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Direct Injury, Myiasis, Forensics Insights on Funeral Practices and Insects Associated With the Tombs of King Ferrante II d’Aragona and Other Renaissance Nobles Augusto Loni,1 Antonio Fornaciari,2 Angelo Canale,1 Valentina Giuffra,2 Stefano Vanin,3 and Giovanni Benelli1,4 1Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124 Pisa, Italy, 2Division of Paleopathology, Department of Translational Research and of New Technologies in Medicine and Surgery, University of Pisa, Pisa, Italy, 3School of Applied Sciences, University of Huddersfield, Queensgate, HD1 3DH Huddersfield, United Kingdom, and4 Corresponding author, e-mail: giovanni.benelli@unipi.it Subject Editor: Michael Rust Received 11 April 2019; Editorial decision 23 May 2019 Abstract The impressive Sacristy of the Basilica of St. Domenico Maggiore contains 38 wooden sarcophagi with the bodies of 10 Aragonese princes and other Neapolitan nobles, who died in the 15th and 16th centuries. To im- prove the knowledge about the entomofauna associated with bodies in archaeological contexts, herein we pro- vide insights on the funerary practices and the insect community associated to Ferrante II King of Naples and other Italian Renaissance mummies of the Aragonese dynasty buried in the Basilica of St. Domenico Maggiore. We identified 842 insect specimens: 88% were Diptera (Muscidae, Fanniidae, and Phoridae), followed by 9% Lepidoptera (Tineidae) and 3% Coleoptera (Dermestidae and Ptinidae). Ninety-seven percent of the specimens were collected from the coffin of Francesco Ferdinando d’Avalos, which was the best preserved. A lack of fly species characterizing the first colonization waves of exposed bodies was noted. The most common fly was the later colonizing muscid Hydrotaea capensis (Wiedemann); only a few Fanniidae (Fannia spp.) were retrieved. The lack of blowflies, coupled with recording H.  capensis as the dominant fly, supports our hypothesis that corpses have been kept indoors for a long time under confined environmental conditions. Other explanations include odorous oils/balms having been used in the embalming process, causing the delay or stopping the arrival of first colonizer flies. Hermetically sealing of the coffin with bitumen may also have played a role in preventing access to the corpses. This scenario describes a historical context characterized by a well-advanced knowledge of body preparation, with specific burial techniques adopted for nobles. Key words: Phoridae, Muscidae, Hydrotaea capensis, Fanniidae, Italian Renaissance Archaeoentomology deals with the collection and analysis of arthropods remain in archaeological contexts. It derives from the tradition of Quaternary entomology, covering the study of insects and insect fossils embracing the last 2.5 million yr. Insect remains can give important information regarding sites of archaeological interest, involved by human activities. They can cover physical en- vironment, vegetation, human subsistence practices as well as hy- giene (Moret 1998, Green et al. 2019). A more specific field within archaeoentomology is represented by funerary archaeoentomology, which mainly focuses on tombs or other burials of archaeolog- ical or historical interest (Huchet 2014, Giordani et  al. 2018). Funerary archaeoentomology can be considered a discipline par- tially overlapped with classic archaeoentomology and forensic en- tomology, since both deal with the study of human cadavers. They share most of the methodology employed in collecting data, but they scopused to the obtaining of different goals (Vanin and Huchet 2017). In the case of funerary archaeoentomology the temporal dis- tance between the collection of the insects and the time of their active presence on the cadaver or on the substrate, can encompass centuries or even millennia (Handschin 1944, Wylie et  al. 1987, Germonpré and Leclercq 1994, Benelli et al. 2014). During this time, many hard- to-predict factors, including environmental ones, could strongly modify the preservation state of the insects. Furthermore, sampling methodologies could also affect the results of the collection. For this reason, data can be difficult to analyze focusing on their quantitative aspect. As a first