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Article in Austral Entomology · November 2018 DOI: 10.1111/aen.12379

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Austral Entomology (2019) 58,638–645

Diets of animal origin and their influence on the development of the immatures of Chrysomya albiceps (Diptera: Calliphoridae): implications for forensic entomology

Mônica Salazar-Souza,1 Wellington Thadeu de Alcantara Azevedo,3 Márcia Souto Couri2 and Valéria Magalhães Aguiar1,3*

1Biomedical Institute, Post-graduate Program in Biological Sciences (Neotropical Biodiversity), Federal University of the State of Rio de Janeiro, Av. Pasteur, 458, Urca, Rio de Janeiro, RJ CEP 22.290-240, Brazil. 2Department of Entomology, Diptera Laboratory, National Museum/UFRJ, Quinta da Boa Vista, s/n., São Cristóvão, Rio de Janeiro, RJ 20940-040, Brazil. 3Biomedical Institute, Department of Microbiology and Parasitology, Federal University of the State of Rio de Janeiro, Rua Frei Caneca, 94-Centro, Rio de Janeiro, RJ CEP 20211-040, Brazil.

Abstract In forensic entomology, the minimum and maximum post-mortem interval (PMI) is estimated on the basis of the developmental stages of necrophagous Diptera larvae on a corpse. The nutritional composition of the decomposing tissue, which can influence larval development rates, may impact the precision of this estimate. We compared the post-embryonic development of Chrysomya albiceps reared on bovine muscle and swine lung. Forty newly hatched fly larvae, per treatment, were placed on 60 g of the following tissues: bovine muscle (control) and swine lung (T1). Each treatment had three replicates. The experiments were maintained under controlled conditions (28°C day/26°C night, 70 ± 10% RH and 12 h photophase). Flies reared on bovine muscle took significantly longer to complete their larval phase (8.1 days) than did larvae reared on swine lung (6.8 days). The total duration of development in bovine muscle was significantly slower (12.3 days) than in swine lung. Larvae that were reared on swine lungs were significantly heavier than larvae reared on bovine muscle. Total larval viability was high on pig lung (over 49%). The sex ratio was closer to the 1:1 ratio in bovine muscle (rs = 0.55), with a slightly greater proportion of female larvae. The percentage of abnormality remained within the predicted range. The results show that the different tissues influenced larval development. This underlines the importance of considering the type of cadaveric tissue when larval development is used to calculate the minimum PMI in forensic investigations. Key words forensic entomology, swine tissue, bovine tissue, post-mortem interval.

INTRODUCTION flies pioneer carcass colonisation. For this reason, they are very important to forensic entomology in the calculation of the Chrysomya albiceps (Wiedemann) is an exotic blowflyfromthe post-mortem interval (PMI) (Souza & Linhares, 1997; Old World tropics. Besides Africa, its current distribution Oliveira-Costa, 2000). Carvalho et al. (2004) observed adults includes South America, parts of Europe and Asia (Guimarães of the species colonising domestic pig (Sus scrofa domesticus et al., 1978; Al Shareef & Al-Qurashi, 2016). The synanthropic L.) carcasses immediately after being exposed in an urban area. and endophilic behaviour of these flies, which is associated with Their observations also confirmed the predominance of these a variety of substrates, may have contributed to their rapid flies throughout the decomposition process, which is possibly adaptation and dispersion (Gagné, 1981; Nespoli et al., 1998). associated with the predatory behaviour of their larvae of other In Brazil, the species is very important in public health as a in the corpse (Queiroz & Milward-de-Azevedo, 1991). mechanical vector of pathogens. These flies are attracted to Other studies in these regions have also documented C. albiceps rubbish dumps, blood, fresh or rotten flesh, and faeces, being larvae in human cadavers in both natural and urban areas also found in open markets. They cause in and (Salviano et al., 1996; Oliveira-Costa et al., 2001; Oliveira- humans (Zumpt, 1965; Linhares, 1981; Braack & Retief, 1986; Costa, 2005; Andrade et al., 2005). Nespoli et al., 1998; Ferraz et al., 2011a, 2011b). Chrysomya albiceps larvae can be used in PMI estimates to Studies on fly succession on carcasses in urban areas of the establish the minimum and maximum time of death based on Brazilian south-east and north have revealed that C. albiceps the age (developmental stage) of the larvae. They can also indi- cate possible post-mortem changes or injuries, cause and circum- stances of death, and aid in entomotoxicological investigations *[email protected] (Leccese, 2004; Oliveira-Costa, 2007).

