1

1ECTOPARASITES OF BATS FROM GOMANTONG FOREST RESERVE, SABAH,

2MALAYSIA.
3
4Nurul Najmaini*1, Ehsan Hadi1, Abdul Hamid Ahmad1 and Hairul Hafiz1
51Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah.
6
7ABSTRACT
8The study of ectoparasites and its association with bats was conducted in Gomantong Forest
9Reserve, Sabah, Malaysia on December 2007 and December 2008. There were 288 bats that belong
10to eleven species were captured. A total of 404 ectoparasites were collected from the infested bats
11consisting three groups of ectoparasites; bat flies, mites, and ticks. Only 389 ectoparasites could be
12identified at genus level and eight at family level; comprising nine unidentified ectoparasite species
13and a family (Bat flies: (1) Nycteribiinae sp., (2) Trichobiinae sp.; Ticks: (1) Dermacentor sp., (2)
14Ixodes sp., (3) Haemaphysalis sp.); Mites: (1) Meristaspis sp., (2) Spinturnix sp., (3) Ancystropus
15sp., (4) Laelaps sp., (5) Family Psoroptidae). Seven ectoparasites are still unidentified even to
16family level consist of five mites, a larva and an insect. The overall prevalence was 50.69% with
17highest infestation rate was seen in Myotis muricola, Rhinolophus creaghi and Rhinolophus
18arcuatus. Bat flies attributed the highest infestation compare to mites and ticks and the most
19preferable host for many kinds of ectoparasites were also Myotis muricola. Ectoparasites from the
20Nycteribiidae sp infected most of the host species, but the most dominant ectoparasites in terms of
21individual numbers were ectoparasites from the Trichobiinae sp. The relationships between
22parasitism and host are discussed.
23Keywords: Ectoparasite, bats, bat flies, mites, ticks
24
25

26INTRODUCTION
27Bat ectoparasite live on the outer surface of its host or in the roosting site. Most of them are evolved
28with small and flattened body, so that facilitated them to remain close to its host body. Current
29research described that there are 19 families of ectoparasite who feed on bats blood (Whittaker et al.
302007). Among them, Nycteribiidae and Streblidae are highly specialized ectoparasite and only
31associate with bats (Dick and Patterson, 2006).
32
33Host specificity is a phenomenon that associated with the degree of confinement of parasite to its
34host body. Generally, the host specificity reflects morphological, behavioural and physiological
35characteristics of the parasite and host. It may also include environmental conditions and the
36geographic range of host (Marshall, 1982).
37
38Early studies of bat flies showed that ectoparasite may have the ability of infesting many species
39many genera (heteroxenous) of bats (e.g Jobling, 1951; Theodor, 1957). However, the increasing
40knowledge of Nycteribidae and Streblidae reveal the contrast. Bat flies are nearly always confined
41to a single species or genus of host (Marshall, 1982). For instance, in Panama Wenzel et al. (1966)
42reported 71% of streblids only found in one host species. Current research in Paraguay also
43described 87% of 31 bat fly species are only associated with a single host species (Dick and
44Gettinger, 2005).
45
46These reports indeed showed the specificity of ectoparasite infested certain host. Yet, the small
47portions of heteroxenous ectoparasite were also indicated variability in specificity (terHofstede et
48al. 2004) and there are truly polyxenous bat flies, infesting two or more host genera. Therefore, the
49host specificity theory of bats ectoparasite remains contentious (Dick and Patterson, 2007). The host
50specificity could be defined as: 1) monoxenous, ectoparasites species are those found in strict

