irrespective of different plant groups (Baker et al., 2020). Hence, researchers often document associations between eucharitid parasitoids and their host plants (e.g. Varone et al., 2010;Torréns, 2013) to understand the mechanisms that enable these parasitoids to directly interact with their hosts and how they subsequently gain access to the ant nest.
Known associations between Orasema species and their Pheidole hosts are relatively scarce in the country. Only twenty-three Orasema species have been documented in association with ant hosts and, from those, only ten Pheidole hosts are unambiguously recognized to species level (Baker et al., 2020).
Specimens were collected at the Reserva Serra Bonita (Serra Bonita Reserve), at the Camacan municipality, state of Bahia, Brazil. This reserve is part of the Serra Bonita Reserve Complex, comprised by a group of four RPPNs (Private Reserve of Natural Heritage), administered by the Uiraçu Institute. It currently protects an area of 1800 ha, with expectations of expansion to 7500 ha of conserved area (Sanchez-Lalinde et al., 2011). The reserve complex is located between the cities of Camacan and Pau-Brasil, within the Atlantic Rainforest, characterized by high relative humidity and elevated temperatures, with the absence of a dry season (Köppen, 1936). The sampling event took place mid-July 2018, during winter. A nest of Pheidole gibba was found within an exposed tree trunk, approximately 40cm diameter in an intermediate state of decomposition, with moderate rigidity and low humidity. Several Pheidole specimens were collected and transferred to vials containing 90% ethanol. We used the identification keys provided by Burks et al. (2018) and Wilson (2003) to establish the specific identity of Orasema and Pheidole, respectively. All specimen observations and image acquisition were made at the Laboratory of Systematics and Ant Biology at the Universidade Federal do Paraná -Brazil and biological vouchers were deposited at Padre Jesus Santiago Moure Entomological Collection (DZUP) in the same institution.
Two specimens of Orasema chunpi (Fig. 1) were collected within the dead trunk that housed the colony of Pheidole gibba (Fig. 2). Both Orasema specimens were found inside the larval chamber, and it was not possible to identify additional specimens of the parasitoid.
One specimen of O. chunpi was identified on site as an obtect pupa, while the second as a newly-emerged adult, with some parts of the previous developmental stage still attached to its body (mainly mouthparts and apical half of the flagellum).
On-site, direct interaction performed by Pheidole workers towards the parasitoid specimens was not observed. There is few documented information on how immature stages of Orasema interacts with immature host ants within the nest (Wheeler, 1907;Vander Meer et al., 1989), with most records describing interactions between adult individuals from both groups, especially after pupal emergence of the wasp (Pérez- Lachaud et al., 2015).
According to Wilson (2003), P. gibba belongs to the tristis species group, which are known to occupy predominantly forest habitats, with some species being partly or wholly arboreal. Most species belonging to this group collect and store seeds, and, according to Wilson (2003), the major workers are commonly timid. However, in this occasion, P. gibba was moderately aggressive during the nest opening, with some major and minor workers acting aggressively towards the collector, while the remaining individuals escaped carrying the brood. There is no documentation on the biology of P. gibba Recently, Baker et al. (2020) summarized the strategies performed by Orasema parasitoids to reach their host's nests. Generally, the behavior is similar to other eucharitid genera, with the planidia interacting with a host plant to circumvent the colony's defenses and access the larval host through adult phoresis. In several Orasema species, however, it is believed that other arthropods (e.g. thrips and immature cicadellids) act as intermediate hosts (Wheeler and Wheeler, 1937;Clausen, 1940aClausen, , 1940bHeraty, 1994Heraty, , 2000, serving as transport to the planidia, being carried by scavenger or predaceous ants back to the nest, where they are placed in direct contact with the larval host (Heraty, 2000).
The present work expands the distribution of both species, providing more knowledge on their overall distribution range. It also sheds light on the specific association of two poorly known genera and their biology, providing insights on ant-eucharitid interactions at species-level.

Acknowledgments
We are indebted to Rodrigo Feitosa for providing the infrastructure to study and document specimens from both species. We would like to acknowledge Javier Torréns, Rodrigo Feitosa, two anonymous reviewers, and Jeffrey Sosa-Calvo for suggestions and recommendations in previous versions of this manuscript. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior -Brasil (CAPES) -Finance Code 001. TSRS was funded by CAPES and Fundação Araucária (process number 88887.354448/2019-00). ACF was funded by the Brazilian Council of Research and Scientific Development (CNPq, grant 140260/2016-1). The sampling event was funded by the Partnerships for Enhanced Engagement in Research (PEER) Science Program (NAS/USAID), through the project 3-188.

Conflicts of interest
The authors declare no conflicts of interest.

Compliance with ethical standards
The specimens were collected in accordance to national legislation and its regulatory resolutions, Lei nº 6.938/1981 (Política Nacional do Meio Ambiente) and Lei Complementar nº 140/2011, and the material is deposited in the Coleção Entomológica Padre Jesus Santiago Moure, Departamento de Zoologia da Univerdidade Federal do Paraná, as imposed by law.

Author contribution statement
TSRS and ACF designed the study, conducted species' identifications and obtained the high-resolution images. ACF collected the specimens and prepared the figure plates. TSRS and ACF wrote the first version of the manuscript. Both authors revised the manuscript and read and approved the final version.