consequence, all the collections of insect in archae- ological contexts represent an incomplete sample of the original set, not giving a full picture of the original scenario. However, especially applyparastyle "fig//caption/p[1]" parastyle "FigCapt" applyparastyle "fig" parastyle "Figure" Journal of Medical Entomology, XX(X), 2019, 1–8 doi: 10.1093/jme/tjz102 Research D ow nloaded from https://academ ic.oup.com /jm e/advance-article-abstract/doi/10.1093/jm e/tjz102/5528168 by U niversita di P isa, giovanni.benelli@ unipi.it on 04 July 2019 mailto:giovanni.benelli@unipi.it?subject= in enclosed environments like a coffin, the remains of insects com- munity can provide many important information about the envi- ronmental, ecological, taphonomical, and sometimes cultural events linked with specific past burial practices. Information in funerary contexts is still poor, despite some efforts in the last decades, leading to the collection of data from excava- tion and exhumations performed in Europe, North Africa and South America (e.g., Panagiotakopulu 2001; Masetti et  al. 2008; Vanin et  al. 2009; Huchet and Greenberg 2010; Panagiotakopulu and Buckland 2012; Huchet et al. 2013a,b; Gaudio et al. 2015; Giordani et al. 2018). In order to improve the knowledge about the entomofauna as- sociated with cadavers from archaeological contexts, herein we analyzed the insects collected from Ferrante II King of Naples and three other Italian Renaissance mummies of the Aragonese dynasty (15th–16th centuries). Mummies had been buried in the Basilica of San Domenico Maggiore in Naples, Italy, and later exhumed and studied by Fornaciari (2006), applying in this archaeological con- text the methodology and techniques used in forensic entomology (Giordani et  al. 2018). The entomofauna collected was analyzed to better understand the funerary practices, attempting to answer the following questions: 1) Did the body concealment in a coffin af- fect the composition of the cadaveric fauna? 2) Did the embalming and mummification process (well-documented for NASD6 and NASD20 (Table 2) influence the composition of the cadaveric fauna? 3)  Did the secondary burial affect the general composition of the cadaveric fauna? Historical and Archaeological Context The Basilica of San Domenico Maggiore (14th century) is one of the largest and most important churches in Naples (Southern Italy). The impressive Sacristy of San Domenico Maggiore (Fig. 1A), located in a suspended gateway close to the vault, hosts 38 wooden sarcophagi containing the bodies of 10 Aragonese princes and princesses and other Neapolitan aristocrats, who died in the 15th–17th centuries (Fig. 1B–D). Most of the individuals had been embalmed and this is cer- tainly not surprising, considering the high social level to which the individuals buried in San Domenico belonged. From the physi- cian Ulisse Aldrovandi, we know that during the Renaissance ‘the Fig. 1. (A) An overview of the sepulchres of members of the royal Aragonese family in St. Domenico Maggiore, Naples. (B) Badly preserved and partially burned artificial mummy of the King of Naples Ferrante II of Aragon (1469–1496, ID: NASD20). (C) Skeletonized artificial mummy most probably of Francis Ferdinand of Avalos, marquis of Vasto and Pescara (1530–1571, ID: NASD6). (D) Disconnected skeleton of the Queen of Naples Joan IV of Aragon (1479–1518, ID: NASD19). 2 Journal of Medical Entomology, 2019, Vol. XX, No. XX D ow nloaded from https://academ ic.oup.com /jm e/advance-article-abstract/doi/10.1093/jm e/tjz102/5528168 by U niversita di P isa, giovanni.benelli@ unipi.it on 04 July 2019 European kings and great personages used to entrust embalming of their bodies to their doctors and surgeons’ (cited in Gannal 1841). The very complex evisceration and embalming method indicates a long-practiced and a diffused embalming tradition. The embalming process by evisceration in the Renaissance had a dual purpose: to preserve the body during the long funerary rituals (which also included prolonged exposure of the body) and to guar- antee maintenance over time of the body of nobles and sovereigns (Giuffra et al. 2016). In Naples, in addition to evisceration and treat- ment with preservative vegetable substances, body preservation was