51association with a single host species; 2) oligoxenous, ecto species parasitize two or more species of
52a single host genus; and 3) polyxenous, ecto species parasitize species of two or more host genera
53(Dick and Patterson, 2007).
54
55In Bornean Tropics, researches on ectoparasite were carried out intensively this few years; on small
56mammals and dogs as hosts (Wells et al. 2011; Wells et al. 2012). However, little is known about
57the information of bats ectoparasite. The purpose of this study was to sample bat parasite at a forest
58reserve in lowland area of Sabah, Malaysia. This study was also designed to examine the pattern of
59host-ectoparasite association in the forest.
60
61MATERIALS AND METHODS
62The study was conducted at Gomantong Forest Reserve in the district of Sandakan, eastern part of
63Sabah. Gomantong Forest Reserve is situated in the Lower Kinabatangan floodplains and
64surrounded by oil palm estates. Most of topography are low hills and narrow alluviat flats. The main
65vegetation types are mixed dipterocarp forest, fresh water swamp forest and peat swamp forest.
66Rainfall was averaged 3000 mm to 3500 mm annually and the temperature range from 22C to 32C
67with humidity more than 65%. For centuries, this forest is famous with its intricate cave system
68called Gomantong Cave which contains valuable edible swiftlet nests. To maintain sustainable
69harvesting activity, the cave and 3297 ha of the surrounding area was gazetted as protected area of
70wildlife and managed by Sabah Wildlife Department.
71
72Bats were captured two times during December 2007 and December 2008. Each sampling activity
73last for five nights of trapping. Mist nets were used as trapping device at five locations within
74reserve area. Locations were set up based on the potential area that could be the flying pathway for
75bats, for example near cave entrance, trails, riparian area, fruit trees, and also the forest edge. The

76traps were manned around dusk and closed until about midnight and reopened during dawn until
77sunrise. After being removed from the nets, bats were placed in separate and clean cloth bags until
78inspected for ectoparasites. Bats were examined thoroughly on the whole body (wing membrane,
79tail, pelage and ear). All ectoparasites were removed from the host by brushing and screening the
80bats and the cloth bag with an intensive light source (Lucan, 2006) then placed in vials containing
8175% ethanol (Wilson and Wodzicki, 1977), using a separate vial for each bat as a preserved
82purpose. Bats were also identified to species, sex and reproductive status and weight was measured
83(Payne and Francis, 2005). All bats were release after the inspection.
84
85All ectoparasites were studied under compound microscope. Because most parasites are minute,
86some specimens were mounted into slide. In case of heavily sclerotized ectoparasites, specimens
87were punctured and soak in lactophenol, heated with high temperature, washed in three to four
88changes of water and mounted on slides in Hoyers medium. The specimens were then placed in an
89oven at no more than 45 0C for four days to a week. All other ectoparasites specimens were cleared
90using 70% alcohol and mounted on temporary slide for identification. Slides were heated over
91flame and leaved at room temperature for seven to ten days for the medium to dry. Parasitism
92parameters that were estimated included prevalence (percentage of infested bats) and mean intensity
93(mean number of ectoparasites per infested bat).
94
95RESULTS
96A total of 288 bats belonging to 11 species were captured during this study; captures consisting
97eight species of insectivorous bats and three frugivorous species. Five species had sample size <10
98and captures were dominated by three species which had >50 sample size (Hipposideros cervinus,
99Rhinolophus creaghi and Myotis muricola) (Table1). Suprisingly, only 50.69% captured bats
100(n=146) were infested by ectoparasites with only nine species harbored ectoparasites.

