Cyclopodia greeffi, Karsch, 1884

Atobatele, Oluwatosin Ebenezer, Olatubi, Iyabo Victoria, Oyeku, Oyeshina Gideon, Ayokunle, Damilare Iyinkristi, Oladosu, Oladipo Olarinre & Ogunnaike, Tolulope Mary, 2023, Analysis of COI gene, prevalence, and intensity of the bat fly Cyclopodia greeffi on roosting straw-coloured fruit bat Eidolon helvum in Southwest Nigeria, International Journal for Parasitology: Parasites and Wildlife 21, pp. 210-218 : 215-216

4.1. Bat host of Cyclopodia greeffi

Our study shows a significant female to male sex ratio of 0.22:1 (male bias) for the straw-coloured fruit bat roosting in Bowen University. High male to female sex ratios have been reported for several species of Myotis and Epstesicus fuscus ( Adams and Hayes, 2018; Patriquin et al., 2019; Piksa, 2008); migratory noctule bat, Nyctalus noctula ( Petit et al., 2001) ; and common vampire bats, Desmodus rotundus ( Delpietro et al., 2017) . The strong male bias may suggest strong sexual segregation and formation of bachelor E. helvum groups for this roosting location. Bachelor roosts have been reported for other fruit bats such as Rousettus aegyptiacus ( Kwiecinski and Griffiths, 1999) and Pteropus mariannus mariannus ( Wiles, 1987) .

C. greeffi infests the tree-roosting fruit bat, Eidolon helvum as seen in this study although double infestation by ectoparasites (tick and insect) has been reported for E. helvum ( Samabide and Lenga, 2018) , where in addition to Cyclopodia , it was infested by the ixodid tick of the genus Antricola . In this study however, E. helvum was parasitized solely by C. greeffi which is similar to the findings from northern Nigerian towns in Bauchi, Benue, Nasarawa and Plateau States ( Kamani et al., 2014, 2022) and Southwest Nigerian town of Ife in Osun State ( Otubanjo, 1985). Monoxenous species parasitize only one host species ( Olival et al., 2013). Cyclopodia greeffi and other nycteribiid bat flies exhibit host specificity. It is likely that C. greeffi is a specialist ectoparasite, being strictly monoxenous on the tree-roosting E. helvum .

4.2. Morphological characteristics of bat ectoparasites

The morphological features of the bat ectoparasites isolated in this study match with earlier reports by Theodor and Urich et al., ( Theodor, 1957, 1959; Urich et al., 1922). C. greeffi differs from other closely related species of Cyclopodia based on size, the number of blunt teeth of the thoracic and abdominal ctenidia, number of spines on the abdominal plates and characteristics of the genitalia.

4.3. Molecular phylogenetic analysis of bat flies

As observed in the phylogenetic tree, the COI gene fragment sequences of C. greeffi from this study (southwest Nigeria) and those from northern Nigeria ( Kamani et al., 2022) formed a single clade, and were clearly differentiated from those of other genera and related species with strong support values, hence, supporting its previous delineation as a species based on morphological features. Similarly, the clearly defined clusters formed by sequences of individual nycteribiid species, e.g., C. dubia , C. horsfieldi , E. theodori , Nycteribia sp. , N. pleuralis and N. allotopa , supports their taxonomic description and the findings from other phylogenetic studies ( Olival et al., 2013; Ramasindrazana et al., 2017).

4.4. Prevalence, infestation intensity and sex ratio of bat ectoparasites

The overall prevalence of 58.9% recorded for C. greeffi during this study is higher than 46.51% reported for the straw-coloured fruit bat from Brazzaville, Congo ( Samabide and Lenga, 2018). However, the mean intensity of 2.3 ± 0.2 individuals for this study is lower than the 2.8 C. greeffi recorded from Brazzaville, Congo ( Samabide and Lenga, 2018) for the straw-coloured fruit bat. An estimated average 1.79 nycteribiids is reported to parasitize Myotis daubentonii and Megaderma lyra bat hosts ( Tendu et al., 2022). Large number of ectoparasites reported for a female E. helvum weighing 220g (Jim´enez and Hazevoet, 2010) supports the broader range of ectoparasitic infestation (0–14 C. greeffi ) recorded during this study as compared to the lower and narrower range (0–4 C. greeffi ) per fruit bat reported earlier from Ife, Nigeria ( Otubanjo, 1985). This study shows no significant difference in intensity of infestation between the sexes. Non-significant sexual differences in nycteribiid infestation of fruit bats was reported for two species of Rousettus and Thoopterus nigrescens in Indonesia ( Nangoy et al., 2021). The significantly higher intensity of infestation and the wider spread of ectoparasitic infestation during the wet season is supported by the report of Otubanjo (1985), who recorded peak infestation abundance from July to September. However, in contrast to the latter author who did not record any infestation during dry season (January to March), this study recorded C. greeffi infestation throughout the period, although with a lower infestation intensity of 1.6 ± 0.1 individuals per fruit bat. C. greeffi recorded no significant difference in sex abundance with a female to male sex ratio of 0.88:1, suggesting a balanced ectoparasitic metapopulation adult sex ratio. Szentiv´anyi et al. (2017) emphasized the importance of host and parasite sex ratio in better understanding host-parasite interactions. Reasons adduced for biased sex ratios include selective host grooming ( Dick and Patterson, 2008), and parasite behaviour and sex-dependent mortality ( Dittmar et al., 2011). This study shows no significant relationship between sex of C. greeffi infestation and host sex on one hand and between sex of C. greeffi infestation and season on the other hand. Barbier et al. (2019) opines that the ectoparasitic load of bat flies on bats is less correlated with environmental factors such as amount of rainfall and vegetation, however, Zarazúa-Carbajal et al. (2016) hinted that seasonality affect bat fly species richness.

The social habit of Eidolon helvum , implies close contact of individuals roosting together; and would suggest a higher prevalence of infestation by bat flies. The prevalence recorded for this study could be higher if some bat flies escaped during capture while the fruit bat was entangled in the mist net prior to removal into cloth bags; and also due to behavioural adaptation to reduce or eliminate bat fly transmission through auto- and allo-grooming activities ( Ramanantsalama et al., 2018; Tendu et al., 2022).

The low regression coefficient (R 2) between ectoparasite intensity and fruit bat body mass indicates that the body mass of E. helvum has no apparent influence on intensity of C. greeffi infestation. Variations of ectoparasitic prevalence and intensity in bat hosts have been reported to be mediated by behaviour, sex and age ( Webber et al., 2015); roost group size, grooming efficiency and energy budgets ( Czenze and Broders, 2011) in a highly gregarious mammals of the genus Myotis . Ramanantsalama et al. (2018) reported similarity in the grooming rates for both sexes of the endemic Madagascan fruit bat, Rousettus madagascariensis . Reports show that ectoparasitic load has no apparent effect on bat’ s health ( Sharifi et al., 2013).