Acta Tropica. Ultrastructural studies of some character of Diptera (Muscidae) of forensically importance

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1 Acta Tropica 142 (2015) Contents lists available at ScienceDirect Acta Tropica jo u r n al homep age: Ultrastructural studies of some character of Diptera (Muscidae) of forensically importance César Carriç o a,b,, Paloma Martins Mendonç a a,c, Lucas Barbosa Cortinhas a,d, Jacenir Reis dos Santos Mallet a, Margareth Maria de Carvalho Queiroz a a Laboratório de Transmissores de Leishmanioses, Setor de Entomologia Médica e Forense, Instituto Oswaldo Cruz, Fundaç ão Oswaldo Cruz, Rio de Janeiro, RJ, Brazil b Doutorando do Programa de Pós-graduaç ão em Biologia Animal Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro, RJ, Brazil c Doutoranda do Programa de Pós-graduaç ão em Ciências Veterinárias Universidade Federal Rural do Rio de Janeiro, Rio de Janeiro, RJ, Brazil d Mestrando do Programa de Pós-Graduaç ão em Biodiversidade e Saúde Instituto Oswaldo Cruz, Fundaç ão Oswaldo Cruz, Rio de Janeiro, RJ, Brazil a r t i c l e i n f o Article history: Received 6 August 2014 Received in revised form 4 November 2014 Accepted 9 November 2014 Available online 14 November 2014 Keywords: Flies Forensic entomology Insecta Morphology Scanning electron microscopy a b s t r a c t Insects are important in the decomposition of cadavers. In the field of forensic entomology, the taxonomic identification is essential to proceed to any procedure. The use of these insects in medico criminal investigation is the object of forensic entomological studies; the flies are generally attracted to cadavers and one of the most important contributions is to estimate the postmortem interval. The scanning electron microscopy, which allows rapid and accurate identification of character could be used to help identify different species of forensics flies, has been highlighted as it allows better visualization of the external morphology of immature and some adults. The aim of this study was to describe the katepisternals in females of Morellia humeralis and Biopyrellia bipuncta; the ommatidia of the compounds eyes of the male of B. bipuncta; the antennae of females of Ophyra aenescens and Ophyra albuquerquei and the ocellar triangle of the last two species and O. chalcogaster examined by scanning electron microscopy to help increase the anatomical database on flies for forensic importance. The katepisternals of M. humeralis and B. bipuncta were densely covered by different groups of sensilla. The surface of the ocellar region of O. aenescens was not covered by sensilla, but in O. albuquerquei and O. chalcogaster were densely covered by different types of sensilla. The coeloconic sensilla were only found in the flagellum of O. albuquerquei Elsevier B.V. All rights reserved. 1. Introduction Forensic entomology is a tool used by justice system which makes use of insects as criminal evidence, not only in estimating the post mortem interval, but also in cases in which displacement of the body, neglect of children, elderly or disabled; use of chemicals and the route of narcotics have been noticed (Benecke, 2001; Benecke and Lessig, 2001; Benecke et al., 2004; Introna et al., 1998; Okiwelu et al., 2008). Groups of insects which show great potential for forensic information belong to the Diptera order, especially Calliphoridae, Muscidae and Sarcophagidae families (Archer, 2003). These families are mostly associated with decaying meat or corpses (Carvalho and Mello-Patiu, 2009). The Muscidae is a large cosmopolitan family, Corresponding author at: Instituto Oswaldo Cruz/Fundaç ão Oswaldo Cruz, Entomologia Medica e Forense, Av. Brasil, 4365, Manguinhos, Rio de Janeiro, RJ, Brazil. Tel.: addresses: carrico82@gmail.com, cesar.carrico@ioc.fiocruz.br (C. Carriç o). and some species are considered associated to human habitats in Brazil (Carvalho et al., 2002). Some species of Biopyrellia Townsend, 1932 and Morellia Robineau-Desvoidy, 1830 adults showed a strong attraction to human faeces and are considered potential vectors of pathogens to humans (Uribe-M et al., 2010; Carvalho et al., 2005). Ophyra Robineau-Desvody, 1830 adults can be floricultural or be attracted by substances in process of fermentation, decomposition and blood or wounds (Pamplona and Couri, 1989). The Ophyra species is a fly of medical and forensic importance in many parts of the world (Sukontason et al., 2007). The larvae were observed in human cadavers, carcasses of animals and others (Pamplona and Couri, 1989; Barbosa et al., 2009). The ultrastructure in adults flies have been the subject of many researchers, such as Stoffolano et al. (1988) who described, by using SEM, the abdominal plaques of both sexes of Tabanus nigrovittatus Macquart, 1847, Apiocera barri Cazier, 1982, Hydrophorus viridiflos (Walker, 1852) and Dolichopus consanguineous (Wheeler, 1899), revealing the presence of small pits, and the authors suggested that these cuticular plaques have a sensory function; Angioy et al. (1999) X/ 2014 Elsevier B.V. All rights reserved.

