Morphology of third instar Boettcherisca highlandica Kurahashi & Tan, 2009 (Diptera: Sarcophagidae)

2015·5.7 MB·

by  C C Heo

ISSN0973-1555(Print)ISSN2348-7372(Online) HALTERES,Volume6,121-131,2015
©Heo,C.C.,Latif,B.,Silahuddin,S.A.andKurahashi,H.
&
Morphology ofthird instar Boetteherisca highlandica Kurahashi Tan,
2009 (Diptera: Sarcophagidae)
*Heo, C.C.1’2 Latif, B.1 Silahuddin, S.A 1 and Kurahashi, H3
, , . .
facultyofMedicine, UniversitiTeknologiMARA, JalanHospital,47000 SungaiBuluh,
Selangor, Malaysia.
instituteofForensic Science (IFS), UniversitiTeknologiMARA, Level4, AcademicBuilding,
FacultyofMedicine, 47000 SungaiBuluh, Selangor, Malaysia,
internationalDepartmentofDipterology, Hikawadai 1-2-21, HigashikurumeCity, Tokyo203-
0004, Japan.
(e-mail: *[email protected])
Abstract
Five species ofBoetteherisca havebeen recordedhitherto inMalaysia. The presentstudy demonstrates that
Boetteherisca highlandica Kurahashi & Tan could be playing a role in forensic investigations as the larvae
were recovered froma rabbit carcass placed at Cameron Highlands, peninsular Malaysia. The third instar
morphology ofB.highlandicais describedforthefirsttime. Thelarvallength rangedfrom 17-18 mm, with
the anterior spiracle composed of28-30 papillae arranged in two irregular rows. The posterior spiracle is
large, heavily pigmented with dilated tails at the upper and lower end of peritreme. Morphological
differences ofthird instar and adults between B. peregrina and B. highlandica are highlighted, and keys to
differentiatespeciesofSarcophagidaeofforensicimportanceareprovidedherein.
Keywords: Boetteherisca highlandica, Sarcophagidae, third instar, forensic entomology, Cameron
Highlands,Malaysia.
Received:28September2015;Revised:15October2015;Online&Published:5November2015.
Introduction
The literature on the species richness Iranihindiamartellata (Senior-White, 1924)was
andbiogeography ofSarcophagidaeinMalaysia documented as a new locality record for
is relatively scarce compared to other dipteran peninsularMalaysia(Tanetal.,2010a).
families such as Calliphoridae. Sugiyama et al. The genus Boetteherisca was
(1990) described six new species of established by Rohdendorf in 1937 where he
sarcophaginefliesfromMalaysiaandSingapore. designated Myophora peregrina Robineau-
Twelve years later, a taxonomic key of the Desvoidy, 1830 as type species. Lopes (1961)
oriental Sarcophagidae was provided by listed seven species inthe checklistincluding B.
Kurahashi (2002), where several new species septentrionalis Rohdendorf; B. formosensis
wereadded. In2007, Kurahashi&Lehlistedthe Kiener & Lopes; B. nathani Lopes; B. javanica
species of Diptera collected in Sarawak, East Lopes, B. peregrina (Robineau-Desvoidy); B.
Malaysia and documented 21 species of karnyi (Hardy) and B. atypica (Baranov). The
Sarcophagidae, along with a new species phylogeny ofBoetteherisca can be divided into
described, Parasarcophaga omari Kurahashi & two monophyletic and one paraphyletic group,
Leh, 2007. Itwasthenfollowedby Kurahashi & namely peregrina-group, septentrionalis-group
Tan (2009) who published a checklist on the and karnyi-group, respectively. Based on the
sarcophagid flies from peninsular Malaysia cladogram analysis and geographic distribution,
whichcomprisedtwo subfamilies, 20generaand the genus Boetteherisca is postulated to have a
45 species. Soon after that, a sarcophagid, Sundalandorigin(Kurahashi&Kano, 1984).
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Heo,C.C.,Latif,B.,Silahuddin,S.A.andKurahashi,H.
Recently, a total of 17 species of been recovered from dead common Indian toad
Boettcherisca were recorded by Xue et al. (Bufo melanostictus) (Das & Dasgupta, 1986).
(2011), wheremostofthe species aredistributed Furthermore, adults have been reared from
in Oriental region. The oriental species include candlebush (Cassia alata L.)(=Senna alata (L.)