101No ectoparasites were found on Balionycteris maculata and Hipposideros dyacorum which were
102also captured in very low numbers (n=1)(Table 1). On the other aspect, Myotis muricola hosted
103almost all ectoparasites species in this study followed by Rhinolophus creaghi and Rhinolophus
104arcuatus (Table 1). These three species had the highest prevalence with Trichobiinae sp. and
105Nycteribiinae sp ranged from 37% to 92%.
106
107In total, 404 ectoparasites were collected from the infested bats consisting three groups of
108ectoparasites; bat flies, mites, and ticks. However, only 389 ectoparasites could be identified at
109genus level and eight at family level; comprising nine unidentified ectoparasite species and a family
110(Bat flies: (1) Nycteribiinae sp., (2) Trichobiinae sp.; Ticks: (1) Dermacentor sp., (2) Ixodes sp., (3)
111Haemaphysalis sp.); Mites: (1) Meristaspis sp., (2) Spinturnix sp., (3) Ancystropus sp., (4) Laelaps
112sp., (5) Family Psoroptidae). Seven ectoparasites could not be identified; consisting five mites, a
113larva and an insect (Table 2). It is possible that the unknown larva and insect specimens were not
114the parasites and they were accidentally been sampled from the bats. The bat fly species,
115Nycteribiinae sp. was found exclusively in fur while Trichobiinae sp. was found either on wing
116membrane or tail membrane. All mites species were also preferred the membrane area while ticks
117group preferred whiskers area (Table 1).
118
119Infection of ectoparasites were divided into single infection and multiple infection. Most bats were
120infected by a single or two species of ectoparasite. The single infections were mainly caused by
121Nycteribiinae sp. and Trichobiinae sp. and most of the double infection were also dominated by the
122combination of these bat fly species. The case of triple or quadriple infection were rare in this study
123(Table 3).
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125It is apparent that bat flies species (Nycteribiinae sp. and Trichobiinae sp.) were dominant
126ectoparasite in this study (Table 2). Nycteribiinae sp. was the most common species, occupying all
127nine infested bats species within 92 individual bats. However, in term of abundant Trichobiinae sp.
128was the highest with 181 individuals of ectoparasites although, this species only parasitized four
129bats species (Table 2). The highest mean intensity was also with Trichobiinae sp., averaged 3
130ectoparasites per infested bats (Table 2). Several other ectoparasites also recorded high mean
131intensity in this study (e.g Psoroptidae, Ixodes sp. and Ancystropus sp. on Myotis muricola;
132Meristaspis sp. on Cynopterus brachyotis) but the sample sizes of ectoparasites and hosts were too
133low to analyze.
134
135Six of ten ectoparasite species including family Psoroptidae was monoxenous. As table 2 shows, all
136monoxenous species parasitized only on a single bat from certain host species (mostly Myotis
137muricola). The numbers of monoxenous ectoparasites were also low, range from one to eight
138ectoparasites.

In contrast, the dominant ectoparasite species (Nyctribiinae sp., Trichobine sp.,

139Spirtunix sp. and Dermacentor sp.) were polyxenous and present relatively in large numbers (n>10).
140
141DISCUSSION
142Locating nearby tropics cave system, bats were expected to have high rate of infestation. However,
143the result of this study indicate only half of total captured bats were infected by ectoparasite. It is
144difficult to explain this result but, it might be related to time of host captures. Bats which were
145captured in dawn most likely lack of ectoparasite or had reduced number of ectoparasite because
146energy gained during foraging activity on previous night allow bats to groom intensively (Vaughan,
1471977; Swift, 1997). On the other hand, captured bats in dusk during emergence time were highly
148infested most probably due to day roost ectoparasite transmission and minimized grooming

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149activities (Kunz, 1982). Thus, when both results were combined, it appear that the infestation and
150the disinfection were evenly matched.
151
152This result also indicate that six host species were infested with more than one species of
153ectoparasite. This finding is consistent with Marshall (1982) which found 28 of bats species in
154Malaysia commonly infested with more than one species of ectoparasite. Interestingly, a single
155species in this study (Myotis muricola) host at least nine ectoparasite species, higher than previously
156recorded by Marshall (1982). Along Rhinolophus creaghi and Rhinolophus arcuatus, this species
157also had high level of prevalence with Trichobiine sp. and Nycteribiinae sp. It seems possible that
158these results are due to the form of the roost. Majority of the captured bats most likely roost in
159crowded populations in nearby cave. This condition favors the ectoparasites to gain high success in
160dispersal, as well as protection and the favorable conditions of humidity and temperature (Marshall,
1611981).
162
163Current study also shows that Nycteribiinae sp. was fur specific. This observation support past
164studies of other ncyteribiids. Marshall (1971) found Basilia hispida in Malaysia parasitized in
165furred region of Tylonycteris species. Similarly, three Basilia species of Nycteribiidae in Central
166America also buried in the bats fur (terHofstede et al. 2004). Nycteribiids morphology appear to
167be an adaptation to live in fur. Nycteribiidae possess several ctenidae or combs that facilitate host
168attachment; preventing the animal from being brushed backwards from the fur. It also move
169relatively well in any direction and agile which may allow them to evade host grooming, the
170greatest cause of mortality in adult bat flies (Dick and Patterson, 2006).
171Many previous studies illustrate that ectoparasite from Streblidae family feed on both membrane
172and furred area of its hosts (Dick and Patterson, 2006; terHofstede et al. 2004). However,
173observation of this study has been unable to find Trichobiinae sp on furred area. The reason for this