favored by the permanence of the corpses in a dry room, in a tank probably filled with volcanic Vesuvian sand. Similar rooms still exist in the basements of the church of San Domenico Maggiore in Naples. However, some well-preserved individuals show no apparent signs of embalming. In this case, the natural mummification of the bodies can probably be attributed to the very dry microclimatic conditions of the Basilica (Fornaciari 1998). The Sacristy of San Domenico Maggiore collection includes 32 individuals (Fornaciari 2006) but, for a first entomological study, four individuals were sampled (Table 1). One of the examined mummies, badly preserved and partially burned, is the King of Naples Ferrante II of Aragon (1469–1496) (NASD20) (Fig. 1B). Another mummy, almost completely skeletonized is Francis Ferdinand of Avalos, Marquis of Vasto and Pescara (1530–1571) (NASD6) (Fig. 1C). The third one, consisting of a disconnected skeleton, belongs to the Queen of Naples Joan IV of Aragon (1479–1518) (NASD19) (Fig. 1D), whereas the last one is a secondary burial of the trunk with well-preserved bones, belonging to Catherine of Moncada, Duchess of Montalto (deceased in 1659) (NASD31). Material and Methods Entomological samples were manually collected with sterile tweezers and paintbrushes from the remains within the coffins and stored in sterile glass vials at room temperature (15–20°C) to avoid any contamination that would damage or interfere with any further molecular investigations of the mummies and the entomo- logical samples. The entomological samples, observed with a stereoscopic micro- scope S9E (Leica, Germany) typically consisted of a combination of intact insects and insect parts or fragments. The puparium represents the nonmobile stage of the fly life cycle and because of its chemical and physical properties can be collected after centuries or millennia (Vanin and Huchet 2017). To estimate the minimum number of puparia that were highly fragmented, each complete puparium was considered as a single specimen; if fragmented, only the parts with the posterior spiracles, which often represent very reliable diagnostic structures, were counted as specimens (Skidmore 1985, Giordani et al. 2019). Part of the material was mounted on entomological card and photographed to create a pictorial archive useful for the identification of the species (Skidmore 1985, Smith 1986, Peacock 1993, Giordani et al. 2018, Pradelli et al. 2019). Where the species identification was not possible because the remains were incomplete, badly preserved or because of the lack of an identification key for that developmental stage or fragment (e.g., Lepidoptera cocoon and Coleoptera exuviae), identification was done to the taxonomic level of genus or family. Results Eight hundred forty-two insect remains belonging to three orders, Diptera, Coleoptera, and Lepidoptera, were collected from the four Aragonese mummies examined in this study. Notably, 738 (87.6%) specimens were Diptera, followed by 77 (9.1%) Lepidoptera and 27 (3.2%) Coleoptera. Eight hundred fourteen (96.7%) of all the insect remains were collected from the coffin NASD6, 13 (1.5%) from NASD20, 10 (1.2%) from NASD19 and only 5 (0.6%) from NASD31 (Table 2). Three families of Diptera were represented, Muscidae, Fanniidae, and Phoridae, along with two families of Coleoptera, Dermestidae and Ptinidae, and one family of Lepidoptera, Tineidae (Table 1). Diptera Among Diptera, Muscidae was the most collected taxon mainly represented by the species Hydrotaea capensis (Wiedemann) (Diptera: Muscidae). Puparia of this species (Fig. 2A and C) were present in all the examined human remains. Some puparia of H. capensis showed the typical exit holes produced by the emergence of Hymenoptera parasitoids (Fig. 2D and E). Hydrotaea capensis adult heads, wings, legs, and fragments of thorax were also present among the studied material (Fig. 3). Twelve puparia belonging to a species in the genus Fannia Robineau-Desvoidy 1830  (Diptera: Fanniidae), were retrieved in sample NASD6. The immature stages of this genus are morpholog- ically characteristic. Puparia are dorso-ventrally flattened and they show well-developed ramified processes on the lateral and dorsal sides (Fig. 4A and B). One single