Bizarre egg-clusters of Notoedres sp. mites (Acari: Sarcoptidae) on the wings of a cave-roosting molossid bat (Mammalia: Chiroptera) in Southeast Asia

Introduction

Bats (Chiroptera) became one of the most widely distributed groups of mammals on the planet, specifically due to the evolution of flight. The ability to fly enabled bats to occupy the most diverse roosts in various habitats like tree holes, foliage, and bird nests, but also caves, dens of larger mammals, and anthropogenic structures. In addition to this, the high physical agility of bats and their special morphological adaptations, such as wings without fur, led bat-associated Acari to evolve a range of morphological features in association with the life of their hosts and feeding on them. For example, bat ticks have relatively long legs and spinturnicid mites developed robust legs with dense setation and strong claws. The majority of bat-associated mites are obligate blood-feeding ectoparasites. Numerous species are scavengers of dead skin or hair follicles and several species are known as endoparasites that live within the skin or in the nostrils and mouth of bats (Baker and Craven Citation2003). The members of the family Sarcoptidae are well-known ectoparasites of many different bat species and a number of sarcoptid mite species have already been described for molossid bats in particular (Klompen Citation1992).

In this study, we report the presence of bizarre egg-clusters with a long stalk and the larvae of a sarcoptid mite species that were collected on a molossid bat in Thailand.

Materials and methods

In total, five egg-clusters were found on the ventral sides of the wings of a female wrinkle-lipped free-tailed bat, Chaerephon plicatus Buchanan, 1800 (formerly Tadarida plicata) during a study on the immunology of cave-roosting bats in Thailand (Wat Khao Wongkot bat-cave, approx. 160 km north of Bangkok, province Lop Buri; 15.018145°N, 100.545205°E; Weise et al. Citation2017). At the time, in early November 2015, females of the colony were mostly in the late-lactation stage with subadults capable of independent flight (Figure 1). Bats were caught and examined as part of the permit #0002/4508 granted by the National Research Council of Thailand (NRCT) and as part of the permit #108/59 granted by the Department of National Park, Wildlife and Plant Conservation (DNP) and were approved by the animal welfare and ethics committee of the Leibniz Institute for Zoo and Wildlife Research. Study animals were captured inside the cave by picking them from the walls of the cave. From 45 bats (20 males/25 females) that were examined, only one carried the parasite egg-clusters that are described here. Two egg-clusters were taken into 70% ethanol. Some photographs of the eggs were taken using a Keyence VHX5000 digital microscope. Later the specimens were placed into lactic acid, and the cleared mites were moved to permanent slides into Hoyer medium. For final identification, preserved specimens were investigated with the help of a Leica 1000 scientific microscope. All measurements are given in μm.

Figures 1–4. Notoedres egg-cluster. 1. Egg-clusters on wing of bat. 2. 2 Egg-cluster in small magnification. 3. Empty eggs within the cluster. 4. Eggs and larvae in and around of cluster

Display full size

Results

Notoedres sp.

Description of the egg-cluster (Figures 1–4)

Egg-cluster cylindrical, a little curved in middle, full length 1770–1950 and 350–490 wide, contained more than 250 eggs. Eggs oval, 115–130 long and 45–58 wide. Stalk 145–180 long and joint with wide apical part to the posterior part of eggs, straight, but in some case curved. Majority of eggs contained larvae, but more than half of them were empty. Eggs opened on apical margin.

Notes. Usually, the females of the Notoedres are visible at the centre of the cluster, half buried in the skin. No females were observed in the field and were not collected together with the eggs. Regarding the large size of the egg-cluster and the absence of the females, it is questionable, that the cluster was produced by one or more females.