2 C. Carriç o et al. / Acta Tropica 142 (2015) confirmed in their ultrastructure study the different functional roles of the abdominal heart and the aorta of Protophormia terraenovae Robineau-Desvoidy, 1830; Sukontason et al. (2004) studied the antennal sensilla of some forensically important flies of the families Calliphoridae, Sarcophagidae and Muscidae, and they observed that the sensilla types were morphologically similar and suggested that each type of sensilla had a function. Sukontason et al. (2006) analyzed the ultrastructure of the adhesive device in flies of the following families: Calliphoridae, Muscidae and Sarcophagidae, and the results provided anatomical information about the successful attachment of theses flies to smooth surfaces as well as the role of these ultrastructure as a mechanical carrier of microorganisms; Sukontason et al. (2007) provided an extensive description of the sensilla on the antenna and palp of a fly specie of medical and forensic importance - Ophyra chalcogaster (Wiedemann, 1824), by using SEM to observe many structures which could not be clearly studied by making use of light microscopy: the chaetic sensilla, trichoidea sensilla and microtrichia, for instance. Zhang et al. (2013a) studied aspects of sensilla on the antenna and maxillary palps of Lispe neimongola Tian et Ma, 2000 and observed that the antennal scape had only chaetic sensilla, the pedicel had two subtypes and the funiculus had three types of sensilla (trichoidea, basiconic and chaetic sensilla). The structures selected in this study were those used in dichotomous keys which offered diagnostic characters, observable through light microscopy. The scanning electron microscopy was used in order to identify ultrastructure that might be responsible for the state of the characters. The purpose of our paper is to describe the ultrastructure of five flies belonging to the Muscidae family: first the katepisternal and humeral callus in adult females of Morellia humeralis (Stein, 1918) and the katepisternal Biopyrellia bipuncta (Wiedemann, 1830); second the male ommatidia the compounds eyes of B. bipuncta; third the antennae of females of Ophyra aenescens (Wiedemann, 1830) and Ophyra albuquerquei Lopes, 1985 and fourth the ocellar triangle of the last two species and O. chalcogaster examined by scanning electron microscopy to help increase the anatomical database on flies for forensic importance. 2. Material and methods The flies M. humeralis, B. bipuncta, O. aenescens, O. albuquerquei and O. chalcogaster were obtained from the Forensic Entomology Project regularly performed by our group. Two domestic pigs carcasses were used as a bait (Sus scrofa L.) and the collections were performed in January 2012, which were put in the West side of Rio de Janeiro, Parque Estadual da Pedra Branca PEPB (Pedra Branca State Park), (23 52 and S and and W), Brazil. The authorization for scientific research INEA (Instituto Estadual do Ambiente a State Environment Institute) is 043/2011. The traps model and the field protocols were the same as those proposed by Salviano (1996). The adults were daily collected, between 09 am and 2 pm and transported to Fundaç ão Oswaldo Cruz Fiocruz Oswaldo Cruz Foundation). In the laboratory, the collector tube was placed in a freezer at 17 C for 40 min. After freezing, the desired insects were transferred to test tubes. Ten specimens were placed on metallic supports, coated with thin layer gold (20 30 nm) and examined under JEOL 6390LV scanning electron microscope (SEM) (Akishima, Tokyo, Japan). It was not necessary any kind of fixing or drying, because of the natural chitin coverage of the specimens. The terminologies of adults flies used in this study followed McAlpine (1981), Carvalho and Couri (2002) and the classification of sensilla followed that of Setzu et al. (2011) and Zhang et al. (2013a,b). 