puparium of Phoridae was present in the sample NASD6. Its shape fits well with the species Conicera tibialis Schmitz (Diptera: Phoridae) (Fig. 4C and D); however, the absence of adults prevents definitive identification to species. Coleoptera Several exuviae of Dermestidae larvae were identified among the studied samples, but they were not identified at the species level despite the presence of short setae that is characteristic/diagnostic of the species in the Anthrenus Geoffroy, or Attagenus Latreille genera  (Coleoptera: Dermestidae) (Fig. 5A). A  single elytron of a spider beetle (Ptinidae) was recovered in the sample NASD20. It is consistently matching with the genus Ptinus Linnaeus (Coleoptera: Ptinidae) (Fig. 5B). Table 1.  Identification of individuals and preservation of the bodies Tomb ID NASD20 NASD19 NASD31 NASD6 Identification Ferrante II (1496) Giovanna IV (1518) Caterina di Moncada (1659) Francesco Ferdinando d’Avalos (1571) Body preservation Artificial mummy Disconnected skeleton Disconnected skeleton Artificial mummy Postmortem damage Fire, grave robbers damage Grave robbers damage Re-deposition in trunk Partial grave robbers damage 3Journal of Medical Entomology, 2019, Vol. XX, No. XX D ow nloaded from https://academ ic.oup.com /jm e/advance-article-abstract/doi/10.1093/jm e/tjz102/5528168 by U niversita di P isa, giovanni.benelli@ unipi.it on 04 July 2019 Lepidoptera Cocoons (Fig. 6A and B) and cephalic capsules of Tineidae (Lepidoptera: Tineidae)  larvae (Fig. 6D and E) were found in all the mummies. No remains of adults were detected, thus genus or species for this taxon remains undetermined. Furthermore, two cocoons showed the typical exit hole of a Hymenoptera parasitoid (Fig. 6C). Unidentified Samples Four insect eggs were recorded from sample NASD20 (Table 2). Discussion To the best of our knowledge, a strictly limited number of earlier studies examined the insect remains characterizing Aragonese tombs. Recently, Benelli et  al. (2014) showed that the black sol- dier fly, Hermetia illucens (Linnaeus) (Diptera: Stratiomyidae), of supposed American origin and acknowledged in Europe only from 1926, was present in Italy several centuries earlier. Indeed, Benelli et  al. (2014) found a larva of this species in the sarcophagus of the Renaissance princess Isabella d’Aragona (1470–1524). Earlier, Fornaciari et  al. (2009) detected a double infestation of the head Fig. 2. Hydrothaea capensis (Diptera: Muscidae): (A) puparia global view, (B) arrows indicate the spiral anterior respiratory horns, (C) posterior spiracula, (D–E) arrows indicate the exit hole produced by the emergence of a parasitoid. Red scale bar: 1 mm; blue scale bar: 500 µm. Table 2.  Abundance of insect remains retrieved from the mummies of Ferrante II d’Aragona, King of Naples (1496), Giovanna IV d’Aragona, Queen of Naples (1519), Caterina di Moncada, Duchess of Montalto (1659), and Ferdinando Francesco d’Avalos, Marquis of Vasto and Pescara (1571) Order, family, and species Abundance of insect remains (no.) Ferrante II d’Aragona (1496) NASD20 Giovanna IV d’Aragona (1518) NASD19 Caterina di Moncada (1659) NASD31 Ferdinando Francesco d’Avalos (1571) NASD6 Total Coleoptera 5 22 27 Dermestidae 4 22 24 Ptinidae, Ptinus sp. 1 1 Diptera 2 4 4 724 738 Fanniidae, Fannia sp. 12 12 Muscidae, Hydrotaea capensis 2 4 4 711 721 Phoridae, Conicera tibialis 1 1 Lepidoptera 2 6 1 68 77 Tineidae 2 6 1 68 77 Not identified Eggs 4 4 Total 13 10 5 814 842 Insect orders are outlined in bold. Within each order, the classification at family or species level was provided. 4 Journal of Medical Entomology, 2019, Vol. XX, No. XX D ow nloaded from https://academ ic.oup.com /jm e/advance-article-abstract/doi/10.1093/jm e/tjz102/5528168 by U niversita di P isa, giovanni.benelli@ unipi.it on 04 July 2019 louse, Pediculus humanus capitis De Geer Anoplura: Pediculidae and the pubic louse, Pthirus pubis (Linnaeus) Anoplura: Pthiridae in the mummy of Ferrante II d’Aragona (1467–1496), King of Naples. This finding stressed that even members of the Renaissance upper classes were afflicted by louse infestations (Fornaciari et al. 2009). However, until now the other Aragonese mummies, buried in San Domenico Maggiore (Naples), remained unexplored. In the