© 2018 Australian Entomological Society doi: 10.1111/aen.12379 Development of the blowfly 639

Several studies have documented the development of cm) and were fed daily (ad libitum) a mixture containing 50% C. albiceps in the laboratory, some of which have employed honey, water and protein (bovine muscle). natural diets with different nutritional contents such as cow meat (Ullyett, 1950; Marckenko, 1985; Al-Misned et al., 2002; Grassberger et al., 2003; Kheirallah et al., 2007; Experimental phase Cordeiro, 2011; Al Shareef & Al-Qurashi, 2016), horse meat (Queiroz & Milward-de-Azevedo, 1991; Aguiar-Coelho & Female flies from the second laboratory generation were Milward-de-Azevedo, 1995; Queiroz, 1996) and rabbits stimulated to oviposit on 60 g of swine muscle. Immediately (Carvalho et al., 2012); and chickens (Richards et al., 2007). after hatching, first-instar larvae were individually transferred There have also been experiments with artificial diets (Estrada with a brush to separate diets of bovine and swine origins. et al., 2009; Ferraz et al., 2011a, 2011b). The frozen bovine and swine tissues used in this study were Pigs have been often used to establish the PMI based on purchased from two supermarket butcher shops from different larval development, because they are considered physiologically slaughterhouses, both meeting the safety standards for human similar to humans (Swindle et al., 1994; Mariano, 2003). consumption. However, not all swine tissues have been extensively Frozen tissue pieces of approximately 500 kg were thawed investigated as larval substrates in the laboratory. Larval for 17 h at room temperature, cut into 2 cm3 cubes and used development times can vary according to the kind of tissue, as according to the following ratio: 40 first-instar larvae/60 g of demonstrated by Beuter and Mendes (2013), who investigated tissue, bovine muscle (control) and swine lung (T1). Three the larval development of C. albiceps on swine fat, brain tissue replicates were used for each treatment, totalling 240 first-instar and meat. larvae. The proportion of diet used followed the ratio as In the course of forensic investigations, larvae collected recommended by Aguiar-Coelho et al. (1995) to rear from cadavers are kept under artificial conditions until the Calliphoridae. emergence of the adults, which are required for precise species The larval diets were packed in 100 mL polystyrene identifications. As larval development rates are important for containers and placed inside 400 mL polystyrene containers forensic entomology estimates, it is important to know how previously lined with sterilised wood shavings. The outer different substrates affect their developmental times. For container was covered with nylon fabric and fastened with example, Clark et al. (2006) observed that larvae of Lucilia elastic. The treatments were kept in a climate-controlled sericata (Meigen) (Diptera: Calliphoridae) developed faster chamber (biochemical oxygen demand) (Thelga/TF35A) at on swine compared with bovine tissues and on swine lung 28°C day/26°C night, 70 ± 10% RH, and 12 h photophase. compared with swine liver. Observations were conducted every 12 h. When third-instar Here, we evaluate the development of C. albiceps reared on larvae (L3) abandoned their diets, they were grouped in batches swine lung, using bovine muscle as a control, as the latter tissue of five in a Petri dish, and their body mass (in grams) was is commonly used to maintain colonies in the laboratory. The weighed on an analytical digital scale. The larvae were then resulting data can be used in forensic entomology estimates to transferred to tubes containing sterilised wood shavings, which evaluate the duration of post-embryonic development of larval were sealed with nylon and elastic fabric, and kept in a body mass gain and to evaluate the respective substrates to rear climate-controlled chamber until the emergence of the adults. C. albiceps flies in the laboratory. Daily observations were made to record the following: the time for post-embryonic larval development and the date of abandonment of mature larvae (L3) from the diet, body mass of the larvae at the time of abandonment, the time to pupation, MATERIALS AND METHODS the time to emergence of the adult flies, the physical appearance of adults (to examine for abnormalities) and the sex ratio of Collecting and establishing the stock colony the adults. Adult specimens of C. albiceps were captured using two aerial Microsoft Excel was used to analyse raw data, and further traps, made with modified 2 L polyethylene terephthalate analyses were conducted in the program R-Project®. Variations (PET) bottles as per Mello et al. (2007). Each trap was baited in the mean body mass of larvae, the duration of larval and pupal with 200 g of fresh sardines. stages and total development (from neolarvae to adult) were The traps were installed approximately 1.5 m above the analysed using the Shapiro–Wilk test to verify the normality ground in a tree, near garbage dumps (22°54020.9″S, between data and the Wilcoxon test for the comparison between 043°13045.8″W), at the Rio de Janeiro Zoo (RIOZOO), Brazil, the two tissues. The rates of larval abandonment, pupation and where they remained for 72 h. They were then taken to the emergence of adults were evaluated by the percentage compared laboratory for sorting and identification. with the number of days. The viability in the larval, pupal and The collected specimens were placed into a freezer for adult stages was evaluated by percentage. The sex ratio was approximately 2 min at 15°C to temporarily anaesthetise the obtained according to the formula rs = F/(F + M) (rs = sex ratio, flies. They were then identified with a stereomicroscope, using F = female, M = male) to compare it with the expected frequency the taxonomic key of Mello (2003). Chrysomya albiceps adults of 1:1 (male : female). Abnormalities were compared according were placed inside polypropylene cages (45 cm × 30 cm × 20 to the expected frequency (%). © 2018 Australian Entomological Society 640 M Salazar-Souza et al.

