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INTRODUCTION

As a group, insects constitute the most successful living organisms in the history of the planet. Insects represent more than 50% of all the eukaryotic species estimated to exist in the world (Grimaldi and Engel, 2005), they live in all land masses of the planet and perform a myriad of ecological functions. Forensic entomology studies the role of insects, and other arthropods, in legal issues (Hall and Huntington, 2010), and thus seeks to apply a vast amount of scientific knowledge about insects, their distribution and their development to solve crime. Ultimately, forensic entomology aids legal and justice systems and provides relief to families and societies.

Ants are an important and ubiquitous component of the insect fauna on all terrestrial habitats, except the poles, with about 140 million years of evolutionary history (Moreau and Bell, 2013). There are currently more than 13,000 ant species recognized worldwide

(Bolton, 2014). They play crucial ecological roles as predators, soil engineers, seed dispersers, plant symbionts, nutrient cyclers and more (Del Toro et al., 2012). In tropical forests ants represent, together with termites, a major proportion (i.e. 30%) of the animal biomass (Fittkau and Klinge, 1973). At the ground level they can reach densities of up to 23 nests per square meter (Kaspari, 1996a).

Most ants are beneficial to human beings. Some species are used as food (DeFoliart, 1999), others produce compounds with pharmaceutical and biomedical applications (Reddy et al., 2011; Brown et al., 2004), they are important in many cultures around the world, and they provide ecological services as seed dispersers, pollinators and biological control agents (Lengyel et al., 2010; Van Mele, 2008; Philpott and Armbrecht, 2006). Some species, however, are detrimental for humans when they establish nearby human settlings. Fire ants, for example, frequently colonize electrical equipment, attack livestock, cause infrastructure

THE ROLE OF ANTS (HYMENOPTERA: FORMICIDAE)IN FORENSIC ENTOMOLOGY

Giovanni Ramón1, David A Donoso2

Instituto Nacional de Investigación en Salud Pública, Iquique N14-285 y Yaguachi, Quito, Ecuador.1

Museo de Colecciones Biológicas MUTPL, Departamento de Ciencias Naturales,Universidad Técnica Particular de Loja; Loja, Ecuador.2

gramonc@gmail.com

ABSTRACT

Ants (Hymenoptera: Formicidae) are an important component of insect biodiversity, and their study may help forensic entomologists to solve criminal cases. We review published literature and ecological principles that may guide forensic entomologists in the usage of ants as evidence with forensic value. Because ants are top predators in litter environments, their activities can affect decomposition processes and influence on the estimation of the post-mortem interval. We also revise artifacts caused by ants on decomposing bodies (e.g. biting, stinging and modification of blood patterns).

KEYWORDS: BIODIVERSITY, biting, post-mortem interval, stinging

RESUMEN

Las hormigas (Hymenoptera: Formicidae) son un componente importante de la biodiversidad de insectos y su estudio puede ayudar a los entomólogos forenses a resolver casos criminales. Nosotros revisamos la literatura y principios ecológicos que pueden guiar a los entomólogos forenses a usar hormigas como evidencia con valor forense. Las hormigas son depredadores en la hojarasca, por lo tanto sus actividades pueden afectar los procesos de descomposición e influenciar la estimación del intervalo post mortem. También, nosotros revisamos los artefactos causados por hormigas en cuerpos en descomposición (p.ej. mordeduras, picaduras y modificación de los patrones en manchas de sangre).

PALABRAS CLAVES: BIODIVERSIDAD, intervalo post mortem, mordeduras, picaduras.

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damage in roads and buildings, and with their painful stings are a nuisance for human activities (Ascunce et al., 2011). Of special concern are ants that invade hospitals, as they represent a nuisance for patients and staff and are capable of mechanically transporting bacteria (Rodovalho et al., 2007; Moreira et al., 2005).

One overlooked utility of ants is their use on forensic investigations. Traditionally, ants have been considered minor actors on forensic studies, well after flies and beetles (Byrd and Castner, 2010). Ants, however, are important in forensic studies in several ways. Here, we search in the literature for the role of ants on forensic entomology, specifically on medicocriminal entomology. First, we review decomposition processes and how ants modify them. We found that ant activities over corpses can influence the estimation of the post-mortem interval (PMI). Second, we explore the role of ants as causing agents of human injuries and death. Third, we list the artifacts ants may cause over corpses. Several of these artifacts can confuse forensic specialists and lead them to erroneous conclusions. Fourth, we review cases where ants can help determine the place of death. Across the paper, we offer our personal observations and suggestions on the ways forward and recognize the underappreciated role of this fascinating group of insects in forensic science.