present study, a remarkably higher number of insect fragments were found in the mummy NASD6 than in the other three Aragonese individuals. NASD6 was also subjected to inspection in Fig. 3. Diptera Muscidae Hydrothaea capensis. (A) Head fragmented, frontal view, (B) thorax; arrow indicates the posterior side with scutellum. Red scale bar: 1 mm. Fig. 4. (A) Diptera Fanniidae puparia global view, (B) detail, (C) Conicera tibialis (Diptera Phoridae) puparia global view, (D) detail. Red scale bar: 1 mm; blue scale bar: 500 µm. Fig. 5. (A) Larval exuviae of Coleoptera Dermestidae, (B) elytron of Ptinus sp. (Coleoptera Ptinidae). Red scale bar: 1 mm. 5Journal of Medical Entomology, 2019, Vol. XX, No. XX D ow nloaded from https://academ ic.oup.com /jm e/advance-article-abstract/doi/10.1093/jm e/tjz102/5528168 by U niversita di P isa, giovanni.benelli@ unipi.it on 04 July 2019 1894 (Amante 1896) and it is the better-preserved deposition, with the skeleton still in partial anatomical connection. In contrast, the other three individuals consist of a mummy strongly damaged by the disas- trous 1506 fire (Volpicella 1847) with disconnected limbs (NASD20) and in two disconnected skeletons (NASD19 and NASD31). The better preservation of mummy NASD6 compared to the other individuals can explain the abundance of the sampled insects. All the insects found in our sampling belonged to species typical of a late cadaver colonization, with a lack of species characterizing the first colonization waves of exposed bodies (e.g., species belonging to the genera Calliphora Robineau-Desvoidy, Lucilia Robineau- Desvoidy (Calliphoridae), Musca Linnaeus, Muscina Robineau- Desvoidy (Muscidae), and Sarcophaga Meigen (Sarcophagidae)). High numbers of H.  capensis puparia, the most represented taxon, have been reported from human remains of historic and ar- chaeological interest (for a review see Giordani et  al. 2018). This species usually colonizes corpses in later succession waves during the ammonia fermentation. However, in concealed conditions, where no arrival of blowflies is possible, H.  capensis is often the domi- nant Diptera species (see also Pradelli et  al. 2019). This supports the hypothesis that corpses have been kept indoors for a long time under protected, confined environmental conditions, without expo- sure to open air (Couri et al. 2009). However, other explanations for NASD20 and NASD6 could be outlined, including an embalming process using odorous oils/balms that could have delayed or stopped the arrival of the first colonizer flies, followed by sealing the coffin with bitumen. On the other hand, the presence of specimens in the genera Fannia and Hydrotaea likely excludes the hypothesis of a preliminary dehydration of the body using volcanic sand, which quickly dries the treated bodies, strongly reducing the suitability of the environmental conditions for the colonization of these species. Overall, this scenario corresponds to a historical context with a well- advanced knowledge about body preparation where specific burial techniques existed and were adopted for the wealthy and aristocrats (Marinozzi and Fornaciari 2005). The large abundance of Diptera puparia fragments is not sur- prising, because puparia represent the most resistant structural element of all the Diptera developmental stages. The puparia for- mation process is characterized by the sclerotization of the mature maggot cuticle rich in chitin, whose chemical structure can survive Fig. 6. Lepidoptera Tineidae. (A) cocoon, (B) parasitized cocoon, arrows indicated the parasitoid exit hole, (C) cocoon detail, arrows indicate red tissue fibers, (D) cephalic capsule ventral view, and (E) dorsal view. Red scale bar: 1 mm; blue scale bar: 500 µm. 6 Journal of Medical Entomology, 2019, Vol. XX, No. XX D ow nloaded from https://academ ic.oup.com /jm e/advance-article-abstract/doi/10.1093/jm e/tjz102/5528168 by U niversita di P isa, giovanni.benelli@ unipi.it on 04 July 2019 for centuries to millennia (Vanin and Huchet 2017). Only a few, very damaged adult fragments of H.  capensis, were found, which may be explained by their fragility (Panagiotakopulu 2004). The scarcity of adult fly fragments suggests that most of them could have had the possibility to fly away