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174is not clear but it may have something to do with body specificity and the streblids movement
175behaviour. Many species of Streblidae occupy specific site on their hosts body but these sites may
176change with the season and with the roosting habits of its hosts (Marshall, 1982).
177
178Mites and ticks in this study only show relatively low infections. The mites in this study,
179(Spinturnicidae, Laelapidae, and Psoroptidae) were found scattered on the wing and tail membrane.
180Likewise, mite Spinturnix myoti also occurs exclusively on wing and tail membrane of Myotis
181myotis in Switzerland (Giorgi et al. 2001). Most likely, their small size and camouflage colour
182helped them to survive from being discarded. On the other hand, the occurences of the Ixodidae
183only on whiskers of its host in current study were unexpected. The reason for this was not clear but
184it might relate to host groomings avoidance.
185
186The current findings also demonstrate that almost every infested bat was infected by Nycteribiinae
187sp or Trichobiinae sp or combination of these two. Single type of infection clearly indicates the
188occurrence of intraspecific competition among Nycteribiidae sp and Trichobiinae sp. Interestingly,
189the mean intensitys result also indicate that Nycteribiinae sp were high territory defense with most
190cases found only one Nycteribiinae sp infected on one host. Meanwhile Trichobiinae sp in almost
191cases showed aggregation on one host. This result can be explained by the morphological factor of
192the ectoparasites. Trichobiinae sp in this study have wings and can fly and it can frequently moved
193from host to host, as long as there are many host. As for wingless ectoparasites, Nycteribiinae sp
194had to reduce competition and the presence of one Nycteribiinae sp on the host may make it
195difficult for other individuals to colonize. This mechanism keep the number of Nycteribiinae sp
196within tolerable limit for the host. In contrast, there was no interspecific competition occured
197between these two. This phenomena most likely was influenced by the factor of site specificity. The

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198Trichobiinae sp in this study only utilized wings and tails area while Nycteribiinae sp occupied
199furred area.
200
201Although low, interspecific competition did happened involving the streblids and mites as both
202ectoparasites have same preferred body area. The low infestations also happen in triple and
203quadriple infections cause by the same reason. A possible explanation for this might be the bats did
204not have enough energy for grooming activities and then increase the parasite populations which
205drive to the competition between the ectoparasites. According to Marshall (1982), intraspecific
206competitions caused by crowded population of ectoparasites were unlikely to occur except on
207unhealthy or injured bats.
208
209Past studies reveals that most ectoparasite especially bat flies confined to a single species of host
210(monoxenous) (Marshall, 1982). Despite that, the results of this study did not support the
211hypothesis. This inconsistency was not fully understood. To date, the host specificity influenced by
212complexity of the morphological, behavioural and physiological characteristics of the parasite and
213host. It may also reflect the environmental conditions and the geographic range of host (Marshall,
2141982).
215
216This result however needs to be interpreted with caution. Indeed, there are ectoparasites which truly
217polyxenous as described by Dick et al. (2003); Wenzel (1976) and Wenzel et al. (1966). However,
218this finding cant be extrapolated because of uncertainties over parasite taxonomy. Therefore,
219further research should be done to clarify the taxonomy of ectoparasites and identify the true host.
220
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223ACKNOWLEDGEMENTS
224I would like to thank Associate Professor Dr. Abdul Hamid Ahmad and Mr. Hairul Hafiz Mahsol for
225their supervising with the helpful comments to improve the expression of this work. I am also
226grateful to Dr. Mariana Ahamad and Dr. Ho Tze Ming from Institute Medical Research of Malaysia
227for their advice and guidance in identifying parasites. I owe a special debt of gratitude to Mr. Ehsan
228Hadi, Mr. Agos Atan, and Mr. Jesper Ong, for their valuable help in collecting specimens and
229describe the mammals. Not forget the undergraduate students of Conservation Biology; Jessica,
230Tracy, Ida and Hidayat for their remarkable commitments in the field and Sabah Wildlife
231Department for providing the accommodation during fieldworks.
232
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