Ants and decomposition processesAt macroscale, decomposition of organic material can be explained as a function of temperature and precipitation (Chapin et al., 2011). However, at local scale differences in decomposition of organic matter are due to substrate quality (e.g. soil), material quality (e.g. plant material decomposes much faster than animal material), and the decomposer community (e.g. bacteria, fungi, and the microorganism of the litter layer) (Chapin et al., 2011). The role of litter predators (such as ants) on the decomposition of plant material has been little studied. Generally, ants play an important role as predators of other arthropods in the leaf litter layer (Wilson, 2005; Kaspari 1996b), and so it has been shown that they may limit the decomposition rates by predating on them and also by altering the composition of the microbial community (Del Toro et al., 2012; Wardle et al., 2011).

The importance of ants on the decomposing process of animal and human carcasses has received less attention. It is commonly recognized that ants are attracted to arthropods that colonize corpses, not the corpses themselves (Campobasso et al., 2009).

This hypothesis is mostly based in observations from temperate regions where ants dwelling in the corpses are attracted to fly eggs, larvae and pupae, but not the flesh itself (Campobasso et al., 2009; Barros et al., 2008). With some exceptions (Valdes-Perezgasga et al., 2010), in tropical ecosystems most reports only mention ants as casual visitors to corpses that feed on arthropods and provide little or none information of forensic relevance at all (e.g. Bermúdez and Pachar, 2010).

Ants (Cephalotes atratus Linnaeus 1758, Crematogaster sp.) however, were found to cut and carry skin and muscle tissue of an experimental fresh pig carcass located in Yasuní National Park in Orellana Province, Ecuador, (Fig. 1) (Emilia Moreno, pers. comm.). This behavior have been observed elsewhere (e.g. Prado e Castro et al., 2014; and references therein) Moreover, among the Ecuadorian Cofan ethnicity (and possibly widespread in the Amazon basin) ants of the genus Dolichoderus are usually used to clean animal bones from their flesh (David Donoso, pers. obs.). Regardless, ant activity can potentially decrease (flesh removal) or increase (fly egg, larvae and pupae removal) the estimation of the post-mortem interval (Early and Goff, 1986)

Interactions of ants with other arthropods around decomposing bodiesWhile they are capable of scavenging on the flesh, the role of ants as predators over other arthropods (and their eggs and larvae) has the most substantial impact on forensic studies. In some instances the predation rate of ants on flies, beetles and their eggs might be so important that it can delay the onset of initial colonization up to 3 days (Byrd and Castner, 2010). Barros et al. (2008) recorded Pheidole and Camponotus ants (two widely distributed genera in Ecuador and elsewhere) removing fly eggs, larvae and pupae from pig carcasses. In Ecuador (Union del Toachi, Pichincha), it has also been observed, repeatedly, that army ants (Formicidae: Dorylinae) raid on decomposing pigs, removing both cadaveric pig remains and fly larvae (Emilia Moreno, pers. comm.).

In some instances, ants are even capable of establishing their colony on decomposing bodies. As social insects, ant colonies as a whole pass through developmental stages in which the number and proportion of castes vary and generally, after a colony has reached a certain size, it begins to produce sexual castes (Peeters and Molet, 2010). When the development time of a given ant species is known it is be possible to estimate PMI based on the time needed to establish a colony or produce

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The role of ants (Hymenoptera: Formicidae) in forensic entomologyGiovanni Ramón1, David A Donoso2

certain castes. This was the case of some human remains discovered inside a tool box; based on the presence of an Anoplolepis gracilipes colony, the PMI was estimated to be 14 to 18 months (Goff and Win, 1997).

Ants as assassins: frequency of injuriesand fatalities caused by ants The continuing expansion in the range of invasive species, especially fire ants (Solenopsis spp.) (Morrison et al., 2005; Rodriguez-Acosta and Reyes-Lugo, 2002; Vinson, 1997), which can inflict painful stings (More et al., 2008; Prahlow and Barnard, 1998), aggravates the problem. At the highly ant-diverse Neotropical region with many potentially “dangerous” species of Ponerinae and Dorylinae ant subfamilies whose stings can produce all the range from mild reactions to severe allergic reactions and even death, the increase in encounters between people and stinging ants could represent a serious public health concern.