from the coffin or that their body could have been consumed by successive populations of the polyphagous insects, such as Dermestidae beetles. Such a situation is consistent with a possible later exhumation of the bodies that could have been exposed for a quite long period, e.g., after the visits of grave robbers. Phoridae are small-size Diptera, well known in the forensic con- text for their ability to enter coffins or to reach deeply buried bodies (Manlove and Disney 2008). Their scarcity could suggest the coffins were well-sealed. However, in our case, the single partial puparium of C. tibialis was found in the sample NASD6, together with the high number of H. capensis remains, suggest that insects had easy access to this corpse. Furthermore, Fanniidae species usually are typical of a later colonization. In relatively advanced decomposed cadavers, the degeneration of the tissues to a liquid state, produces a wet en- vironment on the bottom of the coffin, which is highly attractive for the species of this family, also known as ‘latrine-flies’ (Nuorteva et al. 1974, Smith 1986, Lee and Marzuki 1993). The finding of Fannia specimens in these contexts and, at the same time, the absence of bowflies remains, is consistent with the hypothesis of easier, later access by insects to the NASD6 corpse. For instance, if some slots appeared later in the coffin, due to structural adjustments, under the pressure of the gas produced by the decaying corpse. Both Dermestidae and Ptinidae beetles are later colonizers of corpses, feeding on dried substrates and showing polyphagous habits, by consuming skin, hairs as well as clothes fibers and even other chitinized body parts. The discovery of a limited number of larval exuviae of Dermestidae and no adult remains, which repre- sent the most resistant body parts, indicates that adult specimens had the possibility to leave the corpses quite easily through a well accessible opening. Like Dermestidae beetles, Tineidae moths are associated with the last phases of the body decomposition. They feed on dry tissues, hairs, and textiles fibers, which are visible in the texture of the cocoons structure (Fig. 6B). We detected only cephalic head capsules of larvae and cocoons, without any traces of adult remains, supporting the hypotheses, already formulated for Dermestidae, that adults had the possibility to move out from the coffin after their emergence. Besides, the remarkable presence of moth remains could be associated with the abundance of textiles from the clothes used for the funerary cer- emony of these people of high social status (D’Arbitrio 2001). The finding of H.  capensis puparia and Tineidae cocoons parasitized by Hymenopteran wasps highlights the ability of these parasitoids to reach concealed hosts and could also substantiate the hypothesis that the coffin NASD6, sometime after burial, was partially or entirely exposed to the open environment for a period, allowing a late insect colonization, including parasitoids that attack larvae and pupae of their hosts. Conclusions The examination of more than 800 insect specimens from four mummies belonging to these members of the Aragonese family con- firm the historical information about the burial of people belonging to the Renaissance noblesse. In addition, the findings reported in this article underline how the concealment of the body plays a fun- damental role in the selection of the entomofauna associated with body colonization. Our records, in agreement with previous work, highlight out the role of H. capensis in the colonization and organic material recycling in body located in confined conditions, in contrast to what happens with exposed bodies, where blowflies are the most important taxon in body colonization. To attempt a reply to the three questions formulated in the in- troduction, it can be concluded that: 1) body concealment in coffins significantly affected the composition of the cadaveric fauna; 2)  Furthermore, our results demonstrate that embalming and the mummification process can influence the composition of the cadav- eric fauna as previously shown in other studies (Gilbert and Bass 1967, Huchet 2010, Huchet and Greenberg 2010, Nystrom et  al. 2005). 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