Redescription of three pinworms of the genus Cephalobellus Cobb, 1920 (Nematoda: Oxyuridomorpha: Thelastomatidae) from scarab beetle grubs from Hungary

Syst Parasitol (2024) 101:21 https://doi.org/10.1007/s11230-023-10124-1 Redescription of three pinworms of the genus Cephalobellus Cobb, 1920 (Nematoda: Oxyuridomorpha: Thelastomatidae) from scarab beetle grubs from Hungary Luca Eszter Balog · Mohammed Ahmed Oleksandr Holovachov · Received: 11 September 2023 / Accepted: 2 November 2023 / Published online: 19 February 2024 © The Author(s) 2024 Abstract Larvae of European rose chafer Cetonia aurata (Linnaeus, 1758) and cockchafer Melolontha sp. beetles were collected in Hungary for parasitological study. Intestinal examination revealed the presence of three well-known thelastomatid nematodes belonging to the genus Cephalobellus Cobb, 1920. We report for the first-time Cephalobellus cuspidatum (Rudolphi, 1814) Leibersperger, 1960, C. osmodermae Leibersperger, 1960, and C. potosiae Leibersperger, 1960 in Hungary, all found in scarab beetle larvae. Due to incomplete original descriptions, a comprehensive redescription with detailed morphological data is presented. Additionally, an identification key for closely related Cephalobellus, Thelastoma and Severianoia species infesting scarab beetles worldwide is provided. Newly generated 18S and 28S L. E. Balog Doctoral School of Biology, Institute of Biology and Department of Systematic Zoology and Ecology, Eötvös Loránd University, Pázmány Péter sétány 1C, Budapest 1117, Hungary M. Ahmed · O. Holovachov (*) Department of Zoology, Swedish Museum of Natural History, Box 50007, 104 05 Stockholm, Sweden e-mail: M. Ahmed Department of Evolution, Ecology and Behaviour, Institute of Infection, Veterinary and Ecological Sciences, University of Liverpool, Liverpool L69 7AB, UK rDNA gene sequences of C. osmodermae place it as one of the early branches within Thelastomatidae. Introduction The family Thelastomatidae (Nematoda: Oxyuridomorpha: Thelastomatidae) proposed by Travassos in 1929 currently comprises 1 subfamily, 42 genera and 268 species (Hodda, 2022). Thelastomatid pinworms are obligate endosymbiotic nematodes that occur in the intestinal tract of the invertebrate host and feed on bacterial microbiomes. These species have a worldwide distribution, but their diversity and biology are poorly known. The classification of the genera within the family Thelastomatidae is generally based on morphology, with limited molecular support and likely not reflecting true evolutionary relationships. The current classification of Thelastomatidae categorizes it as a monophyletic group. However, the phylogenetic analyses of ribosomal genes suggest that this group is paraphyletic and poorly resolved (Carreno, 2014; Garduño Montes de Oca & Oceguera-Figueroa, 2020; Zhang et al, 2021) due to existence of many insufficiently known genera and species, along with significant gaps in molecular data. The genus Cephalobellus Cobb, 1920 is the second most species-rich, after Thelastoma Leidy, 1849, within the family Thelastomatidae. The first descriptions of thelastomatid pinworm from arthropods was Cephalobellus cuspidatum (Rudolphi, 1814) Vol.: (0123456789) 13 21 Page 2 of 21 Leibersperger, 1960, originally named Ascaris cuspidata Rudolphi, 1814. This species was isolated from the intestine of the rhinoceros beetle’s grub Oryctes nasicornis (Coleoptera: Scarabaeidae). To date, 34 different species from this genus have been described, isolated from the hindguts of beetle larvae (Coleoptera), crane fly larvae (Tipulidae), adult millipedes (Diplopoda), adult cockroaches (Blattaria), and adults and larvae of flies (Diptera) (Adamson & van Waerebeke, 1992; Camino & Reboredo, 2000, 2005; Jex et al., 2006b; Hodda, 2022). On the other hand, there is very little phylogenetic and ecological data available for these species, besides what was included in the original descriptions. No data about the co-infection of the same host and limited information about phylogenetic relationships of these species were available until now. The differences between the genera Cephalobellus and Thelastoma and the identification of species within each is a challenging task. Recent species descriptions within these genera primarily focus on interspecific differences within particular genera, and do not discuss similarities or differences between Cephalobellus and Thelastoma (Carreno, 2007; Carreno et al, 2018; Jex et al., 2006b; Orsini et al., 2018). With more species described the differences between Cephalobellus and Thelastoma became less clear. For example, Liebersperger (1960) proposed that a filiform tail is characteristic for the genus Thelastoma genus, while a non-filiform tail is typical for Cephalobellus. However, many species with long filiform tails have been reassigned to different genera from Thelastoma since Liebersperger’s original descriptions in 1960. Our attempt to build the identification key revealed that some described species cannot be clearly delineated from each other based on morphological characters and may possibly be synonymous, especially if they inhabit the same host. On the other hand, some species known from distantly related hosts (Diplopoda versus Scarabaeidae) have been synonimised in the literature (Liebersperger, 1960) without much scrutiny – it is not unlikely that these are morphologically similar but ecologically and genetically different cryptic species – a question that cannot be answered without in-depth analysis of their genomes and reproduction. All species redescribed here are known only from their original descriptions; there is no information on their geographic variability and no molecular Vol:. (1234567890) 13 Syst Parasitol (2024) 101:21 data as well. Furthermore, thorough morphological redescriptions of species, accompanied with details on host specificity and geographic distribution, will clarify the systematics and biology of these common but insufficiently studied parasites. Moreover, several species of the genus Severianoia (Schwenk, 1926) Travassos, 1929 are found in scarab beetle larvae and are morphologically similar to Cephalobellus and Thelastoma – they were also included in the key, Certain scarab beetles (Coleoptera: Scarabaeoidea) can be significant threats as agricultural pests, emphasizing the economic importance of studying and examining their parasites (Huiting et al., 2006). However, the knowledge about the nematode parasites associated with these scarab beetles, including members of the family Thelastomatoidea, is still limited. It is noteworthy that no thelastomatid pinworms have been identified in Hungary at species level before (Balog et al., 2022a, 2022b; Balog & Török, 2019). This study presents both ecological data on the co-infection and the redescriptions of three species found in scarab grubs in Hungary: Cephalobellus cuspidatum, C. osmodermae Leibersperger, 1960 and C. potosiae Leibersperger, 1960 using light and scanning electron microscopy. The relationships between closely related genera Cephalobellus, Thelastoma and Severianoia are discuss (...truncated)