Table 1 Duration of the post-embryonic development stages and viabilities according to the expected frequency of larvae, pupae and adults of Chrysomya albiceps from bovine and swine tissues at 28°C day/26°C night, 70 ± 10% RH and 12 h of photophase

Treatments Days VI Viability (%) x±σ Larval phase Control 8.094a ± 0.1095 8.0–8.2 41.0 T1 6.834b ± 0.3321 6.5–7.1 49.0 Pupal phase Control 4.342a ± 0.4538 3.9–4.8 41.0 T1 4.258a ± 0.2409 4.1–4.4 49.0 Total duration Control 12.333a ± 0.3849 12.0–12.7 34.0 T1 11.072b ± 0.4744 10.8–11.2 48.0

Treatments: control (bovine muscle) and T1 (swine lung). The same letters indicate no statistical difference according to the Wilcoxon test. σ, standard deviation; VI, variation interval (minimum and maximum); x, mean number of days.

The mean duration of development (days) of the pupal stages showed no significant difference between the two treatments (P = 0.54) (Fig. 1), with the pupae of the two treatments developing on average in 4.3 days (Table 1). The total duration (first-instar larvae to the emergence of adults) of development (days) differed significantly between treatments (P < 0.001) (Fig. 1). Insects fed the control diet (bovine muscle) developed more slowly, taking an average of 12.3 days to complete their development, differing significantly from T1 (swine lung), where total development took on average 11.1 days (Table 1). The duration of developmental stages and the rate of abandonment of mature larvae from diet, pupation and emergence of C. albiceps adults raised in the pig lung and bovine muscle are shown in Figure 2. The peak of diet abandonment by larvae occurred on the sixth and eighth days in the control (bovine muscle) and on the sixth and seventh days in T1 (swine lung). The larvae began to abandon both diets on the fifth day. Although the total abandonment time was the same in both diets, the larvae presented different rhythms. In the control diet (bovine muscle), the larval began to abandon on the fifth day, with a small peak occurring between the sixth and eighth days of abandonment, while in T1 (swine lung), most of the larvae abandoned the diet between the fifth and sixth days, with a considerable decrease in abandonment observed on the seventh and eighth days. The data demonstrate that larval development in T1 (swine lung) was faster. Fig. 1. Duration (days) of larval and pupal development The pupation phase started on the sixth day in both and emergence time of Chrysomya albiceps adults from bovine treatments, extending until the 10th day in the control (bovine muscle (control) and swine lung (T1) at 28°C day/26°C night, 70 ± 10% RH and 12 h of photophase. muscle). However, even though the larvae had not completed the pupal phase within the same number of days, up to the eighth day, 99% of the larvae had pupated in T1 (swine lung), while in the same period, only 73% of the larvae in the control (bovine RESULTS muscle) had done so. Pupation peaks were observed on the sixth and seventh days in T1 (swine lung) and seventh and ninth day in The mean duration of development (days) of flylarvaewas the control (bovine muscle). significantly different between treatments (P < 0.001) (Fig. 1). The first adults emerged 10 days after the larvae were placed Insects reared on T1 (swine lung) developed faster on average on T1 (swine lung) and 11 days after they were placed on to the (6.8 days) did than insects reared on the control diet (bovine control diet (bovine muscle). The total emergence period muscle) (8.1 days) (Table 1). comprised 10 to 14 days. Emergence peaks were observed early © 2018 Australian Entomological Society Development of the blowfly 641