B. bengalensis Nandi; B. cabrerai Kano & Roxburgh) andon“rotting shells” (Lopes, 1961).
Sugiyama;B. dumoga Sugiyama&Kurahashi;B. Thelarvaecanbeparasitesofsugarcaneloopper,
highlandica; B. javanica; B. koimani Kano & Mocis frugalis (Fabricius) (Mungomery, 1947),
Shinonaga; B. krathonmai (Pape & Banzinger); earthworms, and locust, Chortoicetes
B. nepalensis Kano & Sugiyama; B. talomensis terminefera (Walker) and act as facultative
Magpayo & Kano; B. timorensis Kano & predators of lepidopteran pupae of nymphalid
Shinonaga; and B. yuwanensis (Sugiyama). The andpyralid (Xueetal.,2011).
remaining six species of Boettcherisca have a Previous studies demonstrated that B.
wider geographical distribution viz., B. peregrina breeds on human and animal remains
formosensis (Palaearctic, Oriental); B. invaria (Sukontason et al., 2010) and served as an
(Walker)(= atypica Baranov) (Oriental, causative agent in various kind ofmyiases such
Australasian/Oceanian); B. karnyi (Oriental, as ophthalmomyiasis (Miura et al., 2005),
Australasian/Oceanian); B. nathani (Palaearctic, otomyiasis (Chigusa, 1994), cutaneous myiasis
Oriental); B. peregrina (Palaearctic, Oriental, (Kani et al., 1981), nasal myiasis (Kamimura &
Australasian/Oceanian, Madagascar); and B. Arakawa, 1986),intestinalmyiasis (Hasegawaet
septentrionalis(Palaearctic,Oriental). al., 1992), urogenital myiasis (Jiang, 2002),
In peninsular Malaysia, five species of vaginal myiasis (Chigusa et al., 2005) and
Boettcherisca have been previously recorded. urethral myiasis (Sun & Ren, 1995).
These included B. peregrina, B. karnyi, B. Furthermore, this species was reported in
javanica, B. krathonmai and B. highlandica hospital-acquired myiasis (Uni et al., 2006). In
(Kurahashi & Tan, 2009). However, only four forensic entomological studies, Early & Goff
species were documented in Sarawak (1986)recoveredthelarvaeofB.peregrinafrom
(Malaysian Borneo), with no record of B. the exposed carrion on the island of Oahu,
highlandica (Kurahashi&Leh,2007). Hawaiian islands, USA, as well as on human
ThebiologyofB. peregrina isrelatively remains found indoor in Hawaii (Frost et al.,
welldocumented. Theadultflies ofB. peregrina 2010). Besides, the larvae ofB. peregrina have
are extensively distributed in eusynantrophic as been used in entomotoxicology studies to
well as the semisynanthropic and asynanthropic determine the effect of drug substances on its
zones on human feces especiallyin latrine areas developmetalrates (Goffetal., 1989; Goffetal.,
(Feng et al., 1990). The adult flies feed on 1991). Fromthemedicalperspectives, the adults
garbage, corpses, feces, flowers andfallen fruits havebeenincriminatedasmechanicalvectors of
(Xue et al., 2011). The larvae of B. peregrina etiological pathogens of diseases acquired from
can be found in a wide variety ofdecomposing decaying animal matter and human feces
organic matter such as carrion, dung, garbage (Moribayashi et al., 2001). In molecular
and human feces (Hall & Bohart, 1948; Lopes, taxonomy, molecular profiles of forensically
1961), including dead giant African snail, important flesh flies (which include
Achatina fulica Bowdich (Senior-White et al., Boettcherisca spp.) in Malaysia have been
1940, as Sarcophaga fuscicauda Boettcher). studied thoroughly by Tan et al. (2010b).
However, dead snails are probably not the Besides,thebasiclifecycleandlifehistoryofB.
primary breeding site for B. peregrina. peregrina have been investigated by several
AccordingtoBeaver (1986), B. peregrina rarely researchers (Nishida et al., 1986; Majumder et
A
breeds on fulica in Thailand, andinthree out al., 2012), including a study on its
of five experiments in Malaysia, but only in a developmental rate under different temperature
single snailin each experiment. Thenumbers of conditions (Wangetal.,2010).
individuals bred per snail varied from 1-6, and However, there is little information on
adults emerged from 15-19 days after exposure the biology and ecology of B. highlandica. The
ofthe snails. Other than snails, the larvae have type localities of B. highlandica were Genting
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MorphologyofthirdinstarBoetteheriscahighlandicaKurahashi&Tan,2009
Highlands andCameronHighlands (bothlocated segmentwithoutseparatingitintotwoparts.The
in peninsular Malaysia) and this species excised larvae were placed in 10% potassium
appeared to be only present at high elevations hydroxide (KOH) for clearing purposes.