As many other species in the order Hymenoptera like wasps, bumblebees, velvet ants and hornets, ants possess a sting formed by the modified terminal abdominal segments. With it, ants are capable of injecting venom typically produced in the attached poison glands (Hölldobler and Wilson, 1990). While some ants use the stinging apparatus to send chemical messages to nestmates or to produce trail pheromones (Hölldobler and Wilson, 1990), most of them use it to hunt for prey or as a defense mechanism. It is the latter in which we will focus the discussion of this section.

While humans are not a suitable prey for ants they still can become victims of ant stings when they come cross their paths. Although in most tropical and subtropical countries, ant stings are only a minor concern (McGain and Winkel, 2002), in some, encounters with ants are becoming more common (Kemp et al., 2000; deShazo et al., 1984). As noted by Rodriguez-Acosta and Reyes-Lugo (2002), the reaction from ant stings can range from moderate to extensive local allergic reactions, systemic hypersensitivity, anaphylactic shock and, in extreme cases, even death (Hardwick et al., 1992). In the United States alone, 44 fatalities from fire ant (Solenopsis invicta and Solenopsis richteri) stings have been reported in the last 50 years (Bury et al., 2012). Most fatalities however are attributed to anaphylaxis rather than to the direct effect of the venom (Bury et al., 2012).

Artifacts caused by ants on decomposing bodies:biting, stinging, burying and modification ofblood patterns Ant stings are painful. Some ants, especially poneroids (from the Greek word ponera, for pain), which have primitive characteristics, can inflict some of the most painful insect stings. In the Neotropical region, for example, the bullet ant Paraponera clavata sting has been categorized as “traumatically painful” (Starr, 1985). Similarly, in Australia Myrmecia spp. ants are also respected for their painful stings. It is thought that painful stings evolved as a mechanism to deter vertebrate aggressors (Schmidt, 1990). This stinging behavior can potentially inflict marks in the decomposing body that can provide valuable evidence for the investigation.

Another case of ant sting with forensic value is the fire ants (S.invicta, S. richteri and S. geminata). Introduced in the 20th century from South America to the United States, fire ants have been expanding their range at fast pace. Today they are reported throughout most US southern states (Ascunce et al., 2011) and also in Australia, New Zealand, Taiwan, Hong Kong, Macao, and China (Wetterer, 2011). It has been estimated that between 30 and 60% of people living in infested areas are stung every year; from these in the US it has been reported that 0.6 to 16% presented anaphylactic reactions (Caldwell et al., 1999; Adams and Lofgren, 1981). Fire ants get their names from the painful stings they are capable of inflicting. Scientific and medical literature is full of reports of fire ant stings and their consequences.

Biting can also exert significant damage to corpses. Barros et al. (2008) recorded the presence of Pheidole and Camponotus ants inflicting significant damage to the nose and ears of pig carcasses (e.g. taphonomic marks). Similarly, in a study on the decomposition of rat corpses in Brazil, small injuries made by ants were detected at every decomposition stage and over different parts of the body (Moura et al., 1997). These bites can be confounded with pre-mortem caused injuries. A throughout review of the main artifacts caused by ants on decomposing bodies can be found in Campobasso et al. (2009). Without careful consideration of these ant-inflicted marks, they can misguide investigators about the cause of death.

Another way in which ants can influence the decomposition process is by burying the body, or parts of the body. Fire ants are also a good example as they have been found capable of this. In Texas for example, a wound on the abdominal area of a partially buried human body was found filled with soil by S. invicta, preventing other insects

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from reaching it. Only nine days later were other insects capable of colonizing the corpse to continue the usual decomposition process; as noted by the authors, the estimation of the PMI based only in the fly activity would have been dramatically skewed (Lindgren et al., 2011). Similarly, in a study by Moura et al. (1997) in Brazil, the head and anal area of decomposing rats were found buried by ants, preventing the access by flies.

Ants can make difficult the interpretation of events on a crime scene by altering the bloodstain patterns or by moving blood to new locations. Investigators use the size and shape of the bloodstains to try to understand what happened at the crime scene. Some insects like flies, however, by walking over a corpse or by feeding on blood can alter the blood pattern. Moreover, some of the patterns they leave can be confused with those left by a specific gun or event. Although the possibility exists, we are not aware of any specific report.