Fig. 2. Patterns of larval abandonment, pupation and emergence of Chrysomya albiceps adults from bovine muscle (control) and swine lung (T1), at 28°C day/26°C night, 70 ± 10% RH and 12 h of photophase, in relation to the number of days. on the 11th day in T1 (swine lung) compared with the 13th day greater (x = 90.9 mg) than the body mass of larvae reared in the control diet (bovine muscle). on the control diet (bovine muscle) (x = 69.6 mg) (Table 2). The emergence rate of male and female C. albiceps was similar in the control and T1. In T1 (swine lung), male and female adults started the emergency on the 10th day. All DISCUSSION female adults emerged until the 13th day, while the female adults extended the emergence time until the 13th day. In the control Studies with flies prove that feeding and temperature oscillations diet (bovine muscle), male and female adults emerged on the have an influence on developmental times. The larval stage is the 11th day, with female adults emerging until the 13th day, while decisive stage in obtaining food resources. The larvae exploit the male adults continued emerge until the 14th day (Fig. 3). substrate and compete to consume as much food as possible in The larval and pupal viabilities of insects on the control diet the shortest possible time before resources are depleted. The (bovine muscle) and T1 (swine lung) were between 41% and way female adults distribute the immature forms on to the 49%, respectively (Table 1). The sex ratio differed from the substrate influences the level of competition for food and space expected (ratio 1:1) on swine lung (T1) (rs = 0.92, F = 92.0%, between the immature forms (Levot et al., 1979; Ives, 1988). M = 8.0%; P < 0.001), remaining closer to the expected in the When numbers of larvae are high, competition exerts control (rs = 0.55, F = 55.0%, M = 45.0%; P < 0.001) influence on the quality and quantity of food ingested in the (Table 2). No abnormal insects were observed; that is, there were larval stage, resulting in variations in survival and larval no morphological deformities in any of the treatments. weight. This includes a lower viability of adults (due to food The average individual weight of mature larvae (g) differed stress), and morphologically, adults are smaller with lower significantly between treatments (P < 0.001) (Fig. 4). The fecundity or with fluctuating asymmetric variations (e.g. the body mass of larvae on T1 (swine lung) was significantly presence of small random differences between characters with © 2018 Australian Entomological Society 642 M Salazar-Souza et al.

Fig. 3. Rate of emergence, in days, of male and female Chrysomya albiceps fed on to bovine muscle (control) and swine lung (T1) as larvae, at 28°C day/26°C night, 70 ± 10% RH, and 12 h of photophase, in relation to the number of days.

Table 2 Individual weight (mg) of mature larvae and sex ratio of Chrysomya albiceps reared on swine and bovine tissues and sex ratio at controlled temperature of 28°C day/26°C night, 70 ± 10% RH and 12 h of photophase

Treatments Mean weight (individual) (mg) ± σ VI Sex ratio Control 69.6a ± 0.0031 67.0–73.0 0.55 T1 90.9b ± 0.0017 90.0–93.0 0.92

Treatments: control (bovine muscle) and T1 (swine muscle). Sex ratio calculated using the formula rs = F/(F + M). The same letters indicate no statistical difference according to the Wilcoxon test. σ, standard deviation; VI, variation interval (minimum and maximum).