(i.e., above 1,200 m a.s.l.) (Kurahashi & Tan, Immersion in KOH was continued overnight.
2009). In this study, we had a chance to collect The next day, they were placed in 10% acetic
and examine several B. highlandica larvae acid for five minutes to neutralize the KOH
obtained from a rabbit carcass placed in solution. Forceps, pins and a half-shaved
Cameron Highlands. The third instar wooden stick were used to aid in removing the
morphology of B. highlandica is herein gut contents of the larvae. The larvae were
describedforthefirsttime. placed through a series of ascending
concentrations of alcohol solutions from 70%,
MaterialsandMethods 90%, 95% and absolute alcohol for 30 minutes
A field experiment was conducted at each. They were then placed in xylene for 7
m
CameronHighlands (4.49N, 101.39E, 1,517.3 minutes and in clove oil for 30 minutes for
a.s.l.). Observations and insect collections were colouring purpose. Lastly, the larvae were
carried out for 22 days continuously. A total of placedonglass slides andmountedwith Canada
fiverainswererecordedduringthe studyperiod, Balsam and kept in an oven for drying process.
with mean temperature and relative humidity The slides were labeled and observed under a
23.56 ± 4.04°C and 81.73 ± 21.56%, compound stereoscope (Olympus BX53, Japan)
respectively. A rabbit (Oryctolagus cuniculus with a standardized measurement bar according
(L.)), weighted approximately 2.0 kg, was to the respective magnifications. The pinned
euthanized by phenobarbital overdose and then adult specimenandlarval slides were vouchered
placed on the ground atthe study site on Day 1 in the parasitology laboratory, Faculty of
(initial day of study). The carcass was then Medicine,UniversitiTeknologiMARA.
surrounded by protective fence to prevent
scavengingactivitiesbyvertebrates. ResultsandDiscussions
Three third instar larvae from a same The first sarcophagidthatarrivedonthe
maggotmass were collectedbeneaththe carcass rabbit carcass was Parasarcophaga albiceps
on the last day of observation (on day-22 (Meigen) anditwasobservedonthethirddayof
postmortem). Two of them were preserved in decomposition. Two days later, a male and a
70% ethanol immediately on-site and the other femaleB.highlandicawerenotedonthecarcass,
onewas allowedtogrowbyfeedingitwithbeef indicating a temporal delay in this species to
liver and brought back to the laboratory for locate ephemeral resources (Table 1). Adults of
rearing purposes. The food source (i.e., beef B. highlandica were sighted continuously until
liver) was added ad-libidum until the post- day-13 of decomposition. On the other hand,
feeding stage, andthenthelarvawas transferred Parasarcophaga taenionota (Wiedemann) was
to a dry container for pupation. The resulted also recovered at the later stage of
adultfly was thenkilledbyusingEther, pinned, decomposition.However,neitherP. albicepsnor
and kept in the oven for desiccation over four P. taenionota larviposited on rabbit carcass,
days. The dried specimen was subsequently although the adults were seen frequently on the
labeled and sent to the last author for species carrion. The complete faunal successional data
confirmation. onrabbitcarcassesatCameronHighlands canbe
The preserved larvae were observed retrievedfromSilahuddinetal. (2015).
microscopically and the body length was We did not record the date and time of
measuredbyanordinaryrulerunderadissecting the initial larvipositionby B. highlandica onthe
microscope (Olympus SZX10, Japan). Larval rabbit carcass, the developmental time fromegg
mouthparts, anterior spiracles, posterior tolarvastagecouldnotbepreciselydetermined.
spiracles and other morphological features were However, the duration needed from initial
then prepared by using slide mounting methods pupation stage to emergence ofadult was noted
modified from Lee et al. (2004) as follows: a under a well-controlled laboratory condition
transverse excision was made at eleventh body witha recorded pupariationtime. Thepupawas
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Heo,C.C.,Latif,B.,Silahuddin,S.A.andKurahashi,H.
formed on 3.II.2012 and the adult emerged on andwhollypigmented. Posteriorspiracle: large
20.11.2012. Hence the pupal duration was 18 and heavily pigmented; peritreme incomplete
days (-432 hours) under the laboratory with well developed inner slit projections;
condition (23.7 ± 0.17°C, 83.6 ± 1.82% RH, 10 button absent; spiracular slits slender and long;
h light: 14 h dark cycle). This preliminary data distance between both posterior spiracles is
was based on a single emerged adult, therefore approximately % width of spiracle; tails of the
the duration of pupal stage might vary as there upperandlowerendofperitremedilated(Figs. 1
was no replication. It is necessary to study the and2).