3. Results 3.1. Morellia humeralis The specimens used were adults female. The humeral callus with four setae of similar shape, but which different size; the surface is covered by small setae (Fig. 1A). The analysis of katepisternals shows in the lateral view, a total of two larger setae in opposite sides, both have similarities in shape; one shorter setae with the same shape was noticed, located above the other two and the surface of the katepisternals is densely covered by two types of different groups of sensilla (Fig. 1B and C) Biopyrellia bipuncta The katepisternals in adults females, shows in the lateral view, a larger setae, and the surface of the katepisternals shave one type of scattered sensilla (Fig. 2A and B). The male of this specie shows the anterointernal ommatidia very enlarged and the lower third one with reduced ommatidia (Fig. 2C and D) Ophyra aenescens SEM observations of the ocellar triangle in females revealed that this is large and reaches the frontal structure with the end of the rounded tip (Fig. 3A). The surface of the ocellar region is not covered by sensilla and it has two long bristles, five medium ones and two small ones (Fig. 3B and C) Ophyra albuquerquei The ocellar triangle in the females of O. albuquerquei is slender does not reach the frontal one, tuned tip (Fig. 4A). The surface of the ocellar region is covered by sensilla and has two long bristles, nine medium ones and one small one (Fig. 4B and C) General shape of the antennae of O. aenescens and O. albuquerquei The ultrastructure of the head of both flies is equipped with a pair of antennae frontally situated, between the large compound eyes (Figs. 3A and 5A). Antennal morphology of two species consists of three segments: short proximal scape (Sc), pedicel (Pe) and a distal flagellum, the latter is composed of a seta called arista (Ar) located laterally and an enlarged basal funiculus (F) (Fig. 5B and C) Scape The Sc of O. albuquerquei have two types of sensilla, fourteen small chaetic sensilla (ChI) of similar length which were noticed arranged in a single row and trichoidea sensilla (Tr), were more numerous, densely and variable in length (Fig. 6A). However, the Sc of O. aenescens have approximately six chaetic sensilla (ChI), like the first one and arranged in a single row and trichoidea sensilla (Tr) variable in length (Fig. 6B). The cuticular surface of the Sc of both species is covered by small spinules of microtrichia (Mc) Pedicel The second antenna segment is called pedicel, in both species, and the surface is covered by short Mc. Besides, the Tr is similar to those found on the scape and it is also more numerous, densely and variable in length in O. albuquerquei than O. aenescens (Fig. 6B and A). Two morphological types of chaetic sensilla (small ChI and bigger ChII) are distributed on the pedicel, variable in length and shape in O. aenescens, and the ChII is similar to those found in the Sc (Fig. 6B). However, in O. albuquerquei, only ChI was noticed on the Pc, but more numerous and varying in length (Fig. 6A).

3 98 C. Carriç o et al. / Acta Tropica 142 (2015) Fig. 1. Scanning electron micrographs of adult female Morellia humeralis (Diptera: Muscidae). (A) Prothorax with the humeral callus composed of groups of setae (arrows) and the surface covered by small setae ( 100). (B) katepisternals in the lateral view with anterior and posterior bristle setae (arrows), and one shorter above the posterior bristle (arrow) and the surface of the katepisternals covered by two types of different group ( 200). (C) Detail of the anterior bristle (arrow) ( 100) Flagellum The distal flagellum is the largest segment of the antenna in both species and numerous sensilla are found in this segment. The segments of Ar of O. aenescens and O. albuquerquei are around covered by short Mc (Fig. 7A and B). In the enlarged basal Fn of O. aenescens three morphological types of sensilla are distributed on the entire surface Tr, two types of basiconic sensilla (BaI and BaII) and Mc (Fig. 7C) However, the Fn of O. albuquerquei has four Fig. 2. Scanning electron micrographs of adult of Biopyrellia bipuncta (Diptera: Muscidae). (A) Katepisternals of the adult female in the lateral view with posterior bristle ( 200) (arrows). (B) The surface of the katepisternals covered by one type of scattered sensilla and detail of the posterior bristle ( 100) (arrow). (C) Head of the adult male bearing pair of large compound eyes, eyes (E), antenna (A) and palp (P) ( 500). (D) Close-up view ommatidia of compound eye the adult male ( 100).

