Corresponding author: Michael W. Hastriter ( firstname.lastname@example.org )
Academic editor: Pavel Stoev
© 2017 Michael W. Hastriter, Kelly B. Miller, Gavin J. Svenson, Gavin J. Martin, Michael Whiting.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Hastriter MW, Miller KB, Svenson GJ, Martin GJ, Whiting MF (2017) New record of a phoretic flea associated with earwigs (Dermaptera, Arixeniidae) and a redescription of the bat flea Lagaropsylla signata (Siphonaptera, Ischnopsyllidae). ZooKeys 657: 67-79. https://doi.org/10.3897/zookeys.657.11095
Lagaropsylla signata (Wahlgren, 1903), previously known only from the Island of Java, Indonesia is redescribed and reported for the first time in Deer Cave, Gunung Mulu National Park, Sarawak, Malaysia (west coast of Borneo). Many were found clinging to the earwig Arixenia esau Jordan, 1909. A similar account of a phoretic flea (Lagaropsylla turba Smit, 1958) on the same species of cave-dwelling earwig has been reported in peninsular Malaysia in a well-documented association with the hairless naked bulldog bat, Cheiromeles torquatus Horsfield, 1824. The association of L. signata with A. esau is parallel to the evolution and co-existence with bats in Deer Cave just as in the case of L. turba, A. esau, and C. torquatus. The evidence suggests that L. turba and L. signata are obligate phoretic parasites whose survival depends on A. esau to access a bat host. Arixenia esau is reported for the first time in Deer Cave and the occurrence of L. signata on the island of Borneo represented a new record, previously being found only on the island of Java. Images of L. signata attached to A. esau are provided. Xeniaria jacobsoni (Burr, 1912), often associated with A. esau in other geographical areas, was not present in the material examined from Deer Cave. The natural history of the earwig genera Arixenia Jordan, 1909 and Xeniaria Maa, 1974 are discussed and summarized relative to their associations with phoretic fleas and their bat hosts.
Arixenia esau, Deer Cave, Gunung Mulu National Park, insect phoresy, Lagaropsylla turba, Xeniaria jacobsoni
Phoresy occurs in some insects and arachnids in which one species attaches to another species in a commensal relationship for the purpose of increasing their ability to disperse from one place to another. There is seldom a detrimental effect on the transporting host species. In some cases, attachment to another species is accidental, while others have evolved into vital components of their life history. Although there is an account of a bird flea attaching to a wasp (Rothschild & Clay, 1952), this was attributed to an accidental association of a wasp foraging on a flea-infested avian carcass. Lagaropsylla turba Smit, 1958 is the only documented species of flea that truly demonstrates phoretic behavior for which there was an association between a flea, another insect (A. esau Jordan, 1909), and a bat host (the naken bulldog bat Cheiromeles torquatus Horsfield, 1824). In this scenario, an earwig provides a vehicle for L. turba to come into contact with its only known host, C. torquatus. Nakakta & Maa (1974) provided a summary of the commensal forms of the dermapterid suborder Arixeniina and their associated molossid bat species. Important works cited by
Earwigs were collected from the floor of Deer Cave while conducting a general insect survey of Gunung Mulu National Park in October 2006 (04°01'18"N, 114°49'24"E) (KBM & GJS) and in January 2009 (04°02'32.8"N, 114°48'49.6"E) (GJS). Specimens were collected in the same location deep within the main gallery of the cave in the early evening. No earwigs were found in the entrance area and path through the first half of the cave, although mixed rock and guano piles were present. Approximately 1000 m and within sight of the “Garden of Eden doline” (a cave ceiling collapse that allows light to enter the main gallery), the path climbed an isolated, cone-shaped hill. Very few earwigs were present at the base of this hill, but numbers increased with elevation. The top of the hill, the observation path, and railings included earwigs. Thousands were present in October 2006 and only a few were present in January 2009. Individuals were observed actively walking, mating, and resting in small cracks. Males, females and nymphs were collected using forceps to overcome their strong grip on the surface of rocks, railings, and clothing. The greatest concentrations of individuals were at the highest points on the hilltop, which suggests a negative geotactic behavior. Individuals were not observed in the area around the base of the hill and nearby cave walls.