complete development duration of B. Comparative remarks. Since both B.
highlandica as this species could have peregrina and B. highlandica are carrion
ecological implications and forensic value breeders, we provide taxonomic keys adapted
especiallyintheecoregionofmontaneforest. from Sukontason et al. (2010) to distinguish
Description: third instar B. highlandica these species and prevent misidentification in
(n=2). General: length from 17-18 mm, body the future. We hereby highlighted some
slender-shaped, creamy white in color. morphological differences betweenB. peregrina
Cephalopharyngeal skeleton: medium sized and B. highlandica larvae (Table 2) and adult
and heavily pigmented; basal piece of mouth stage (Table 3). The differences in their
hook rectangular, hook part short, stout and bionomicsarealsocomparedinTable4.
pointed downward slightly; ventral cornua We hope the information provided in
approximately half length of dorsal cornua; this paper could be useful to forensic
anterodorsal processes inapparent. Anterior communities where B. highlandica could
papillae: arranged in two rows with 28-30 potentially serve as a forensic indicator in the
papillae. Bodyspination: each segmentcovered determination ofminimum postmortem interval
by spinations; the spine is of single spike and the location of body recovery.
(unicuspid), long, slender, sharp pointed at tip
Table 1. SuccessionofSarcophagidaeonarabbitcarcassplacedatCameronHighlands,
Malaysia
Speciesrecovered Adultsightedon Larvalrecoveredfrom
rabbitcarcass
Parasarcophaga albiceps
(Meigen) Day3 No
Boettcherisca highlandica
Kurahashi &Tan Day5-13 Yes (larvaecollectedon
Day-22postmortem)
Parasarcophaga taenionota
(Wiedemann) Day 12-18 No
124
MorphologyofthirdinstarBoettcheriscahighlandicaKurahashi&Tan,2009
Table2.LarvalmorphologybetweenB.peregrinaandB.highlandica
Keyfeaturesof Boettcheriscaperegrina Boettcheriscahighlandica
thirdinstarlarva (adaptedfromSukontason
etal.,2010)
Cephalopharyngeal Apparentanterodorsal Inapparentanterodorsal
skeleton processes processes
Anteriorspiracle Arrangedintworows with Arrangedintworows with28-
24-26papillae 30papillae
Bodyspination The spineis ofsingle spike, Thespineis ofsingle spike,
long, slender, sharppointedat long, slender, sharppointedat
tip andwhollypigmented tip andwhollypigmented
Posteriorspiracle Tailoftheupperendof Tails oftheupperandlower
peritremeis dilated ends ofperitremearedilated
mm mm
Lengthofthirdinstar 17 17-18
larva
Table3.AdultmorphologybetweenB.peregrinaandB.highlandica
Keyfeaturesoftheadult Boettcheriscaperegrina Boettcheriscahighlandica
(adaptedfrom (adaptedfromKurahashi
Sukontasonetak,2010) & Tan,2009)
mm mm
Bodylength 10-12 10-12
Gena Black Black
Thirdantennasegment Black Black
Palpus Blackordarkbrown Black
Postsuturalac Present Present
Abdomen Greypollinosityatleaston Goldenyellowpollinosity
tergite4-5 inmale atleastontergite4-5
Epandrium Brown, occasionally Reddishbrown
blackishorreddish
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Heo,C.C.,Latif,B.,Silahuddin,S.A.andKurahashi,H.