Determination of place of deathInsect species found inside a decomposing body that do not correspond to the insect fauna normally found at the area can indicate that a body has been moved from a different place, and given the case that the geographic distribution of the insect is known, it can even signal the site from which the body was relocated (Catts and Goff, 1992). In their study, Chen et al. (2014) found that the distribution of ants was irregular, so the ants found in monkey remains were useful in determining the place of death.

In the Neotropics, composition of ant communities of various sites has been well documented. For instance, in Ecuador, the ant community composition of a pre-montane forest (Ramón et al., 2013; Donoso and Ramón, 2009), of an Amazonian forest (Mertl et al., 2010; Ryder Wilkie et al., 2010; 2009; 2007) and of mountain forests in the southern provinces (Delsinne et al., 2013; 2012; Jacquemin et al., 2012) have been well documented in the last years. This knowledge could aid forensic investigators to resolve criminal cases if, for example, ants are found in a corpse that has been moved to determine the site of origin. Forensic investigations would benefit from more studies of local ant communities in natural and urban environments, and of their seasonal changes in composition, in Ecuador in particular and in the Neotropical region in general.

CONCLUSIONS

Our main conclusion after reviewing the literature and from our field experience, is that ants cannot be overlooked anymore as merely casual or secondary visitors at crime scenes. We have seen that ants can cause errors in the estimation of the PMI in three ways: by acting as predators of other arthropods that feed on carrion, by altering the composition of the microbial community and by directly removing chunks of the corpse. The latter one has been overlooked in the Neotropical region and needs to be researched more deeply in the future.

While traditionally flies and beetles have been used to establish the PMI, we found that ants that establish their colonies within decomposing bodies can also be used for that purpose. By determining the number of individuals on each caste, or by observing the production of sexual individuals, a fairly precise estimate of the PMI can be obtained with a previous knowledge of the species life cycle. In this regard, forensic entomology would benefit from the study of the life cycle of the most common local species at each country.

While the stings of most species are capable of causing an acute pain at the most, some people can present allergic reactions that can even cause death. In view of the increasing expansion of cities towards rural areas and with the increase in the geographical range of invasive species like fire ants, encounters between ants and humans are expected to become more frequent. This could start to become a health problem that needs to be researched in order to reduce its impact.

When ants are found on a crime scene, or a body is found in a place where ants are abundant, evidence should be interpreted with care. By biting, stinging, burying the body or by altering the blood stain patterns; ants can lead forensic investigators not only to make mistakes on the estimation of the PMI but also can be misguided when looking for the possible cause of death.

Finally, when ants are found within a body that has been moved, their identifications may help investigators to determine the original place where the body was located after identifying the ants found to species level. This, however, requires a previous knowledge not only of the ecology but also of the biogeography of ant communities.

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The role of ants (Hymenoptera: Formicidae) in forensic entomologyGiovanni Ramón1, David A Donoso2

With the ongoing interest from forensic investigators and related institutions in Central and South America in the last years (e.g. Pujol-Luz et al., 2008; Arnaldos 2006; Centeno, 2000), there are now more opportunities to increase the knowledge on the insects of forensic importance and the role they play in the decomposition process. As previously mentioned, ants are important actors of the decomposition process and forensic science in the Neoptropical region would greatly benefit from more studies on their biology.

ACKNOWLEDGMENTS

This work was financed, in part, by UTPL Grant # PROY_CCNN_0022 to DAD. The authors would like to than Álvaro Barragán and Emilia Moreno for inviting us to write this manuscript. The authors thank Thibaut Delsinne and Aura Paucar for the valuable comments to earlier drafts of the manuscript. DAD thanks UTPL and Aventura Lojana for the constant support. We further thank the FGE of Ecuador for the support given to the development of forensic sciences in Ecuador.

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FIGURE 1. A) Cephalotes atratus workers tearing apart the skin on the leg of a dead pig (bloating stage) at Yasuní National Park, Ecuador, B) detail of a C. atratus worker biting out the flesh of the dead pig and C) some Crematogaster sp. workers tearing apart the skin of the dead pig. Photos courtesy of Ricardo Jaramillo.