All specimens were collected into and stored in 95% ethanol and later examined in the laboratory. During microscopic examination, many fleas were noted attached to the earwigs. One species of earwig was present and the mouthparts and genitalia were dissected to facilitate and confirm our identification. Earwigs were photographed in ethanol with the aid of a Canon 6D DSLR camera and Visionary Digital Passport II imaging system. Image stacks were montaged with Zerene Stacker v.1.04. Fleas were mounted on microscope slides in accordance with procedures outlined by
Ceratopsylla signata Walgren, 1903, Banjuwangi, Java, 22 V 1899, Carl Aurivillius, Nyctinomus plicatus [= Chaerophon plicata (Buchanan, 1800)] [number or sex of specimens in type series not recorded] (Swedish National Museum, Stockholm, not examined).
Lagaropsylla signata (MH-905). 1 Overview of male 2 Overview of female (arrow indicates group of setae on S-II). Scale bars: 0.2 mm.
Lagaropsylla signata (MH-905). 3 Manubrium, basimere, and telomere, male 4 Terminal view of aedeagus, male 5 Sterna VIII and IX, male 6 Terminalia of female, illustrating T–VIII and S–VII. Scale bars: 0.1 mm (3, 4, 6), 0.2 mm (5).
Both sexes may be distinguished from all other species of Lagaropsylla by a narrow band separating the margin of the frons from a white area anterior to the frontal row of fine setae. This band is hardly wider than that of the marginal layer of the frons (Figs
Head. Frons evenly rounded with very thin band layered between margin and a broader white area caudad; caudal margin of white zone lined with a dozen small setae from oral angle to upper antennal fossa. Second genal tooth longer than first. Pre-oral tuber short and thick, only half the length of first genal tooth. Eye fused into upper heavily sclerotized margin of genal lobe, hardly discernible as distinct eye. Labial palpus of five short segments; sub-equal to length of maxillary palpus. Occipital area with dorsal incrassations (Figs
Thorax. Length of pronotum equal to height of pronotum; 18 sharp ctenidial spines (both sides) equal to length of pronotum. One dorsal incrassation in pronotum; two dorsal incrassations in meso- and metanota. Prosternosome with antero-ventral area expanded ventrad. Pleural rod fused in center of sclerotic dome. Mesosternum and mesoepimeron fused as one; with two tuberculiform sclerotizations at juncture of sternum and epimeron. Pleural ridge feebly developed; pleural arch lacking. Lateral metanotal area dorso-ventrally flattened. Metepimeron with 12 setae in male and 21 or 22 in female (Figs
Legs. Oblique suture of mesocoxa only indicated on ventral margin. Notch in metacoxa vestigial. All femora lacking lateral or mesal setation. Dorsal margin of all tibiae with six dorsal notches. Distitarsomeres each with five pairs of lateral plantar bristles; most proximal pair set onto plantar surface between second pair (Figs
Unmodified abdominal segments. Abdominal terga I–VII each with a dorsal incrassation. Main rows of setae on T-I–VI interrupted; one seta below level of each spiracle. Spiracles round. One long antesensilial bristle. Sternum II of male without lateral setae. Female S-II with lateral patch of 14 setae; some short and others long and slender (Fig.
Modified abdominal segments, male. Saddle of T-IX and manubrium forming an obtuse angle. Basimere more convex on ventral margin than dorsal margin. Basimere with two or three small setae along dorsal margin; two moderately stout setae at apex. Acetabulum of telomere placed approximately midway between base and apex of basimere. Telomere half the length of basimere; slightly angled at ventral apical third terminating as acute angle at apex. Telomere with five or six minute setae along ventral margin; one minute seta at apex and two minute setae on dorsal margin (Fig.
Modified abdominal segments, female. Tergum VIII with two small setae near spiracle VIII, three or four long lateral setae, and four or five mesal marginal setae (two stout, two or three fine). Sternum VIII tube-like without setae. Caudal margin of S-VII with broad, truncate lobe with slight concavity at middle; with vertical row of four setae. Anal stylet twice length of width; with two minute setae at base of two slender apical setae. Ventral apical seta not much longer than anal stylet; dorsal seta twice length of stylet (Fig.
Male average length: 1.6 mm (n =10), range: 1.4–1.8 mm. Female average length: 1.7 mm (n = 7), range: 1.5–1.9 mm.