Description of larvae(Figures 5–6)

Idiosoma oval, twice as long (ca 95–100) than wide (ca 50–53). Dorsal idisoma with predorsal and postdorsal shield-like structures. Anal opening in caudal position. All dorsal setae long and needle-like. Setae ve ca. 8–9, sce 17–19, sci 28–30, c1, c2, d1, d2, e1, e2, and h1 15–17. Striation between sce-sce transversal, between d1-h1 longitudinal. Ventral idiosoma with six pairs of needle-like setae, 1a apically curved and ca 21–22 long, 3a, 3c, and cp straight and 17–19 long. Coxal apodeme I Y-shaped and reach to 1/5 of 1a, apodemes II apically wider a little bifurcated, reach to 2/3 of 1a. Apodemes III narrow and long. Some longitudinal striae present on the lateral part of ventral idiosoma between apodemes II–III. Legs I–II with a rounded suction cup – like ambulacrum, leg III with a long (ca 78–82) apical seta.

Figures 5–6. The found Notoedres sp., larvae. 5. Dorsal view. 6. Ventral view

Display full size

Discussion

To date, the following 14 species of sarcoptid mites were found parasitizing molossid bats around the world: N. (B.) helicothrix Fain & Lukoschus, Citation1975; N. (B.) lasionycteris (Boyd & Bernstein, Citation1950); N. (N.) alexfaini Lavoipierre, Citation1968; N. (N.) cheiromeles Fain, Citation1959; N. (N.) elongatus Fain, Citation1963; N. (N.) rajamanickami Lavoipierre, Citation1968; N. (N.) yunkeri Fain, Citation1962; N. (N.) tadaridae Fain, Citation1959; N. (N.) tritis Fain & Marshall, Citation1977; and N. (N.) ovatus Dusbabek, Citation1980; in particular, N. (N.) dewitti Klompen, Lukoschus, Fain, & Nadchatram, Citation1983, and N. (N.) ismaili Klompen, Lukoschus, Fain, & Nadchatram, Citation1983 have been found on Chaerephon plicatus in Malaysia (Klompen Citation1992). Also, Ixodes kopsteini (Oudemans) parasitizes C. plicatus (Corpus-Raros & Lit Citation2015), yet no species of hard ticks were found on the bats examined during this study.

The idisoma of the larvae reported here is oblong and not rounded. There are two Notoedres species (N. (B.) helicothrix and N. (B.) lasionycteris) associated with molossid bats, where the larvae are oblong and not rounded. But the following differences are visible between these two species and the one presented here. Setae h1 are distinctly longer than the other opisthosomal setae in N. (B.) helicothrix, but these setae are the same in length in specimens of this study. On the other hand, setae sci of N. (B.) lasionycteris are short (ca 5 μm), in contrast to the long ones on our specimens.

Eggs have well-developed stalk in some of the species having rounded larval body within this genus (e.g. N. (N.) ismaili, N. (N.) tritis, N. (N.) dewitti, N. (N.) yunkeri, and N. (N.) tadaridae). Among these species, only N. (N.) ismaili, N. (N.) tritis, N. (N.) dewitti, and N. (N.) yunkeri have long (20 μm or longer) setae sci, similarly to those on the larvae presented here. However, (N.) dewitti and N. (N.) yunkeri also bear minute setae, which were not observed on our specimens. The seta d1 is shorter than d2 and rod-like in N. (N.) ismaili, but similar in shape and length on the larvae presented here. The posterior part of apodeme I is bifurcated and the dorsal shield is covered by oval pits in N. (N.) ismaili; on the contrary, apodeme I is not bifurcated and there are no pits on the dorsum of idiosoma of the larvae presented here.

Based on the latter characters, the specimens presented here either belong to an unknown Notoedres species or belong to a known species of which the larvae are not yet described. Because we did not find any adults on the investigated bats, we were not able to link the larvae to one of the previously described adults, and thus we cannot describe them as a new species. Therefore, we could describe them as “Notoedres sp.” only.

The location of the egg-clusters on the bats’ body, however, is paradoxical. The ventral side of the wings, in particular the forearms, is easy to clean by the bat itself. How the egg-clusters overcame daily grooming remains unexplained. At the same time, it is unclear why the egg-clusters were not found on other parts of the body, e.g. the dorsal tail membrane that is more protected from self-grooming.