Table4.NaturalhistorybetweenB.peregrinaandB.highlandica
Significantnatural Boetteheriscaperegrina Boetteheriscahighlandica
history
Medicalandforensic Bothmyiasis andforensic Nomyiasis orforensiccase
importance caseswerereportedfrom yettobereportedfrom
humanandanimalcarcasses humancorpses. Thelarvae
wererecoveredfromanimal
carcass athighelevation,
indicatingitspotentialrolein
decompositionatthe
highland
Habitat Lowland (highestaltitude Highlands withmontane
m m
recordedwas 1,300 a.s.l.) forestmorethan 1,200
(Xueetal., 2011) secondary above sealevel
forest, ruralandurbansettling,
plantations
Geographicaldistribution PeninsularMalaysiaand PeninsularMalaysia
MalaysianBorneo, Singapore, (GentingHighlands and
Bangladesh, Bhutan, Laos, CameronHighlands)
Myanmar, Nepal, Vietnam,
Cambodia, Thailand,
Indonesia, Japan, China,
Taiwan, NorthKorea, South
Korea, India, SriLanka,
Seychelles, NewGuinea, New
Britain, FrenchPolynesia, Fiji,
Samoa, VolcanoIsland, Bonin
Island, GilbertIsland, Guam,
Kiribati, HawaiiandMariana
Island, PapuaNewGuinea,
Australia, NewZealand
(Kurahashi&Kano, 1984;Xue
etal., 2011)
Ecology Synantrophic andwidely Asynantrophic. Larvaebreed
distributed. Larvaeare oncarrionathighelevation
necrophagous andadults are
coprophilous (Heo etal., 2010)
126
MorphologyofthirdinstarBoettcheriscahighlandicaKurahashi&Tan,2009
Fig. 1.MicroscopicmorphologyofthirdinstarB.highlandica. A, Cephalopharyngeal
skeleton. B,Anteriorspiraclewith28-30papillaearrangedintwoirregularrows. C,Body
spineswithsinglespike(unicuspid). D,Leftposteriorspiracle. Peritremewithdilated
upperandlowerends (arrows)
30pm 167pm 200pm
Fig. 2. Internal structures ofthirdinstarB. highlandica. A, Cephalopharyngeal skeleton. B,
Anteriorspiracle. C,Leftposteriorspiracle
127
Heo,C.C.,Latif,B.,Silahuddin,S.A.andKurahashi,H.
Fig. 3.Alarandthoracicsquamae.A,Boettcheriscaperegrina. B,Boettcherisca
highlandica. Circleshowedlowermarginofalarsquama. Arrow showedbaseofalar
squama
Fig.4.Lateralviewofhead. A,Boettcheriscaperegrina, genaclothedwithyellowishhairs
posteriorly. B,Boettcheriscahighlandica,genaclothedwithblackhairs. Circleshowedthe
genaregion
Key to adult sarcophagids of forensic 3. Innerlowermarginofalarsquamaandouter
importanceinMalaysia lowermarginofthoracic squamawithtuftof
palewhitehairs (Fig. 3A); genaclothedwith
1. Propleuronbare 2 yellowishhairsposteriorly(Fig. 4A)
- Proplueronhairy 3 Boettcherisca peregrina
2. Third antennal segment largely orange; (Robineau-Desvoidy)
palpus wholly orange; epandrium orange; Innerlowermarginofalarsquamaandouter
postsuturalacabsent lowermarginofthoracic squamawithtuftof
LiopygiaruficomisFabricius fuscous black hairs (Fig. 3B); gena clothed
- Thirdantennal segmentlargelyfuscousblack; withblackhairs (Fig.4B)
palpuswhollydarkbrown;epandriumbrown; Boettcherisca highlandica
postsutural ac present Kurahashi&Tan
Parasarcophaga (Liosarcophaga) dux
Thomson
128
MorphologyofthirdinstarBoettcheriscahighlandicaKurahashi&Tan,2009
Key to third instar of sarcophagids of Japanese Journal of Sanitary Zoology45:
forensic importance inMalaysia (parts ofthe 153-157.
key were adapted from Sukontason et al., Chigusa, Y., Shinonaga, S., Honda, M., Kanma,
2010) W., Kakinuma, H., Kirinoki, M. and
Matsuda, H. 2005. Vaginal myiasis due to
1. Marginal papillae of anterior spiracle Sarcophaga peregrina (Diptera:
arrangedinoneregularrow, composedof11- Sarcophagidae) on a patient with atrial
17papillae 2 fibrillation, cerebral infarction and leg
- Marginal papillae of anterior spiracle amputation.Medical Entomology and
arranged in two or more irregular rows; Zoology56(3): 247.
composedof24-30papillae 3 Das, S.K. and Dasgupta, B. 1986. Observation
2. Anterior spiracle with 11-15 papillae; inter- of certain stages of development of three
slitprojectiondistinct;lowerendofperitreme species of Sarcophaga (Sarcophagidae:
located near base of middle or upper Diptera) in laboratory condition in Calcutta,
slit LiopygiaruficomisFabricius India.Journal of Bengal Natural History
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Acknowledgements In: Current Concepts in Forensic
We would like to extend our gratitude to the Entomology. Netherlands: Springer. 93-108
reviewers who improve the content of this pp.
manuscript. Sincere thanks to Mr. Edward G. Goff, M.L., Brown, W.A., Hewadikaram, K.A.
A&M
Riley (Texas University) forproofreading andOmori, A.I. 1991. Effect of
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