Malaysia, Sarawak, Deer Cave, Gunung Mulu National Park, 2♂, 3♀ attached to A. esau, 15♂, 35♀ from bat guano, 6 X 2006, KBM. An additional 5♂ and 12♀ were removed from the bodies of five specimens of A. esau collected in January 2009 by GJS.
Arixenia esau is a robustly built, highly mobile earwig capable of transporting many fleas for significant distances (Fig.
10 Arixenia esau, female dorsal habitus, thought to be penultimate instar 11 Female Lagaropsylla signata attached to leg of female Arixenia esau. Scale bars: 10.0 mm (10); 1.0 mm (11).
Arixenia esau, Deer Cave, 162 m, Gunung Mulu National Park, 04°01'18"N, 114°49'24"E, Sarawak, Malaysia, 16 X 2006, KBM, (20 adult ♂, 45 adult ♀, 34 nymphs). Arixenia esau, Headquarters, 23 m, Gunung Mulu National Park, 04°02'32.8"N, 114°48'49.6"E, Sarawak Malaysia, 14–16, 21–25 I 2009, GJS, (2 adult ♂, 2 adult ♀, 5 nymphs).
Lagaropsylla signata was previously known only from the type series. Although the host was listed as Ch. plicata, no information of how the bat was collected (mist net), or its habitat (cave, open field, hollow tree, human dwelling, etc.) was provided. Banjuwangi, Java is only a general locality, since modern Banjuwangi is a sprawling metropolis at the eastern extreme of Java along the Straights of Bali. In our study, a total of 72 L. signata were collected from the bodies of A. esau (7♂, 15♀) and from bat guano on the cave floor (15♂, 35♀). Cheiromeles torquatus was not found in Deer Cave in our study. Evidence of its historical presence was documented by Cranbrook (2010) in Niah Cave from archaeological records from the Pleistocene (40,000 years ago). Niah cave is approximately 115 km from Deer Cave. The finding of both L. signata and L. turba on A. esau implies that they have both adopted the same phoretic vehicle to access a bat host. Such evidence suggests that C. torquatus is present in Deer Cave and may serve as the principle host for L. signata but the definitive bat host for L. signata is unknown.
Because of the association of A. esau (Fig.
Records of Arixeniina taxa reported on bats and/or their environs by geographical localities (listed fleas apply only to localities, see footnotes).
|Localities and fleas||Dermaptera species|
|Arixenia camura||Arixenia esau||Xeniaria bicornus||Xeniaria jacobsoni||Xeniaria truncata|
|Malaysia, Peninsular||Hollow Tree||Hollow Tree|
|Lagaropsylla mira**||C. torquatus||C. torquatus|
|Lagaropsylla turba†||Ch. plicata|
|C. parvidens||Ch. plicata|
|Sabah, Malaysia||C. torquatus|
|Lagaropsylla signata††||C. torquatus|
Cheiromeles torquatus is distributed in southern peninsular Thailand, Malaysia, the insular portions of Indonesia (Java, Sumatra, Borneo), and Palawan, Philippines (
Both L. turba and L. signata appear to require earwigs to transport them to a viable bat host that would otherwise be inaccessible. Such obligate phoretic behaviors requires additional studies, especially to elucidate the association of L. signata and its yet unknown bat host species.
We thank Michael Naegle for his phylogenetic work on Arixenia which directly led to the discovery of the phoretic fleas. Specimens were collected under permits from the Government of Malaysia; Economic Planning Unit of Malaysia, UPE: 40 ⁄200 ⁄19 SJ.1040 (permit ID no. 1389) and 40 ⁄200 ⁄19 ⁄1481 (permit ID no. 1933). We thank Brian Clark and Gunung Mulu National Park and staff; Fatimah Abang and the University of Malaysia Sarawak; Haji Ali Bin Yusop and Sarawak Forests Department; Lucy Chong, Sarawak Forestry Corporation and the State Government of Sarawak. We are also grateful to Glen D. Chilton and Terry D. Galloway for providing valuable suggestions to improve this paper. Portions of this project were funded with NSF Grants #DEB-1557114 (MFW), #DEB-0515924 (KBM), #DEB-0738179 (KBM), and #DEB-0845984 (KBM).