bilateral distribution, such as the width of the thorax, wings or head) (Von Zuben et al., 2000; Reigada & Godoy, 2005; Vásquez & Liria, 2012). Despite efforts to develop alternative diets to rear flies, finding a low-cost diet with adequate nutritional content for Fig. 4. Average individual weight (g) of mature larvae of larval development in the laboratory has been challenging when Chrysomya albiceps adults from bovine muscle (control) and swine fl it comes to ies of forensic relevance (Estrada et al., 2009). lung (T1) at 28°C day/26°C night, 70 ± 10% RH and 12 h of Animal-based diets are the natural substrate of these necropha- photophase. gous insects and need to be employed. Furthermore, it is easy to add chemical substances for entomotoxicological studies to theses diets (Rabêlo et al., 2011). The results presented here weight gain (Ribeiro & Milward-de-Azevedo, 1997; confirm the suitability of swine and bovine meats as larval sub- Salazar-Souza et al., 2017). strates. However, when both tissues were compared, swine lung Previous studies have underlined the importance of the diet proved to be more suitable than bovine muscle. This is reflected used to establish and maintain the colony stock, and the possible in the faster development and greater body mass gain of insects influence of the maternal effect on nutrient intake (Ribeiro & reared on the former. This finding corroborates studies that ob- Milward-de-Azevedo, 1997; Barbosa et al., 2004). For the study served that the time of larval development and the rate of assim- herein, the flies that produced the larvae that were subsequently ilation of nutrients are factors that together influence larval evaluated in the two tissues were maintained on the same food © 2018 Australian Entomological Society Development of the blowfly 643 substrate as in the control (i.e. bovine muscle). Thus, it is are the origins and strain of the fly species used in the unlikely that the substrate influenced the results of the nutritional experiments (Aguiar-Coelho et al., 1995; Aguiar-Coelho & potential and results of the diets that were compared. Milward-de-Azevedo, 1995), and the environmental conditions The development of C. albiceps has been analysed in other employed in the study (Queiroz & Milward-de-Azevedo, 1991; trials using bovine and swine tissues as a larval substrate. The Aguiar-Coelho et al., 1995; Richards et al., 2007). results of the study herein differ from some of the previously Likewise, the consistency of the tissue may have been published data. Da Silva Mello et al. (2012), using ground influential in that the larvae reared on swine lung developed bovine meat (27 ± 1°C, 60 ± 10% RH and 12 h photophase), faster and larger. obtained a shorter development time for C. albiceps (5.7 days), Owing to the importance that C. albiceps has in forensic although the body mass of larvae was similar to that obtained investigations, it is essential to maintain stock colonies of this in the present study (70.0 mg). species in the laboratory. The results on the performance of both Estrada et al. (2009), using ground beef as a control diets highlight the potential of both, especially swine lung, as a (27 ± 1°C, 70 ± 10% RH and 12 h photophase), obtained a mean favourable diet for the maintenance of the larvae of this species. time of larval development of 5 days and body mass of the larvae Although the larvae reared on bovine muscle developed slower of 84.9 mg. In study herein, the mean larval weight was lower and had less mass, the viability of the larval, pupal and total than that observed in the bovine muscle (control) in the Estrada stages did not differ statistically from the results obtained with et al. (2009) study, with longer development time, and although swine lung. we observed the mean larval weight was higher in swine lung The fact that C. albiceps is used in the first wave of carcass (T1), the development time was longer. colonisation has been widely documented (Oliveira-Costa, Beuter and Mendes (2013) compared the development of lar- 2007). The species has been observed colonising rabbit carcasses vae on four different swine tissues, among which included in all stages of decomposition (fresh to dry) (Souza et al., 2005). ground meat (25 ± 1°C, 70 ± 10% RH and 12 h photophase). More experiments using swine and bovine tissues in different They obtained a shorter mean larval development time (5 days) stages of putrefaction need to be carried out to increase our and mature larvae that weighted more than observed in the knowledge on the development of this forensically important present study (62.5 mg). species. The differences in larval developmental times observed here The prevalence of female adults observed in both diets may are relevant for forensic entomology as this parameter is used have been influenced by the fact that female adults reproduce to calculate the min/max PMI. Norris (1965) emphasised that monogenically. The female adults originate only pure female the colonisation of different tissues and/or viscera may alter the prole (telegenic) or pure male progeny (arrenogenic) (Queiroz immature development times of scavenger insects. This et al., 1996). According to Ullerich (1963) and Queiroz (1991), reinforces the need to carry out studies in different geographic male adults cannot influence the sex of their descendants, and regions that present variations of humidity, heat or cold, with one generation may contain only male or female adults. different strains of C. albiceps, different tissues and varying The differences observed here in larval development rates on controlled environmental conditions. the different tissues may assist forensic entomologists when There are other factors that would need to be considered in larvae of C. albiceps are colonising cadavers or carcasses in PMI calculation. This includes the mechanical action of larvae estimating the min/max PMI. during feeding. The larvae need to penetrate the tissue, using vigorous movements of the head, and the buccal parts for scraping and maceration of the food, reducing the meat in pulp. The feeding does not occur through a passive act of suction ACKNOWLEDGEMENTS (Hobson, 1932). Another factor is the influence of microbial action, which We thank the Universidade Federal do Estado do Rio de Janeiro contributes to putrefaction and liquefaction of the flesh, and \UNIRIO, the Programa de Pós-Graduação em Ciências may be inhibited by the extra-digestive action resulting from Biológicas (Biodiversidade Neotropical)\UNIRIO and the proteolytic enzymes present in larval excretions, which digest Conselho Nacional de Desenvolvimento e Pesquisa (CNPq) for fi the structural parts of muscle tissue but are unfavourable to the nancial support and the Jardim Zoológico do Rio de Janeiro proliferation of bacteria in the corpse, delaying the process of (RIOZOO). decomposition, considering the amount of mass larva colonising the corpse (Hobson, 1932). 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