4 C. Carriç o et al. / Acta Tropica 142 (2015) Fig. 3. Scanning electron micrographs of features on the head of adult female of Ophyra aenescens (Diptera: Muscidae). (A) Head bearing pair of large compound eyes, eyes (E), ocellar triangle (OT) and antenna (A) ( 500). (B) The surface of the ocellar region with different types of bristles ( 100). (C) Close-up view of the ocellar region ( 50). morphological types of sensilla distributed on the entire surface. The different types are: basiconic sensilla, robust coeloconic sensilla, and the surface is densely covered by Tr and Mc (Fig. 7D) Ophyra chalcogaster The ocellar triangle in the females is short, not reaching the frontal suture (Fig. 8A). The surface of the ocellar region is covered by sensilla and has two long bristles and four small ones of different sizes (Fig. 8B). 4. Discussion The humeral callus of M. humeralis was selected for this study, since in the light microscopy we could observe a yellow coloration (Carvalho et al., 2002). It was supposed that this coloration was due Fig. 4. Scanning electron micrographs of features on the head of adult female of Ophyra albuquerquei (Diptera: Muscidae). (A) Head bearing pair of large compound eyes, eyes (E), ocellar triangle (OT) ( 500). (B) The surface of the ocellar region with sensilla and different types of bristles ( 100). (C) Close-up view of the ocellar region ( 100).

5 100 C. Carriç o et al. / Acta Tropica 142 (2015) Fig. 5. Scanning electron micrographs of features on the head of adult female of Ophyra aenescens and O. albuquerquei (Diptera: Muscidae). (A) Head of O. albuquerquei showing antennae (A) located centrally between large compound eyes (E) ( 200). (B) Antennal morphology of O. aenescens comprised of three antennal segments: scape (Sc), pedicel (Pc) and flagellum with arista (Ar) and Funiculus (F) ( 100). (C) Antennal morphology of O. albuquerquei comprised of three antennal segments: scape (Sc), pedicel (Pc) and flagellum with arista (Ar) and funiculus (F) ( 200). to the presence of small setae, but this was not observed by SEM. In addition, through the light microscopy, we observed only the presence of two bristles at the katepisternum of M. humeralis and small bristles covering the integument (Carvalho et al., 2002), but in this study we observed one short setae which had the same shape located above the posterior bristle. The katepisternum of B. bipuncta just had the posterior bristle setae (Carvalho et al., 2002). The same was observed in this study of ultrastructure. The integument of B. bipuncta had just one type of small bristle observed by SEM. The dipteran has a series of structures which serve as sensory organs in the head, with the compound eyes being the most preeminent of them (Sukontason et al., 2008). The distribution of ommatidia in the compound eyes of the male B. bipuncta had the anterointernal ommatidia very enlarged and the lower third one with reduced ommatidia which differs from those found in the fly of the Calliphoridae family, such as Calliphora vicina (Wunderer and Smola, 1982) with just the marginal ommatidia with distinct morphological from the others ommatidia, as well as with Musca domestica of the Muscidae family (Carlson and Chi, 1974). The sensilla in the antennae of the insects are important to find the opposition sex, food sources, orientation in shape and other aspects (Setzu et al., 2011; Zhang et al., 2013a). The external morphology of the different sensilla identified on the three antennal segments of O. aenescens and O. albuquerquei had similar characters of antennae described in many other flies species (Setzu et al., 2011; Sukontason et al., 2004; Sukontason et al., 2007; Zhang et al., 2013a,b). In the study of O. albuquerquei and O. aenescens antennae, four types of sensilla were distributed throughout the different antennae segments, but only microtrichia and trichoidea sensilla were observed in all of them. The chaetic sensilla were found only in the scape and pedicel of both species and basiconic sensilla was found just in the flagellum segment. These distributions are also found in the O. chalcogaster (Sukontason et al., 2007), however Fig. 6. Scanning electron micrographs of features on the scape and pedicel of adult female of Ophyra aenescens and O. albuquerquei (Diptera: Muscidae). (A) Cuticular surface of the scape and pedicel of O. albuquerquei with chaetic sensilla (ChI) and dense covering with trichoidea sensilla (Tr) ( 50). (B) Cuticular surface of the scape of O. aenescens with chaetic sensilla (ChI) and the pedicel with two types of chaetic sensilla (ChI and ChII), both segment covering with trichoidea sensilla (Tr) ( 50).

6 C. Carriç o et al. / Acta Tropica 142 (2015) Fig. 7. Scanning electron micrographs of features on the Flagellum of adult female of Ophyra aenescens and O. albuquerquei (Diptera: Muscidae). (A) The arista of O. aenescens displaying short microtrichia (Mc) on the distal end of the first and second segment and on the proximal half of the third segment ( 20). (B) The arista of O. albuquerquei displaying short microtrichia (Mc) on the distal end of the second segment and on the proximal half of the third segment ( 20). (C) Funicular (Fn) surface magnification of O. aenescens, Tr (trichoid sensilla), Mc (microtrichia), BaI and BaII (basiconic sensilla) ( 10). (D) Funicular (Fn) surface magnification of O. albuquerquei, Tr (trichoid sensilla), Mc (microtrichia), Ba (basiconic sensilla) and Cl (coeloconic sensilla) ( 10). in O. aenescens were not observed the coeloconic sensilla in the flagellum. According to Sukontason et al. (2004), the number of sensory sensilla on the flagellum varies in the different species; also, in this record we observed it. The flagellum was the largest segment of the antenna in both species, and microtrichia, trichoidea and basiconic sensilla were found in this segment and which resembled those described in other dipteran species, such as O. chalcogaster (Sukontason et al., 2007), M. domestica (Sukontason et al., 2004), Fannia scalaris and F. canicularis (Zhang et al., 2013b), Lispenei mongola (Zhang et al., 2013a) and P. terraenovae (Setzu et al., 2011). The morphology of the basiconic sensilla also resembled those described in other insects like the beetle Phoracantha semipunctata (Lopes et al., 2002). According to Setzu et al. (2011), the trichoidea, basiconic and other sensilla display a multiporous wall, indicating that de flagellum is a plain of olfactory organ and these organs permitted to detect chemical cues from the corpse decomposition (Greenberg and Kunich, 2002). Through light microscopy, it was possible to observe the dark coloration of the ocellar triangle of the Ophyra selected species in this study, and it was supposed that this coloration was due to the presence of small setae, which was not observed by SEM, but the distribution and variety amount of setae in each species studied were observed. In insects, there are usually three small ocelli forming an ocellar triangle on top of the head, the importance and function of the ocelli are to control the movement of flight and to record cyclic changes in light intensity (Gullan and Cranston, 2008). The vertex is the area in which ocelli is usually located, but in some insects the can be found in different positions on the head (Resh and Cardé, 2003). The position of the ocelli of O. aenescens, O. albuquerquei and O. chalcogaster was in the vertex as it is in the dipterans Calliphora vicina (Wunderer and Smola, 1982), Chrysomya pinguis (Sukontason et al., 2008), the Mecoptera Fig. 8. Scanning electron micrographs of features on the head of adult female of Ophyra chalcogaster (Diptera: Muscidae). (A) Head bearing pair of large compound eyes, eyes (E), ocellar triangle (OT) and antennae (A) ( 200). (B) The surface of the ocellar region with sensilla and different types of bristles ( 100).

7 102 C. Carriç o et al. / Acta Tropica 142 (2015) Sinopanorpa tincta and Bittacus planus (Wei and Hua, 2011), and in the cockroach Periplaneta americana (Weber and Renner, 1976). In O. albuquerquei and O. chalcogaster, the surface of the ocellar region was covered by sensilla, but in O. aenescens the ocellar region was not covered by sensilla, in this way, the ocellar ultrastructure differed greatly among groups of insects and it might have some phylogenetic implications in Hexapoda (Wei and Hua, 2011). In conclusion, this investigation shows that some diagnostics structures of the family Muscidae is only possible to observe with SEM. These results provide more anatomical information of adult flies to increase the database on flies for forensic importance. Acknowledgements We are grateful to Paulo Vander Ferreira Santana for his helpful reviewing of the manuscript. 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